Horticultural Reviews (Volume 30)

HORTICULTURAL REVIEWS Volume 30

Horticultural Reviews is sponsored by: American Society for Horticultural Science

Editorial Board, Volume 30 Martine Dorais Wilhelmina Kalt Raphael Goren

HORTICULTURAL REVIEWS Volume 30

edited by

Jules Janick Purdue University

John Wiley & Sons, Inc.

This book is printed on acid-free paper. Copyright © 2004 by John Wiley & Sons. All rights reserved. Published by John Wiley & Sons, Inc., Hoboken, New Jersey Published simultaneously in Canada No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, (978) 750-8400, fax (978) 750-4470, or on the web at www.copyright.com. Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, (201) 748-6011, fax (201) 748-6008, e-mail: [email protected]. Limit of Liability/Disclaimer of Warranty: While the publisher and author have used their best efforts in preparing this book, they make no representations or warranties with respect to the accuracy or completeness of the contents of this book and specifically disclaim any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives or written sales materials. The advice and strategies contained herein may not be suitable for your situation. You should consult with a professional where appropriate. Neither the publisher nor author shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. For general information on our other products and services or for technical support, please contact our Customer Care Department within the United States at (800) 762-2974, outside the United States at (317) 572-3993 or fax (317) 572-4002.

Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. For more information about Wiley products, visit our web site at www.wiley.com. Library of Congress Cataloging-in-Publication Data: ISBN: 0-471-35420-1 ISSN: 0163-7851 Printed in the United States of America 10

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Contents Contributors Dedication: Dale E. Kester

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Thomas M. Gradziel

1. Girdling: Physiological and Horticultural Aspects

1

R. Goren, M. Huberman, and E. E. Goldschmidt I. II. III. IV. V. VI.

Introduction Girdling Concepts and Techniques Girdling and Physiological Studies Endogenous Plant Hormones Girdling in Horticultural Practice Concluding Remarks Literature Cited

2. Irrigation Water Quality and Salinity Effects in Citrus Trees

2 7 12 16 19 25 26

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Yoseph Levy and Jim Syvertsen I. II. III. IV. V. VI. VII.

Introduction Managing Salinity Experimental Methods in Salinity Research Physiological Responses Salinity and Biotic Stresses Benefits of Moderate Salinity Summary Literature Cited

38 39 49 55 68 70 72 72

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CONTENTS

3. Red Bayberry: Botany and Horticulture

83

Kunsong Chen, Changjie Xu, Bo Zhang, and Ian Ferguson I. II. III. IV. V. VI.

Introduction Botany Physiology Environmental Requirements Horticulture Concluding Remarks Literature Cited

4. Protected Cultivation of Horticultural Crops in China

84 87 96 99 101 110 111

115

Weijie Jiang, Dongyu Qu, Ding Mu, and Lirong Wang I. II. III. IV. V. VI.

Introduction The Energy-Saving Greenhouse Vegetable Crops Floriculture Fruit Trees Future Development of Protected Horticulture Literature Cited

5. Greenhouse Tomato Fruit Cuticle Cracking

116 121 126 141 149 158 159

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Martine Dorais, Dominique-André Demers, Athanasios P. Papadopoulos, and Wim Van Ieperen I. II. III. IV. V. VI.

Introduction Fruit Characteristics Related to the Development of Cuticle Cracking Genetic Aspects of Fruit Resistance to Cuticle Cracking Climatic Factors Related to the Development of Cuticle Cracking Cultural Factors Related to the Development of Cuticle Cracking Conclusion Literature Cited

164 166 170 171 174 178 179

CONTENTS

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6. Fresh-Cut Vegetables and Fruits

185

Jeffrey K. Brecht, Mikal E. Saltveit, Stephen T. Talcott, Keith R. Schneider, Kelly Felkey, and Jerry A. Bartz I. II. III. IV. V. VI. VII.

Introduction Physiology Sensory Quality Phytonutrients Microbiology Treatments to Maintain Quality Conclusions Literature Cited

186 190 203 209 217 224 230 231

7. Postharvest Physiology and Storage of Widely Used Root and Tuber Crops

253

Uzi Afek and Stanley J. Kays I. II. III. IV. V.

Introduction Causes of Postharvest Losses Tuber Crops Root Crops Corm and Rhizome Crops Literature Cited

8. Metabolic Control of Low-Temperature Sweetening in Potato Tubers During Postharvest Storage

255 255 259 276 295 299

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R. W. Blenkinsop, R. Y. Yada, and A. G. Marangoni I. II. III. IV. V. VI. VII. VIII.

Introduction Starch Metabolism Sucrose Metabolism Glycolysis Oxidative Pentose Phosphate Pathway Mitochondrial Respiration Metabolic Factors Affecting Chip Color Development Conclusion Literature Cited

318 321 325 335 339 340 342 345 346

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CONTENTS

9. Cassava-based Multiple Cropping Systems

355

V. Ravi and C. R. Mohankumar I. II. III. IV. V. VI. VII.

Introduction Growth and Productivity of Cassava Growth and Productivity of Associate Crops Intercropping Cassava Relay Sequential Cropping Cassava Multi-Cropping Management Conclusion and Future Prospects Literature Cited

356 361 374 394 417 420 460 463

Subject Index

501

Cumulative Subject Index

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Cumulative Contributor Index

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Contributors Uzi Afek, Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, Gilat-Agricultural Research Center, Mobile Post Negev 85280, Israel, [email protected] Jerry A. Bartz, Plant Pathology Department, University of Florida, Gainesville, FL 32611-0680 R. W. Blenkinsop, Department of Food Science, University of Guelph, Guelph, ON, Canada, N1G 2W1, [email protected] Jeffery K. Brecht, Horticultural Sciences Department, University of Florida, Gainesville, FL 32611-0690, [email protected] Kunsong Chen, Department of Horticulture, Huajiachi Campus, Zhenjiang University, Hangzhou, 310029, P. R. China Dominique-André Demers, Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre, Harrow, ON, Canada, N0R 1G0 Martine Dorais, Agriculture and Agri-Food Canada, Centre de Recherche en Horticulture, Université Laval, Ste-Foy, QC, Canada, G1K 7P4, [email protected] Kelly Felkey, Food Science and Human Nutrition Department, University of Florida, Gainesville, FL 32611-0370 Ian B. Ferguson, The Horticulture and Food Research Institute of New Zealand, Private Bag 92 169, Auckland, New Zealand, Iferguson@ hortresearch.co.nz E. E. Goldschmidt, Kennedy-Leigh Centre for Horticultural Research, The Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel Raffi Goren, Kennedy-Leigh Centre for Horticultural Research, The Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel, rgoren@ agri.huji.ac.il Thomas M. Gradziel, Department of Pomology, University of California, Davis, CA 95616-8683, [email protected]

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CONTRIBUTORS

M. Huberman, Kennedy-Leigh Centre for Horticultural Research, The Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel Weijie Jiang, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun S. Street, Beijing, 100081, China, [email protected] Stanley J. Kays, Department of Horticulture, The University of Georgia, Athens, GA, 30602-7273, [email protected] Yoseph Levy, Agricultural Research Organization, Department of Fruit Tree Sciences, Gilat Research Center, Mobile Post Negev, 85-280, Israel, [email protected] A. G. Marangoni, Department of Food Science, University of Guelph, Guelph, ON, Canada, N1G 2W1, [email protected] C. R. Mohankumar, Central Tuber Crops Research Institute, Sreekariyam, Trivandrum, India, 695 017 Ding Mu, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun S. Street, Beijing, 100081, China Athanasios P. Papadopoulos, Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre, Harrow, ON, Canada, N0R 1G0 Dongyu Qu, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun S. Street, Beijing, 100081, China V. Ravi, Central Tuber Crops Research Institute, Sreekariyam, Trivandrum, India, 695 017, [email protected] Mikal E. Saltveit, Department of Vegetable Crops, University of California, Davis, CA, 95616-8631 Keith R. Schneider, Food Science and Human Nutrition Department, University of Florida, Gainesville, FL 32611-0370 Jim P. Syvertsen, University of Florida, IFAS, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, FL, 338502299, [email protected] Stephen T. Talcott, Food Science and Human Nutrition Department, University of Florida, Gainesville, FL 32611-0370 Wim Van Ieperen, Horticultural Production Chains Group, University of Wageningen, Marijkeweg 22, 6709 PG, The Netherlands Lirong Wang, Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, Henan Province 450009, China

CONTRIBUTORS

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Changjie Xu, Department of Horticulture, Huajiachi Campus, Zhenjiang University, Hangzhou, 310029, P. R. China R. Y. Yada, Department of Food Science, University of Guelph, Guelph, ON, Canada, N1G 2W1 Bo Zhang, Department of Horticulture, Huajiachi Campus, Zhenjiang University, Hangzhou, 310029, P. R. China

Dale E. Kester

Dedication: Dale E. Kester

Volume 30 of Horticulture Reviews is dedicated to the productive career of Dale Emmert Kester, who has been a leader in pomological research and horticultural education at the University of California at Davis. Dale was born July 28, 1922, the third in a family of seven, and grew up on a self-supporting Iowa farm producing corn, small grain, alfalfa, pasture, vegetable gardens, and fruit orchards (apple, mulberry, black walnuts, sour cherry, plums, and seedling peaches). He still retains vivid memories of cultivating corn behind a team of horses, haying, shocking grain, picking corn by hand, and milking cows each morning and evening. Dr. Kester’s education included grade school at a rural school that included a daily walk of one mile between home and the school house and later, at high school in Audubon, Iowa. Early on, Dale developed a passion for birds, perhaps nurtured by the fact that the county in which he grew up, Audubon County, was an oasis for bird life of all kinds. His parents were conservative politically but very progressive in farming practices. They pioneered soil conservation practices and the use of improved seeds such as hybrid corn. They were also strong supporters of 4-H and Future Farmer programs, as well as Farm Bureau and Iowa State College sponsored programs. After High School, Dale spent a year as a farm worker both at a neighboring farm and at his parents’ farm. Then, with the help of a Sears and Roebuck scholarship, he entered Iowa State College in the Fall of 1941, majoring in Horticulture. He supported himself by working in the greenhouses of the Department of Horticulture at Ames, by waiting tables in the girls’ dormitory, and by summer work in the pea canneries in DeKalb, Illinois. During World War II, he joined the Air Force Reserve and was called into service in February 1943. He flew 28 missions, flying P-40s and P-51s, escorting bombers from Italy to Central Europe. Immediately after the war he returned to Iowa State to complete his degree. In July 1946, Dale married Daphne Dougherty, whom he met in Baton Rouge, Louisiana, during his Air Force training. They have two children, William Kester and Nancy Kester Baysinger, and three grandsons.

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DEDICATION: DALE E. KESTER

In December 1947, the Kesters moved to Davis, California, where he entered graduate school as a Masters Candidate in Pomology. Dr. Kester’s work consisted, in part, of collecting fruit samples of peaches, plums, and apricots for Dr. Claron Hesse, the newly hired plant breeder in the Department. His Ph.D. thesis examined the requirements of in-vitro peach embryo development following cotyledon removal. He was awarded a Ph.D. in Plant Physiology in June, 1951. At that time, Dale was hired by the Department of Pomology, UC Davis, as an Instructor in Pomology and a Junior Pomologist in the Experiment Station. Subsequently, he advanced to the rank of Assistant Professor, Associate Professor, and Professor in the College of Agriculture, with corresponding titles in the Experiment Station of Assistant Pomologist, Associate Pomologist, and Pomologist. Dale retired as emeritus Professor in 1991. Dr. Kester’s professional interests can be divided into three principal areas: the genetics and physiology of almond, the identification and characterization of clone degeneration with vegetative propagation, and teaching. The immediate requirement of the Pomology Departmental position was to take control of a long-term (1923–1948) almond breeding project that had existed previously as a cooperative project with the USDA. The University/USDA programs were separated in 1948, after two cultivars, ‘Jordanolo’ and ‘Harpareil’, were released in 1938. Although initially commercially successful, within five years the two cultivars both developed symptoms of a genetic disorder subsequently identified as noninfectious bud-failure. The prevalence of this disorder was so pronounced and widespread that commercial production of both cultivars was quickly abandoned. A further responsibility of the almond breeding project was to complete the evaluation of advanced selections and of the several thousands of almond seedlings from controlled crosses. ‘Davey’ was jointly released in 1953 from this project. A second program to develop a smaller-sized version of the major almond cultivar ‘Nonpareil’ led to the release of ‘Kapereil’ (1963) and ‘Milow’ (1975). While all three cultivars met the requirements for which they were selected, none became widely planted. This early experience convinced Dr. Kester that successful cultivar breeding depended upon a comprehensive understanding of the entire range of biological, cultural, and marketing characteristics of almond. His subsequent efforts to achieve this breadth of understanding has led to his recognition today as a world authority on almond genetics, culture, and improvement. Dr. Kester’s rootstock evaluation and selection programs also included studies on almond/Marianna plum incompatibility and the develop-

DEDICATION: DALE E. KESTER

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ment of peach × almond hybrids rootstocks. Three hybrid clones, ‘Hansen 2168’, ‘Hansen 536’, and ‘Nickels’ have been released, with the last two attaining important commercial use. In collaboration with statewide county extension personnel, a comprehensive system of cultivar evaluations in Regional Variety Trial plots was established throughout California. These have facilitated the more recent testing and introduction of new almond cultivars, including ‘Solano’, ‘Sonora’, ‘Padre’, and ‘Winters’. The identification of pollen incompatibility alleles was also carried out in a series of controlled hand-pollination studies replicated over a period of many years. The majority of established almond cultivars were shown to belong to a single family arising from natural crossings between the two principal founding cultivars: ‘Nonpareil’ and ‘Mission’ (syn. ‘Texas Prolific’). These studies, in turn, have served as the basis for subsequent molecular characterization of the pollen self-incompatibility factor in almond, making this species an important model for pollination studies in the Rosaceae. Transfer of self-fertility to almond from peach, Prunus mira, and later Prunus webbii was accomplished in related research. The extensive gene introgression involved in these transfers demonstrated that wild almond species originating in southwest Asia and southeast Europe could be valuable sources of new germplasm. Large numbers of interspecific hybrids and backcross breeding lines were also established. Studies were carried out on the inheritance of time of bloom, the correlations between bloom time and germination requirements, and heritability of numerous other almond genetic traits including pioneering work on isozyme analysis. A major effort begun in 1954 and continuing through the rest of Dr. Kester’s career was a series of genetic and physiological studies of noninfectious bud-failure. These eventually led to the critical distinction between the potential for occurrence and the actual level of phenotypic expression of this epigenetic disorder that increases with time and clonal age (cycles of propagation). Subsequent studies of clone variability within individual cultivars resulted in his strategies of clonal source selection for low bud-failure potential. Promising clonal sources (i.e., foundation sources for subsequent nursery vegetative propagation of true-to-type cultivars) were identified by a combination of individual tree source selection and subsequent vegetative progeny testing. In 1969, California’s clean tree stock program was thrown into turmoil because of the unexpected occurrence of early and severe noninfectious bud-failure in the Foundation Plant Material source of the principal almond cultivar ‘Nonpareil’ that accounts for half of the almond crop area in California and over half of the world’s production. The following years were dominated

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by genetic, physiological, and epidemiological research on this problem. Related research examined another clonal variability problem in ‘Mission’ involving nonproductivity in commercial nursery source material. By the time of retirement in 1991, new low bud-failure potential clone sources of essentially all almond cultivars except for ‘Carmel’ were identified and made available through the UC Foundation Plant Material Service. In addition, the protocols utilized in source maintenance had showcased procedures to stabilize low potentials for noninfectious bud-failure in individual clones, although this accomplishment was not recognized at the time. In 1989, a series of research initiatives in collaboration with department and extension colleagues not only detailed a comprehensive model for the development of noninfectious bud-failure in almonds, but also defined measures for its control. Key findings include the demonstration of the existence of two periods of seasonal dormancy in almond species; the discovery of an epigenetic, somaclonal decline of genes controlling high temperature summer dormancy, and the demonstration of predictable distribution patterns for this epigenetic factor following sexual and asexual reproduction. Nursery management practices introduced to control the resulting noninfectious bud-failure disorder include the identification and evaluation of elite source clone selections, and cultural management procedures for stabilizing source clones in subsequent propagations. Specific source clones developed by these methods account for approximately 70% of the 550,000 acres of almond presently planted in California. Dr. Kester has been a major professor to 16 M.S. and Ph.D. students and is remembered as a patient mentor whose keen insights and sanguinity were always available. He has published over 111 papers in refereed journals and conference proceedings, and has coauthored 76 reports. Dr. Kester’s first teaching assignment in the Department of Pomology was a course on Plant Propagation and he later taught General Pomology, Species and Environmental Aspects of Pomology Crops, and Nut Crops of California. In the early 1970s, Dr. Kester started a lifelong collaboration with Dr. Hudson Hartmann, who had also been teaching plant propagation. In 1979, this collaboration resulted in the preparation of a textbook, Plant Propagation, Principles and Practices. This publication has now gone through seven editions and has become the world standard text and reference in this field, having been translated into Spanish, Russian, and Italian. Following the death of Dr. Hartmann, Dr. Kester has coauthored later editions with Dr. Fred T. Davies and Dr. Robert L. Geneva, thus keeping this important reference current with emerging technologies.

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Dr. Kester helped found the Western Region of the International Plant Propagator Society, and he has served that organization in many capacities including Western Region President in 1997. He also served as the first Chair of the Propagation Working Group of the American Society of Horticultural Sciences. He has been a participant in many international symposia on almond, tissue culture, and breeding and has been recognized throughout the world for his expertise in those areas. In 1997, Dr. Kester became a fellow of the American Society for Horticultural Sciences, and in 1980 he received the Stark Award for pomological research. In recognition of his lasting contributions to pomological research and the education of horticulturalists throughout the world, he was honored as the Spencer Ambrose Beach Lecturer at Iowa State University in 1998. Dale Kester is truly a scholar and a gentleman who has devoted his life to science and who continues to contribute to horticultural progress in California and the world. Thomas M. Gradziel Department of Pomology University of California Davis, CA 95616-8683

1 Girdling: Physiological and Horticultural Aspects R. Goren, M. Huberman, and E. E. Goldschmidt* Kennedy-Leigh Centre for Horticultural Research The Institute of Plant Sciences and Genetics in Agriculture The Hebrew University of Jerusalem P.O. Box 12, Rehovot 76100, Israel

I. INTRODUCTION II. GIRDLING CONCEPTS AND TECHNIQUES A. Site of Girdling B. Morphology of the Girdle C. Damage D. Healing III. GIRDLING AND PHYSIOLOGICAL STUDIES A. Phloem Transport B. Assimilate Accumulation C. Translocation D. Source-Sink Investigations E. Flowering IV. ENDOGENOUS PLANT HORMONES V. GIRDLING IN HORTICULTURAL PRACTICE A. Rooting and Vegetative Growth B. Floral Induction and Juvenility C. Fruit Set D. Fruit Size E. Yield F. Fruit Maturity and Quality VI. CONCLUDING REMARKS LITERATURE CITED

*The valuable comments and suggestions for improvement of the manuscript by J. A. Barden, F. Bangerth, F. G. Dennis, and T. Robinson are gratefully acknowledged. Special thanks are due to J. Janick for his help with specific sections of the article. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 1

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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT

I. INTRODUCTION Farmers have practiced the use of girdling and related techniques in horticulture for thousands of years in order to increase crop production. Theophrastus (285 B.C.E.) refers to root pruning, girdling the stems, and driving iron pegs into the trunks of pear and other methods of “punishing trees” to hasten bearing. Girdling has been mentioned by Albertus Magnus (1193–1280), and is also described in a French apple growth manual from the 16th century (Spiegel-Roy 1976). In Maison Rustique (1616), the use of lead for pre-blossom girdling to improve both flowering and apple fruit quality is described (Janick 1972). An early mention of girdling can be also found in Shakespeare’s writings: . . . [We] at time of year Do wound the bark, the skin of our fruit-trees, Lest being over-proud in sap and blood, With too much riches it confound itself; . . . (Richard II, Act III, Scene IV, lines 57–60)

The culture of fruit trees is geared toward production of a high-value crop, integrating quantity and fruit quality. This is achieved by various techniques, including breeding, nutrition, pest control, and bioregulators as well as direct manipulations of the plant itself. Direct plant manipulations leading to the desired yield consist of two kinds of horticultural agrotechniques: (1) removal of certain tree organs (e.g., pruning, fruit thinning); and (2) interference with translocation between major tree organs (e.g., girdling, ringing, scoring [Table 1.1]; branch bending, which modifies auxin distribution, may be included in this second category). Fruit trees might be viewed as a system of sinks and sources (leaves, reproductive organs, and roots) interconnected via vascular organs (trunk, branches, scaffold roots). Girdling is basically an intervention in the phloem transport between canopy and roots, in an attempt to manipulate the distribution of photosynthate, mineral nutrients, and plant bioregulators. Girdling and similar techniques (Table 1.2) have also been used in physiological investigations of translocation processes in higher plant systems. Girdling has immediate and long-term effects, and local, as well as whole-plant, effects. Horticultural and physiological studies have addressed various direct and indirect aspects of girdling with numerous plant systems. The general response of the tree to girdling follows a wellknown pattern. Botanists have conducted many variations of girdling

1. GIRDLING: PHYSIOLOGICAL AND HORTICULTURAL ASPECTS Table 1.1.

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A glossary for girdling and related techniques.

Cincturing

Cutting a very narrow wound completely around the trunk or target branch.

Girdling

A procedure by which a ring of bark (or, in some cases, bark and sapwood) is removed from the trunk or branch of a tree or a ligature is tied tightly.

Hacking or frilling

A single line of overlapping downward axe cuts, leaving a frill into which toxic materials may be poured.

Notching

A shallow cut into the wood directly above a bud.

Nicking

A shallow cut into the wood directly above a bud (Syn. to notching).

Ringing

A form of girdling in which a cut is made with a pruning knife or a similar instrument around the circumference of a trunk or branch, with or without removal of a ring of bark.

Scoring

A form of girdling in which a narrow cut is made with a pruning knife or a similar instrument around the circumference of a trunk or branch.

Strangulation

Depressing the bark of the trunk or branches using a steel wire.

Stripping

Peeling off a band of bark completely around the tree.

Wiring

Depressing of the bark of the trunk or branches using a steel wire (Syn. to strangulation).

experiments for over 200 years and the conclusions have been essentially the same. Namely, the primary effect is the blocking of the downward flow of photosynthetic products at the girdle, while water and mineral transport from roots to the canopy is not directly affected. The use of girdling in forestry and its implications has been discussed extensively by Noel (1970). Two main factors limit the extensive application of girdling: (1) difficulties related to determining the optimal timing and environmental conditions for each species and location; and (2) uncertainties concerning the effect of girdling on trees, and fear of causing severe or even lethal damage by single or repeated treatments. In spite of these reservations, girdling is widely used even today with grapes, citrus, apple, peach, and other fruit tree crops, mainly in order to improve fruit set, size, and quality (Tables 1.3 and 1.4). The development of other agrotechnical practices, such as growth regulator treatments, has not always provided an efficient substitute for girdling in commercial horticulture. There is a vast horticultural literature on girdling. The purpose of the present review, however, is to provide a conceptual analysis, pointing out areas of comprehension as well as gaps in current knowledge. We

4 Table 1.2.

R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT Description of girdling techniques.z

Cincturing Girdling

Double girdling Guillotine girdling Ring-girdling Chemical girdling Hot girdling (Steam) Hot girdling (wax collar) Cold girdling

Hacking or frilling Notching Ringing

Scoring

Strangulation Stripping

Wiring

Cutting a very narrow wound completely around the trunk or target branch Complete removal of a bark cylinder, either narrow or wide, around the trunk or individual branches Usually in different sites of the tree Two opposing, deep horizontal chain-saw cuts made one-third the diameter of the tree trunk, separated vertically 20 cm Two opposing half-circle cuts on the trunk of the tree separated vertically 20 cm Painting a ring of chemical solution (i.e., of morphactin) around the trunk Encircling the petiole or stem by a flash of steam Hot wax (80–85°C) poured into a wooden collar sealed around the petiole A cold jacket applied around the petiole, cooled (1–3°C) by circulation of an ethanol/water mixture A single line of overlapping downward axe cuts, leaving a frill into which toxic materials may be poured Removing a piece of bark from directly above a bud, cut into the sapwood A form of girdling in which a cut is made with a pruning knife or a similar instrument around the circumference of a trunk or branch, with or without removal of a ring of bark Severing the bark tissue with a knife, by a single thin cut completely encircling the trunk, without removal of bark Depressing the bark using a steel wire, depth and tension as required Peeling off a band of bark completely around the tree. Synonymous with girdling, although it was pointed out that penetration of the sapwood might be involved Depressing the bark using a steel wire, depth and tension as required (synonymous to strangulation)

George et al. 1993 General literature

Winkler et al. 1974 Hoying and Robinson 1992 Hoying and Robinson 1992 Shulman et al. 1986 Moing et al. 1994 Goldschmidt and Huber 1992 Ntsika and Delrot 1986 Noel 1970

Hoying 1993 General literature

Powell and Howell 1985 Yamanishi et al. 1994 Kumar and Chhonkar 1974

Kim and Chung 2000

z A representative reference article is given for each technique; text of the table is not a quotation from the article.

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Table 1.3. Effect of girdling on fruit yield (selected references). Intensity of response is indicated by number of (+) signs. Crop

Effect

Comments

Reference

Apple (Malus × domestica)

++ ++ +

Second and third years Reduced tree size Restricted tree growth

Greene and Lord 1983 Williams 1985 Wang and Zheng 1997

Avocado (Persea americana)

++ +++ +++

Increased no. of fruits/tree Increased no. of fruits/tree Reduced shoot growth

Hackney et al. 1995 Kohne 1992 Ibrahim and Bahlool 1979

Citrus (Citrus spp.)

+++ +++

Increased fruit set Decreased no. of fruits/tree the following year Increased no. of fruits/tree

Agusti et al. 1990 Huberman and Goren 1996

+++ ++ +++ ++

Increased fruit splitting

Koller et al. 2000 Monselise et al. 1981 Rabe et al. 1996 Tuzcu et al. 1992

Grape (Vitis vinifera)

+ ++ ++ +++

Mango (Mangifera indica)

+++ ++ ++

Reduction of vegetative growth

Leonardi et al. 1999 Maiti et al. 1981 Rabelo et al. 1999

Nectarine (Prunus persica)

++

Yields were enhanced both years by all ringing treatments Fruits from girdled trees were significantly larger at harvest

Agenbag et al. 1992b

++ Olive (Olea europaea)

++ + ++ ++

Peach (Prunus persica)

+++

Persimmon (Diospyrus spp.)

+++ ++ ++

+++ +++

Increased bunch weight Increased fruit mass Delayed ripening

Increased no. of panicles/ shoot, fruit/panicle

Young branches more responsive Larger fruit, reduced shoot growth Reduced shoots growth Consistently advanced harvest Doubled flowers Fewer and shorter lateral branches

Botiyanski et al. 1998 Jawanda and Vij 1973 Ramming and Tarailo 1998 Wolf et al. 1991

Wand et al. 1991a Barut and Eris 1993 Ben-Tal and Lavee 1985 Gezerel 1984 Lavee et al. 1983 Allan et al. 1993 Perez and Rodriguez 1987 Powell and Howell 1985 Aoki et al. 1977 Blumenfeld 1986 Hasegawa and Nakajima 1991

6 Table 1.4.

R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT Effect of girdling on fruit quality (selected references).

Crop

Effects

Reference

Apple

Increase TSS and acidity, reduced Ca content Improved fruit color Improved fruit color

Arakawa et al. 1998

Reduced peel suberizing and uneven softening Various fruit parameters

Adato 1979

Citrus

Improved fruit color, TSS/acid Various fruit parameters Increased TSS/acid and sucrose

Peng and Rabe 1996 Simoes et al. 1999 Yamanishi 1995

Grape

Accumulation of anthocyanin Increased TSS Increased TSS and sugar/acid ratio Improved fruit color, dry matter, storage quality Improved fruit color, dry matter, storage quality Increasing dry matter and pulp color

El-Hammady and Abdel Hamid 1995 Jawanda and Vij 1973 Kim and Chung 2000 Kumar and Chhonkar 1974 Kumar and Chhonkar 1979 Simmons et al. 1998

Nectarine

Various fruit parameters Enhanced fruit coloring, early harvest Early ripening TSS, reduced in Ca content

Agenbag et al. 1992a Agusti et al. 1998 Vaio et al. 2001 Zhang 1997

Olive

Increased oil content

Proietti et al. 1999

Peach

Increased sugar content Increase in TSS and firmness Improved fruit color and TSS

Allan et al. 1993 El-Sherbini 1992 Yoshikawa 1988

Persimmon

Reduced no. of seeds/fruit, improved color Increase in TSS Improved fruit color and TSS

Hasegawa and Nakajima 1991 El-Shaikh et al. 1999 Hasegawa and Sobajima 1992

Avocado

Williams 1985 Wilton 2000

Trochoulias and O’-Neil 1976

intend to discuss practical and physiological aspects of fruit-tree girdling, and to evaluate the possible effects of girdling on various endogenous systems of fruit trees.

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II. GIRDLING CONCEPTS AND TECHNIQUES A series of synonymous, slightly overlapping terms can be found in the literature. Table 1.1 contains definitions of most girdling terms, mainly following the horticultural glossary of Soule (1985). Careful review of the literature indicates that slightly different meanings have been assigned to specific girdling terms by different authors. Nevertheless, throughout the present review, the terms used by the cited authors have been adopted. Table 1.2 lists the most frequently used girdling techniques in some detail. Some girdling instruments are pictured in Fig. 1.1. The various methods of girdling range from mechanical wounding techniques, through pressure by steel wires, to chemical girdling by application of morphactin solutions. Also, girdling has been used and is still being used in physiological investigations, mainly with herbaceous plants. In such studies, girdling is applied either to stems or to leaf petioles. One major technique used in physiological studies is heat girdling, which involves application of steam or a wax collar, causing phloem necrosis. A more delicate, non-damaging technique is cold girdling, which is discussed in detail in Section III. The type of girdling applied, especially its width, is very important and should be selected according to the desired effects (Krezdorn and Wiltbank 1968). Neither cambium nor deeper tissues should be damaged in regular horticultural girdling procedures (Noel 1970; Goren and Monselise 1971; Winkler et al. 1974; Jensen et al. 1975). Damage to the cambium prevents the formation of callus bridges over the exposed surface and xylem damage interferes with water and mineral supply to the canopy. Moreover, a cut in the xylem will prevent a complete recovery of the severed surface (Heinicke 1933; Winkler et al. 1974). Shulman et al. (1986) compared chemical (morphactin) and mechanical girdling (ringing) in grapevine and reported that neither method caused any visible damage in the year of treatment or in the following year. Using the criteria of berry size and total soluble solids (TSS) accumulation, Shulman et al. (1986) concluded, nevertheless, that chemical girdling was generally less effective than mechanical girdling. A. Site of Girdling The question often arises whether girdling of the trunk and girdling of the main branches have identical effects. In grape, cane girdling gave better results than arm or trunk girdling (Bhujbal and Chaudhari 1973) but, in general, all sites of girdling give comparable results. The susceptibility

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Fig. 1.1. Girdling instruments. A. “The Great Girdler©”, produced by Juran Works Ltd. Rishon LeZion, Israel, adapted from the original instrument developed by the late Dr. A. Cohen, Volcani Center, Israel. B. “Spanish” girdling scissors.

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of the tree to girdling must, however, be taken into account. Whenever there is a danger of causing severe damage to the tree, girdling should be applied to the main limbs, and one or two limbs should be left ungirdled (Krezdorn and Brown 1970; Lahav et al. 1971). This part-tree girdling prevents root starvation and reduces potential damage. In shy-bearing avocado trees, the common practice is to girdle only half of the limbs every year (Lahav et al. 1971). B. Morphology of the Girdle Classical botanical literature describes the morphology of the girdle and its healing. As mentioned above, girdling basically consists of a cut through the phloem; in most cases it involves the removal of a strip of bark from the circumference of the trunk or scaffold branch (Schneider 1954 and Fig. 1.1). For a schematic illustration of the anatomy of the girdle, see Fig. 1.2. Morphological responses to girdling were observed in

Fig. 1.2. Schematic illustration of a girdle, cutting through the bark in the trunk of a citrus tree (after Schneider 1954).

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citrus (Schneider 1954) and peach (Schneider 1945) in the trunk both above and below the girdle and in the roots below the girdle. Degeneration of sieve tubes and companion cells was accompanied by hypertrophy near the girdle (4 cm), followed by similar damage further from the wound (Schneider 1954). Phloem degeneration appeared within two weeks when girdling was performed in July but only after nine months when done in October (Schneider 1954). Another factor to be considered is the width of the ring. A ring of 3 mm caused partial death of summer branches in pistachio because the closing rate of the girdled area was too slow (Crane and Nelson 1972). Scoring was significantly less effective for increasing grape berry weight than 4.8 mm wide girdling (Jensen et al. 1981). Girdles up to 5 mm in width did not damage Shamouti orange trees treated at five dates during the year (Wallerstein et al. 1973). As a rule, a wider ring provides a more prolonged effect, but increases the risk of damage to the tree (Fernandez-Escobar et al. 1987). Relatively wide ringing should therefore be applied only to strong and vigorous trees that are capable of surviving the treatment (Krezdorn and Brown 1970; Goren and Monselise 1971; Lahav et al. 1971; Cohen et al. 1972). C. Damage Growers often regard girdling as a dangerous technique; indeed, damage or even the death of trees is occasionally observed. Sometimes, the growth of the trunk and the overall development of the tree may be retarded even though no external damage is apparent (Shamel and Pomeroy 1944; Winkler et al. 1974). The most common symptom of damage is leaf chlorosis, followed by leaf drop, which may occur even several months after girdling (Noel 1970). The rate of leaf drop determines the ability of the tree to recover. If leaf drop is intensive, the tree degenerates rapidly. Girdling damage is more pronounced in cases where the trees are weak and are grown under unfavorable conditions (Goren and Monselise 1971). Wounding can induce ethylene evolution and/or resin secretion. In some cases, the damage in the girdled area is related to diseases, mostly virus diseases (Krezdorn and Brown 1970). In extreme cases, branches dry up and the whole tree collapses (Lahav et al. 1971; Cohen et al. 1972). Root starvation is a serious problem when a complete trunk girdle is performed. In young citrus seedlings, the respiration rate of roots decreased immediately after girdling, accompanied by a gradual decrease in starch content of the main roots (Wallerstein et al. 1978a). Nematode-induced ethylene evolution may play a role in root damage

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and pathogenesis (Glazer et al. 1984). The most serious damage is done by the larvae, which bore into the bark and along the cambium of roots and often cause girdling of single roots or even the root collar (Kozlowski 1973). Trees can be severely injured or even killed if their trunks, taproots, or large lateral roots are partially encircled by other roots so that movement of water and nutrients through them is severely impeded or cut off. The strangling effect, similar to that caused by a wire tied tightly around a branch and left for a few years, does not cause sudden death, but results in deterioration evidenced over a period of a few years by weak growth and dying back of branches that normally would be supplied by the girdled root. Excess accumulation of carbohydrates in the canopy has been observed in girdled citrus and apple trees (Schaffer et al. 1986; Nii 1989). The damage due to excess carbohydrates is particularly striking in the absence of fruits or other sinks in the canopy. Ultrastructural studies indicated that leaf chlorosis, which is typically observed under these conditions, results from an unusual increase in the size of starch granules, causing a degeneration of the chloroplasts (Schaffer et al. 1986; Nii 1992). Additional causes of damage may be associated with disturbance of bi-directional transport of plant hormones, nutrients, and metabolites. D. Healing Healing of the wound and reestablishment of regular contact between root and canopy is critical for the future of the branch or tree. Healing consists of the regeneration of the vascular connection, which depends on cambial activity. For this reason, special care should be exercised to avoid any damage to the cambium. Persistence of effect of girdling depends on the length of time required for the formation of new callus bridges across the ring. New callus is formed at the margin of the cut surface, spreading gradually over the entire exposed surface (Sharples and Gunnery 1933). In peach, callus growth from the upper edge of the girdle downward was most prominent (Dann et al. 1985). In apple, very little callus is formed on the distal end of the girdle. The cambium begins to develop in this callus. Callus cells change into cambial cells wherever the intact vascular cambium impinges upon them. Thus, the callus cambium differentiates from all margins of the wound toward the center, the process being comparable to the closing of a diaphragm (Esau 1953). The new vascular cambium forms xylem and phloem in continuity with the same tissues in the uninjured portion of the stem. A periderm develops in the outer portion

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of the callus in line with the original stem periderm, if present (Sharples and Gunnery 1933). In citrus, the new callus bridges are formed about three weeks after ringing, at the time when the respiration level starts to recover and the decrease in starch level ceases (Wallerstein 1976). In grapes, callus bridges start to develop 16 days after ringing and a few days later phloem elements can already be detected in the callus (Sidlowski et al. 1971). In sugar maple, the rate of xylem and phloem element formation in the cambium surface of the girdled area depends on the season at which trees were girdled (Evert et al. 1972). Since differentiation of vascular elements in the callus depends on cambial activity, it takes longer for elements to form when girdling is performed during dormancy than when it is applied at a time of high cambial activity. It is advisable, therefore, whenever possible, to girdle during periods of intensive growth, when the time required for the formation of callus bridges is relatively short. Humidity is another factor that determines the rate of recovery. Wrapping the girdle with plastic strips can control humidity. If the cambium is not allowed to dry out, it should immediately start to produce callus and replace the phloem.

III. GIRDLING AND PHYSIOLOGICAL STUDIES A. Phloem Transport Girdling has been used for decades, and is still being used, as a major tool in physiological studies of translocation and source/sink relationships. This includes immediate, short-term as well as long-term effects (Curtis and Clark 1950). The main problems investigated using girdling techniques are phloem transport, metabolite distribution, and photosynthesis of source leaves. The preferable technique in physiological studies is “cold girdling” that consists of cooling of the stem or the petiole. Cold girdling causes a transient block of phloem transport without physical damage, unlike mechanical and heat girdling (Neales and Incoll 1968). Some investigators used temperatures of 1° to 3°C (Swanson and Geiger 1967; Ntsika and Delrot 1986), while others used temperatures up to 5°C (Krapp and Stitt 1995). Temperatures above 7°C are considered ineffective (Neales and Incoll 1968). A one- to three-centimeter length of petiole or stem was usually exposed to the low temperature treatment (Swanson and Geiger 1967; Ntsika and Delrot 1986; Krapp and Stitt 1995). In cold girdle of sugar beet, following the immediate decrease of transport there is a gradual recovery of transport, even while the stem

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13

is being cooled. Such rapid reversal of low temperature transport inhibition may not apply to all plant species (Swanson and Geiger 1967). Cold girdling is the major method enabling direct study of the translocation processes per se. Inhibition of translocation apparently results from physical blockage of sieve plates rather than from inhibition of metabolic processes (Giaquinta and Geiger 1973). When cold girdling blocked the export of photosynthates, Gamalei et al. (2000) reported that in coleus, cucurbits, pea, and sunflower the endoplasmic reticulum of intermediary cells collapsed, and the vacuoles of transfer cells enlarged. These changes were accompanied by starch accumulation in the mesophyll cells of all species studied. The condensation of the cytosol observed in the transfer cells (reminiscent of plasmolysis) was probably an osmotic response to cold girdling in the case of symplastic species. The possibility that cold-induced callose formation in the sieve plates is involved in blocking transport has been ruled out in sugar beet and bean (Swanson and Geiger 1967). B. Assimilate Accumulation One of the best-known effects of girdling is the accumulation of assimilates above the girdle (Mason and Maskell 1928; Ticho 1963; Greene 1937; Engard 1939; Murneek 1941; Weaver and McCune 1959; Zimmermann 1960; Stoltz and Hess 1966; Plaut and Reinhold 1967; Amir and Reinhold 1971; Little and Louch 1973; Wallerstein et al. 1974; Goldschmidt et al. 1985; Mataa et al. 1998). Assimilates may accumulate directly above the girdle, but generally increased levels of carbohydrates can be found throughout the canopy (Weaver and McCune 1959). Leaves that are the primary source organ store large amounts of carbohydrates, since their export is inhibited for a relatively long period (Engard 1939). Increased carbohydrates levels in the leaf are often associated with reduced photosynthesis. Trunk girdling of grapevine reduced the net CO2 assimilation rate by approximately 30%, and increased stomatal resistance, as compared with ungirdled control, 13 days after treatment. The reduction of photosynthetic rates due to girdling was smaller when vines were also sprayed with GA3 (Harrell and Williams 1987). Foliar carbohydrates were higher in girdled vines four weeks after the girdling treatment was imposed and, concomitantly, root carbohydrate concentrations were lower than in the untreated control (Roper and Williams 1989). Accumulation of sucrose and starch has been detected within 30 min. in heat-girdled bean leaves (Ntsika and Delrot 1986) and a rise in apoplastic sucrose within 60 min. (Ntsika and Delrot 1986; Voitsekhovskaja et al. 2000). Sorbitol, which is a major storage carbohydrate in woody Rosaceae

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(Wallaart 1980), accumulated within 60 min. in steam-girdled peach leaves (Moing et al. 1994). Longer response times (several hours or even days) may be expected when branch or trunk girdling is employed. The accumulation of those assimilates in the leaves apparently results from inhibition of phloem loading (Ntsika and Delrot 1986; Voitsekhovskaja et al. 2000). According to Jordan and Habib (1996), girdling of three-year-old peach seedlings mainly affected the accumulation of insoluble carbohydrates (starch?) in leaves and shoots above the girdle and their depletion in roots and rootstock-trunk bark. Soluble carbohydrate levels were not significantly affected, above or below the girdle. In a subsequent study, Jordan et al. (1998) showed that girdling strongly reduced nitrogen uptake in peach to 19% of that of non-girdled trees. However, almost all absorbed nitrate was reduced in the roots in both the girdled and non-girdled trees. They suggest that nitrogen uptake is strongly dependent on the continuous supply of photosynthates from shoots to the roots and that girdling modifies the nitrogen balance at the whole plant level. Girdling affected the activity of key enzymes involved in carbohydrate metabolism of the growing apple fruit (Beruter et al. 1997). When fruit-bearing wood was girdled during the period of active starch synthesis, sucrose and sorbitol content declined to 20–30%. Fructose concentration was unaffected and starch level decreased continuously with a concomitant rise in glucose content. Girdling increased the activities of hexokinase, fructokinase, phospho-fructo-phospho-transferase, and pyruvate kinase, suggesting that girdling activates glycolysis as a means of meeting the increased energy requirements (Beruter et al. 1997). C. Translocation Even with a mechanical girdle, certain components of translocation may by-pass the girdle. A study of the translocation of sucrose in one-yearold sour orange seedlings revealed two transport systems that responded differently to girdling. One is responsible for the slow (mass-flow) transport of sucrose in the phloem and is affected by girdling. The other is very rapid (2,040 m/hr), involves a minor amount of sucrose, and is unaffected by girdling (Wallerstein et al. 1978b). In the first, slow system, assimilates accumulate in the leaves as a result of girdling. Several hours later, assimilates start to migrate from the leaves and their accumulation is evident throughout the canopy (Wallerstein 1976; Wallerstein et al. 1978b). In mature trees, this is probably the system responsible for the beneficial effect of girdling on the reproductive organs. The other, rapid system supplies constant, although small, quantities of assimilates to the root during the immediate period after girdling. This movement is influ-

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15

enced by water tension, and might be related to movement on molecular surfaces (Hardy and Possingham 1969; Wallerstein et al. 1978b). Assimilates carried in the fast transport system appear to by-pass the girdled area. Experiments involving the application of 14C-sucrose to leaves revealed no differences in levels of radioactivity in the roots of girdled vs. non-girdled plants, supporting the assumption that girdling does not inhibit transport via the fast system (Wallerstein et al. 1978b). Assimilates in the form of sugars, glutamine and malic acid are known to bypass the girdle via the xylem in grapes (Harel and Reinhold 1966; Hardy 1969). In annual plants, too, sugars are capable of by-passing girdled areas (Zucconi et al. 1980), indicating that this ability is widespread in the plant kingdom. This is further demonstrated by a study of Stebbins and Dewey (1972), designed to determine the role of xylem and phloem in the accumulation of calcium in leaves. Girdling of apple seedlings indicated that the phloem was the primary route of 45Ca translocation. However, calcium appeared to leak into the xylem at increasing rates in the young stem and near the growing apex. D. Source-Sink Investigations The interruption of phloem transport and the ensuing accumulation of assimilates further influences the activity of source leaves. Girdling has been instrumental in attempts to verify the “sink feedback inhibition of photosynthesis” hypothesis (Neales and Incoll 1968). Girdling of grapevines eliminates the roots as a sink for assimilates, leading to assimilate build-up in leaves and causing a consistent reduction in photosynthesis (Kriedemann and Lenz 1972; Harrell and Williams 1987). Sink feedback inhibition builds up gradually following carbohydrate accumulation. Excess carbohydrates may interfere with photosynthesis through several mechanisms: (1) enlarged starch granules damaging the chloroplasts (Schaffer et al. 1986); (2) closure of stomata (Goldschmidt and Huber 1992); (3) accumulation of phosphorylated intermediates and depletion of inorganic phosphate (Krapp and Stitt 1995); and (4) indirect action by repressing the expression of genes that encode proteins needed for photosynthesis (Krapp and Stitt 1995). In a study aimed to explore the effect of crop load and girdling on apple fruit and leaf characteristics (Schechter et al. 1994a,b), fruit on mature girdled trees had higher dry weight and dry-matter concentration than fruit on nongirdled trees. In fruiting trees, leaves on girdled limbs had slightly lower photosynthetic rates but, in nonfruiting trees, leaves of the girdled limbs had 70% lower photosynthetic rates, high stomatal resistance, and high leaf internal CO2 concentration. The authors concluded, nevertheless,

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that the results do not necessarily support the concept of feedback inhibition of photosynthesis, and propose alternative explanations for the relationship between leaf activity and excessive carbohydrate accumulation in leaves. Similar conclusions were reached by Harrell and Williams (1987) in a study of girdling-induced depression of photosynthesis in grapevine. It may still be argued, however, that the data of these studies are best interpreted through the “feedback inhibition of photosynthesis” concept. Girdling is also used in long-term source/sink experiments in fruit trees, as a means for isolating a fruit-bearing branch from the rest of the tree (Fishler at al. 1983; Bustan et al. 1995; Laing and Clark 1996). Such an experimental system has also been used for modeling of fruit development (Genard et al. 1998; Lescourret et al. 1998). E. Flowering The elusive florigen, nowadays more often called “floral stimulus,” is believed to move via the phloem. Girdling has been used extensively in flowering research, as a means for interrupting the movement of the floral stimulus, as well as for determination of the precise timing and velocity of this movement (Lang 1965). Among fruit trees, girdling has been most frequently used with mango, to demonstrate the role of leaves in supplying the floral stimulus (Reece et al. 1949; Davenport and Nunez-Elisea 1997). In a recent study of flowering in Sinapis alba, Havelange et al. (2000) showed that girdling interfered with the movement of sucrose into roots and at the same time reduced the export of cytokinins from the roots to the shoots. Girdling seems therefore to remain an efficient tool for physiological studies in both herbaceous and perennial plants.

IV. ENDOGENOUS PLANT HORMONES Girdling-induced interruption of phloem transport should affect not only assimilates but also other organic compounds. Among these, plant hormones may be of special interest since they are known to play regulatory roles in various processes of growth and development. Changes in the distribution of plant hormones may therefore be anticipated, as well as effects on their biosynthesis in distant organs. Contrary to the rather consistent horticultural effects of girdling (promotion of floral induction, fruit set and enlargement, fruit quality, yield), the picture

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emerging from girdling-related endogenous hormone studies is fragmentary and somewhat confusing. Dann et al. (1985) found in peach a transient accumulation of IAA above the girdle, that peaked within 24 hr after girdling. This might be causally related to the often-observed thickening of the branch above the girdle (Chalmers 1985; Dann et al. 1985). Girdling-induced thickening of the branch above the girdle of a young citrus tree is shown in Fig. 1.3. In addition, Dann et al. (1984) suggest that lower cytokinin and/or gibberellin synthesis/activation by the roots may be a secondary effect of

Fig. 1.3. Thickening of the branch above the girdle of a young ‘Murcott’ tangerine hybrid citrus tree.

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girdling, resulting from the diminished supply of phloem-borne substances to the roots. This hypothesis was substantiated by Cutting and Lyne (1993). They found a significant reduction in the concentration of the cytokinin, zeatin-riboside, and gibberellin A1 and A3 in the xylem sap of peach shoots above the girdle that persisted for 7 weeks, and a corresponding reduction in shoot growth. Trunk girdling of apple trees at full bloom also reduced the content of zeatin riboside above the girdle (Skogerbo 1992). A similar decrease in cytokinins above the girdle was found by Skene (1972) in grape vine shoots and by Havelange et al. (2000) in Sinapis alba. These observations presumably indicate a depression of hormone biosynthesis in roots, which might be associated with carbohydrate depletion and reduced root growth. Weaver and Pool (1965) reported an increase of gibberellin-like substances in some fractions of grape berry extracts in girdled vines, while other fractions showed a decrease. Trunk girdling of citrus trees induced an increase of gibberellin-like substances in bark and leaves above the ring (Goren et al. 1971). On the other hand, Wallerstein et al. (1973) found a decrease in gibberellin-like substances in young citrus fruitlets above the girdle. In a seasonal study, ringing caused in most cases an increase in gibberellin-like substances in new lateral shoots, while the opposite trend was found in rootlets. Attempts to establish a relationship between citrus’s floral induction and endogenous IBA, IAA, ABA, and gibberellins in leaves of ringed branches did not lead to conclusive results (Koshita et al. 1999). Various modes of girdling had little effect on the distribution of endogenous ABA in grape vines (During 1978). Girdling reduced IAA and ABA levels in sitka spruce branches (Little and Wareing 1981). Girdling reduced the level of auxin above the girdle in hibiscus (Stoltz and Hess 1966). Dann et al. (1985) reported that girdling did not entirely deplete the IAA immediately below the girdle; it reduced it by 75% and severely reduced growth and cell division of the cambium. The decrease in IAA concentration below the girdle strongly indicated that girdling interrupts the basipetal transport of auxin (Little and Wareing 1981; Dann et al. 1985). Wilson (1968) reported an increase in radial cell number in white pine up to 310 cm above the girdle. He suggested that this might be explained by the effect of girdling in blocking the polarized auxin transport as well as the non-polarized phloem transport system. Girdling of nectarine trees two weeks before pit hardening increased the rate of endogenous IAA accumulation during stage II of fruit development, when the growth rate was also higher. Thereafter, the IAA concentration fell to control levels, but total pericarp IAA content remained

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higher. Reducing IAA transport by applying 2,3,5-triiodo-benzoic acid (TIBA) reduced the amount of calcium entering the fruit. On the other hand, girdling reduced the calcium concentration during stage II, but increased it during stage III so that fruits from girdled trees had a much higher calcium content at harvest (Wand et al. 1991b). Similar results, showing that both TIBA and girdling decreased calcium concentration, were obtained in fruits of certain apple cultivars (Tomala and Dilley 1989). Girdling of young ‘Red Fuji’ apple trees resulted in increased contents of zeatin riboside and IAA in spur buds (Li et al. 1996).

V. GIRDLING IN HORTICULTURAL PRACTICE The use of girdling as a horticultural technique requires consideration of tree age, health and vigor, as well as growing conditions. The grower must take into account the anticipated benefits as against the risks involved. The success of girdling depends upon careful execution of this delicate manipulation. The accumulation of carbohydrates in the canopy provides a rich source of energy for all the stages of reproductive development; flowering, fruit set, fruit enlargement, and ripening. The most common purpose of girdling is to increase fruit set by reducing fruitlet drop. Girdling is also performed to increase fruit size. In alternate-bearing trees, girdling increases the carbohydrate level in the canopy during “off” years, following the intensive utilization of carbohydrate reserves during “on” years (Crane and Nelson 1972). Weaver and McCune (1959) argue that the increase in carbohydrates following girdling is not the only reason for the increase in fruit set and fruit size in grapes. They base their argument on the fact that thinning, which also increases the availability of carbohydrates to the cluster, has only a slight effect on fruit size. A. Rooting and Vegetative Growth Girdling is being used to promote rooting of hardwood cuttings (Noel 1970; Hartmann and Kester 1975). Girdling shoots before their removal from stock plants presumably blocks the downward translocation of carbohydrates, hormones, and other root-promoting factors, leading to an increase in root initiation (Hartmann and Kester 1975). In some cases, girdling promotes rooting even without addition of synthetic auxins (Wood 1989). Details of this technique have received considerable attention (Evert and Smittle 1990; Oliveira et al. 2000).

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Girdling has often been observed to reduce canopy shoot growth (Dennis and Edgerton 1966; Priestly 1976; Greene and Lord 1983; Cutting and Lyne 1993). Some restriction of vegetative growth is desirable in vigorous apple cultivars. Notching, scoring, and ring girdling have been used successfully to reduce apple shoot growth (Hoying 1993). Both ring girdling and the related “guillotine girdling” (Table 1.2) reduce trunk cross-sectional area, average shoot length, and average number of shoots per tree (Hoying and Robinson 1992). Notching is used to ensure scaffold development in young trees (Hoying 1993) by stimulating lateral shoot growth (Greene and Autio 1992). Notching above apple vegetative buds was most effective when performed with buds on the top of the branch 2 to 4 weeks prior to full bloom (Greene and Autio 1992). The mechanism is presumably hormonal; the notch (Fig. 1.2) blocks basipetal flow of auxin, which normally inhibits lateral shoot growth (Greene and Autio 1992). Another facet of the same phenomenon, though mostly undesirable, is the formation of water sprouts directly below the girdle, generally known as basal sprouting (Noel 1970). B. Floral Induction and Juvenility Girdling and similar techniques have been used in attempts to induce earlier flowering of seedling apple trees (Zimmerman 1972; Meilan 1997). Maximum response was obtained with trees that were on the verge of flowering or had already produced a small number of flowers. Way (1971) reported that scoring 4- to 7-year-old apple seedlings was more effective in inducing flowering than scoring 3-year-old seedlings. Girdling branches of mature apple trees significantly increased flower bud formation (Dennis and Edgerton 1966). Ringing between May 30 and July 30 inhibited flower formation in the following year (Jona and Casale 1976). Induction of flower formation was found to be a fairly gradual process that culminated in mid-June and was complete by late July. Scoring ‘Delicious’ apple for three consecutive years consistently reduced terminal growth and increased yield during the second and third years (Greene and Lord 1983). Li et al. (1996) reported an increased flower bud formation in 5-year-old ‘Red Fuji’ apple with girdling (+534%), girdling plus paclobutrazol (+648%), and paclobutrazol alone (+154%). Ringing hastened flowering of juvenile citrus seedlings. More than 60% of 7-year-old trees flowered the year after ringing, but only 3% of 3-year-old trees flowered (Furr et al. 1947). Autumn girdling increased flower number of ‘Murcott’ citrus three-fold and markedly intensified

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the flowering of ‘Shamouti’ orange (Goldschmidt et al. 1985) and ‘satsuma’ mandarin (Erner 1990; Iwahori et al. 1990; Garcia-Luis et al. 1995). Girdling shortened the juvenile period of avocado seedlings (Lahav et al. 1986). Girdling before bloom, at full bloom, and after full bloom did not significantly affect the yield of ‘Fuerte’ avocado (Gregoriou 1989). In avocado trees girdled several months before flowering, only the timing of floral expression seemed to be altered, not the number of flowers or inflorescences (Ibrahim and Bahlool 1979). In some cases, girdling had no apparent effect on flowering of avocado (Lahav et al. 1971). Girdling induced formation of pistillate flowers on juvenile pecan clones (Thompson 1986). Girdling was ineffective in induction of flowering in sweet cherry (Oliviera and Browning 1993). Ben-Tal and Lavee (1984) report a significant increase of flowering following girdling of biennial bearing olive trees during their “off” year. Girdling has an inconsistent effect on flowering in mango, as noted by Davenport and Nunez-Elisea (1997), who summarized numerous earlier reports. The promotion of flowering by girdling may reflect the need for threshold levels of carbohydrate in the canopy for flower formation (Goldschmidt et al. 1985). Bernier and co-workers assign a role for sucrose in the floral induction of Sinapis alba (Bodson and Outlaw 1985; Havelange et al. 2000). However, girdling also interfered with the transport of plant hormones (Cutting and Lyne 1993) and other metabolites. Thus, a specific role played by carbohydrates in the initiation of flowering has not been unequivocally demonstrated (Davenport and Nunez-Elisea 1997). C. Fruit Set Fruit set is a critical process in cropping. Persistence of the young fruitlets or their abscission is a major physiological event resulting from a variety of endogenous and environmental factors (Goldschmidt 1999). Girdling, close to or during bloom, increases fruit set in numerous tree crops, mostly by reducing fruitlet abscission as in: citrus (Monselise et al. 1972; Cohen 1981; Barry and Bower 1997), apple (Dennis and Edgerton 1966; Dennis 1986; Kyun et al. 1997), olive (Fortanazza et al. 1987), and persimmon (Hasegawa and Sobajima 1992). Similar effects were also found after strangulation of citrus in early spring (Yamanishi et al. 1994). In avocado, on the other hand, girdling in order to increase fruit set is commonly employed during the preceding autumn (Tomer 1977). Carbohydrate level is one of the factors limiting fruit set (Garcia-Luis et al. 1988; Caspari et al. 1998; Goldschmidt 1999). Since girdling causes accumulation of carbohydrates in the canopy, the effect of girdling on

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fruit set may be a result of increased supply of carbohydrates to the reproductive organs. In avocado, girdling increases the level of carbohydrates in the pistil (Tomer 1977). In cultured flowers, addition of sugars to the medium enhanced the growth of the pollen tube and its penetration into the ovule. This suggests that, at least in avocado, girdling affects fruit set by increasing the level of carbohydrates in the pistil, which causes faster growth of the pollen tubes (Tomer 1977). The involvement of plant hormones in fruit set processes is recognized (Crane 1964; Monselise 1986), thus the effect of girdling on fruit set may also involve changes in hormonal balance. Indeed, application of gibberellins is often combined with girdling to ensure adequate fruit set in grape (Winkler et al. 1974) and citrus (Goren et al. 1992; El-Otmani et al. 2000). Girdling may lead to higher yield in citrus, even when performed during the fruitlet abscission period due to reduction of the last stages of fruitlet drop (Koller et al. 2000; A. A. Schaffer and E. E. Goldschmidt, unpublished data). D. Fruit Size The positive effect of girdling on fruit size is well documented and girdling for this purpose is widely used in grape (Weaver and McCune 1959; Jawanda and Vij 1973; Peruzzo 1994; Dokoozlian et al. 1995; Kim and Chung 2000). Girdling-induced increase in fruit size has also been reported in peach (El-Sherbini 1992; Allan et al. 1993; Agusti et al. 1998), nectarines (Fernandez-Escobar et al. 1987; Villiers 1990; Agusti et al. 1992), mango (Bhattacharyya and Mazumdar 1990; Simmons et al. 1998), avocado (Davie et al. 1995), olive (Lopez Rivares and Suarez Garcia 1990; Barut and Eris 1993; Proietti et al. 1999), and persimmon (Hasegawa and Sobajima 1992; El-Shaikh et al. 1999). Less effect of girdling on fruit size was found in apple (Arakawa et al. 1998; Miller 1995; Wilton 2000). Grape vines are girdled after the termination of fruit set in order to avoid effects on fruit number. Girdling when 50% of the berries were 4–5 mm in diameter reduced the incidence of berry shatter and improved berry size (Wolf et al. 1991). Girdling-induced increase in grape berry size is commonly combined with GA3 treatment (Weaver and McCune 1959). In peach and nectarine, girdling is most effective prior to stage II of fruit growth (pit hardening). Girdling at this stage shortened stage II and caused peak fruit growth rate to occur earlier in the season (Day and DeJong 1990; Agusti et al. 1998). It increased fruit weight by 22 to 25%, and more than doubled the percentage of fruit in the larger fruit size category (Day and DeJong 1990). Similar results were obtained in an earlier study of apricot (Lilleland and Brown 1936).

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Ringing of apple trees 3 weeks after full bloom caused slight fruit elongation (Webster and Crow 1969). Girdling of grapefruit trees during anthesis may increase fruit set but eventually reduce fruit size (Cohen 1981). Girdling at different times during fruit growth invariably increased fruit size; early summer girdling was most effective (Hochberg et al. 1977; Fishler et al. 1983; Cohen 1984). Up to 100% increase in fruit weight was obtained in grapefruit following girdles in late May (Cohen 1984). Girdling combined with fruit thinning had a dramatic effect on fruit size (Goldschmidt 1999). Double girdling (15 cm below the scaffold branches junction level, and a second girdling 5 cm above it) at 75% petal fall markedly increased fruit size and yield of clementine citrus (Tuzcu et al. 1992). Girdling-induced increase in fruit size is most probably caused by improved supply of photosynthates to the developing fruit. This is indicated by the fact that, in citrus, girdling is effective throughout fruit development (Fishler et al. 1983), while auxins (and other plant growth substances), are effective only during the early stage of fruit development (Ortola et al. 1997).

E. Yield Increasing yield is one of the main goals in fruit tree culture. Since yield is a product of fruit number and fruit weight, an increase in yield may result from either an increased number of fruit units or from larger fruit (or their combination). Girdling often increases yield in various tree crops (Table 1.3), especially when yield of controls is low, as in young trees or in alternate bearing orchards. Excessive numbers of fruit units may produce a large crop of small, low-price fruit, which requires adjustment by thinning. This situation is often encountered with grapes and with tangerine hybrids; girdling may be necessary to secure adequate fruit set, but fruit thinning is subsequently applied to ensure reasonable fruit size (Winkler et al. 1974; Galliani et al. 1975).

F. Fruit Maturity and Quality While fruits approaching maturity are still actively growing, additional processes that are characteristic of maturity occur, primarily changes in sugars, acids, and pigmentation, all of which are highly dependent upon the supply of photosynthates. Girdling enhances maturation in various crops, particularly in grape and peach. Effects of girdling on grape maturation and quality have been described by Winkler et al. (1974). Girdling for hastening of maturation and improving quality is performed

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in grape at the beginning of ripening (veraison), or combined with earlier girdling after fruit set (double girdling) (Winkler et al. 1974; Carreno et al. 1998). Jacob (1931) recommended that girdling be done when the berries are about half-grown and that the wound be kept open during the ripening period. In one experiment, Weaver (1952) showed that the best coloration resulted from girdling ‘Red Malaga’ grapes when total soluble solids (TSS) reached about 13 or 14%, and that TSS increased more rapidly with early girdling. In a later study, Weaver (1955) reported that early girdling, when TSS content of ‘Red Malaga’ and ‘Ribier’ grapes was only 5 or 6%, usually resulted in the most rapid maturation. He suggested that girdling at this time coincides with decreased vegetative activity of the vine. Girdling of ‘Italia’ grape at the beginning of ripening significantly increased soluble solids and maturity index, and improved berry color, reduced titratable acidity, and advanced fruit ripening by five days (Carreno et al. 1998). Girdling table grapes after fruit set in cool climate growing areas markedly increased yield but consistently reduced soluble solids concentration, presumably due to dilution of the photosynthates (Zabadal 1992). Girdling or scoring consistently advanced peach harvest (Powell and Howell, 1985). In nectarine, girdling during the beginning of stage two of fruit development increased TSS concentration by about a half (Day and DeJong 1990), but girdling during stage three did not affect fruit maturation or quality (El-Sherbini 1992). In another study, fruit coloration was also enhanced (Bakr et al. 1981; Agusti et al. 1998). Girdling increased total phenolic content and high-molecular-weight phenols of peach fruit (Kubota et al. 1993a) as well as L-phenylalanine-ammonia-lyase activity (Kubota et al. 1993b). Enhanced ripening of peach and nectarine on girdled branches was associated with an earlier climacteric, resulting in higher ACC, ACC oxidase, and ethylene values (Agusti et al. 1998). Some investigators found that girdling sometimes increases the frequency of pit splitting (Kubota et al. 1993a), while others did not detect such an effect (Day and DeJong 1990; Allan et al. 1993; Agusti et al. 1998). Girdling of olives in mid-August increased fruit dry weight by 15% and oil content from 5 to 10% (Proietti et al. 1997). Fruit on girdled cherry trees were higher in soluble solids and color (Roper et al. 1987). Trunk strangulation of pummelo citrus tree increased sucrose and citric acid content in juice (Yamanishi et al. 1995). In apple, girdling as late as three weeks before harvest increased fruit firmness and TSS concentration (Elfving et al. 1991). Girdling and bark inversion of apple trees improved the eating quality of the fruit by increasing TSS content, while reducing water and calcium content (Arakawa et al. 1998). In apple

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flowers, girdling suppressed nectar production and reduced the sugar concentration of the remaining nectar (Campbell et al. 1991). More details are presented in Table 1.4.

VI. CONCLUDING REMARKS Girdling has a broad range of horticultural effects. As discussed above, all stages of reproductive development are influenced: flowering, fruit set and development and, in many instances, fruit maturity and quality as well. A model describing the effects of girdling on the distribution of photosynthate, feedback inhibition of leaf activity, and the transport of plant hormones is illustrated in Fig. 1.4. However, mechanism(s) through which girdling operates are not yet fully understood. The supply of water and mineral nutrients via the xylem is not generally affected by girdling. Logically, therefore, girdling must affect phloem-transported components. Two major candidates are apparent: photoassimilates (carbohydrates) and plant hormones. Evidence for involvement of carbohydrates in girdling effects is extensive and detailed (Weaver and McCune 1959; Priestley 1976; Goldschmidt and Huber

Fig. 1.4. A model illustrating the effects of girdling on the flow of carbohydrates and hormones in fruit trees. Arrows indicate the direction of transport and not the vascular site of transport.

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1992). Numerous studies have reported the accumulation of carbohydrates in canopy organs above the girdle and a simultaneous decline in carbohydrates below the girdle, often resulting in root starvation (Weaver and McCune 1959; Noel 1970). The multitude of carbohydrates in the canopy provides additional dry matter and energy for reproductive processes, that have a high energy and dry matter demand (Bustan and Goldschmidt 1998). This involves all of the reproductive stages mentioned above, thereby providing an explanation for the positive effects of girdling in all these stages. The evidence supporting the involvement of endogenous plant hormones in girdling effects, on the other hand, is somewhat equivocal and incomplete. Nevertheless, the following relationships can be portrayed. Auxins, known to be transported basipetally, seem to accumulate above the girdle (Dann et al. 1985), stimulating, in many cases, excessive growth immediately above the girdle (Fig. 1.3). At the same time, girdling seems to reduce the supply of cytokinins to the canopy (Skogerbo 1992; Cutting and Lyne 1993; Havelange et al. 2000). This may be responsible for the often-observed inhibition of shoot growth (Priestley 1976; Cutting and Lyne 1993). Other lines of circumstantial evidence also point to the role of cytokinins as regulators of shoot growth (Hall 1973). Since cytokinins are presumably produced in roots and transported upward via the xylem, the reduced supply of cytokinins to the canopy in girdled trees does not seem to result from blockage of transport but, rather, from an indirect effect on cytokinin production (Cutting and Lyne 1993), brought about perhaps by root starvation. In general, the effect of girdling on root-associated processes needs closer attention. The advance of plant science in recent years has indicated that plant responses to agrotechnical manipulations are likely to involve molecular up- and down-regulation of gene activity. It may, therefore, be assumed that responses to girdling also include changes in gene expression. Future girdling research will undoubtedly address this assumption, leading to more focused insight into the multiple far-reaching effects of girdling.

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Agenbag, H., and I. du Toit. 1992b. Girdling as an aid to harvest scheduling. Deciduous Fruit Grower 42:410–412. Agusti, M., V. Almela, and J. Pons. 1992. Effects of girdling on alternate bearing in citrus. J. Hort. Sci. 67:203–210. Agusti, M., V. Almela, and A. M. Mingo-Castel. 1990. Effect of kinetin and ringing on fruit set in the orange cultivar ‘Navelate’ (Citrus sinensis (L.). Osbeck). Investigacion Agraria, Produccion, Proteccion-Vegetales 5:69–76. Agusti, M., I. Andreu, M. Juan, V. Almeta, and L. Zacarias. 1998. Effects of ringing branches on fruit size and maturity of peach and nectarine cultivars. J. Hort. Sci. Biotech. 73:537–540. Allan, P., A. P. George, R. J. Nissen, and T. S. Rasmussen. 1993. Effects of girdling time on growth, yield, and fruit maturity of the low chill peach cultivar ‘Flordaprince’. Austral. J. Expt. Agr. 33:781–785. Amir, S., and L. Reinhold. 1971. Interaction between K-deficiency and light in C14-sucrose translocation in bean plants. Physiol. Plant 24:226–231. Aoki, M., K. Tanaka, and N. Okada. 1977. Effects of nitrogen fertilization and ringing treatment on initial yield of persimmon (Diospyros kaki), cv. ‘Wasejiro’. Research Bul. Aichi Ken Agr. Res. Center, Horticulture 9:119–130. Arakawa, O., A. Kanetsuka, K. Kanno, and Y. Shiozaki. 1998. Effects of five methods of bark inversion and girdling on the tree growth and fruit quality of ‘Megumi’ apple. Japan. Soc. Hort. Sci. 67:721–727. Bakr, E. I., K. M. Abdalla, M. A. Meligi, and I. A. Ismail. 1981. Floral differentiation in mango as affected by growth regulators, ringing and defoliation. Egyptian J. Hort. 8:161–166. Barry, G. H., and J. P. Bower. 1997. Manipulation of fruit set and stylar-end fruit split in ‘Nova’ mandarin hybrid. Scientia Hort. 702:243–250. Barut, E., and A. Eris. 1993. Research on the effects of girdling, thinning and plant growth regulators on yield, quality and alternate bearing in olive cv. ‘Gemlik’. Doga,Turk Tarim ve, Ormancilik-Dergisi. 17:953–970. Ben-Tal, Y., and S. Lavee. 1984. Girdling olive trees, a partial solution to biennial bearing. II. The influence of consecutive mechanical girdling, on flowering and yield. Riv. Ortoflorofrutt. It. 68:441–451. Ben-Tal, Y., and S. Lavee. 1985. Girdling olive trees, a partial solution to biennial bearing. III. Chemical girdling: its influence on flowering and yield. Riv. Del. Ortoflorofrutt. It. 69:1–11. Beruter, J., M. Feusi, and E. Studer. 1997. The effect of girdling on carbohydrate partitioning in the growing apple fruit. J. Plant Physiol. 151:277–285. Bhattacharyya, A. K., and B. C. Mazumdar. 1990. Quality of mango fruits due to ringing of fruit bearing shoots and auxin application on leaves of ringed shoots. Agr. Res. 5: 75–78. Bhujbal, B. G., and K. G. Chaudhari. 1973. Yield and quality of ‘Thompson seedless’ grape (Vitis vinifera L.) as influenced by girdling and gibberellins. Res. J. Mahatma Phule Agr. Uni. 4:108–112. Blumenfeld, A. 1986. Improving productivity of ‘Triumph’ persimmon. Alon Hanotea 40:539–544. Bodson, M., and W. H. Outlaw, Jr. 1985. Elevation in the sucrose content of the shoot apical meristem of Sinapis alba ay floral evocation. Plant Physiol. 79:420–424. Botiyanski, P., T. Mokreva, and V. Roichev. 1998. Biometric characteristics of seed-buds and grapelets, formed after girdling of seedless grapevine varieties. Bulgarian J. Agr. Sci. 4:605–611.

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Heinicke, A. J. 1933. The assimilation of carbon dioxide by apple leaves as affected by ringing the stem. Proc. Am. Soc. Hort. Sci. 29:225–229. Hochberg, R., S. P. Monselise, and J. Costo. 1977. Summer girdling and 2,4-D effects on grapefruit size. HortScience 12:3, 228. Hoying, S. A. 1993. Benefits and pitfalls of nicking, notching, ringing, girdling and root pruning apple trees. Compact Fruit Tree 26:66–68. Hoying, S. A., and T. L. Robinson. 1992. Effects of chain saw girdling and root pruning of apple tree. Acta Hort. 322:167–172. Huberman, M., and R. Goren. 1996. Effects of plant growth regulators and girdling on yield of ‘Sweetie’ (‘Oroblanco’) (in Hebrew with English abstr.). Alon Hanotea 50:194–199. Ibrahim, I. M., and S. El D. Bahlool. 1979. The effect of girdling on flowering, fruiting and vegetative growth of avocado trees. Agr. Res. Rev. Hort. 57:55–66. Iwahori, S., A. Garcia-Luis, P. Santamarina, C. Monerri, and J. L. Guardiola. 1990. The influence of ringing on bud development and flowering in ‘Satsuma’ mandarin. Expt. Bot. 41:1341–1346 Jacob, H. E. 1931. Girdling grape vines. Calif. Agr. Exp. Service Circ. 56. Janick, J. 1972. Biological control. p. 248–256. In: Horticultural science. San Francisco, CA. Jawanda, J. S., and V. K. Vij. 1973. Effect of gibberellic acid and ringing on fruit set, cluster and berry characters and fruit quality of ‘Thompson seedless’ grape. Indian Agr. Sci. 43:346–351. Jensen, F., H. Andris, and R. Beede. 1981. A comparison of normal girdles and knife-line girdles on ‘Thompson seedless’ and Cardinal grapes. Am. Enol. Vitic. 32:206–207. Jensen, F., F. Swanson, W. Peacock, and G. Leavitt. 1975. The effect of width of cane and trunk girdles on berry weight and soluble solids in table ‘Thompson seedless’ vineyards. Am. Enol. Vitic. 26:90–91. Jona, R., and L. Casale. 1976. Studies on the time of flower induction in ‘Golden delicious’ apple. Fruticoltura 38:39–41. Jordan, M. O., and R. Habib. 1996. Mobilizable carbon reserves in young peach trees as evidenced by trunk girdling experiments. J. Expt. Bot. 47:79–87. Jordan, M. O., R. Habib, and M. Bonafous. 1998. Uptake and allocation of nitrogen in young peach trees as affected by the amount of photosynthates available in roots. Plant Nutr. 21:2441–2454. Kim, W. S., and S. J. Chung. 2000. Effect of GA3, ethephon, girdling and wiring treatment on the berry enlargement and maturity of ‘Himrod’ grape. J. Korean Soc. Hort. Sci. 41:75–77. Kohne, J. S. 1992. Increased yield through girdling of young ‘Hass’ trees prior to thinning. Yearb., South-African Avocado Growers’ Assoc. Vol. 15 issue 68. Koller, O. L., E. Soprano, A. C. Z-da. Costa, O. C. Koller, and O. K. Yamanishi. 2000. Flowering induction and fruit production in oranges cv. ‘Shamouti’. Laranja 21:307–325. Koshita, Y., T. Takahara, T. Ogata, and A. Goto. 1999. Involvement of endogenous plant hormones (IAA, ABA, GAs) in leaves and flower bud formation of ‘Satsuma’ mandarin (Citrus unshiu Marc.). Sci. Hort. 79:185–194. Kozlowski, T. T. 1973. Shedding of plant parts. p. 560. Academic Press, New York. Krapp, A., and M. Stitt. 1995. An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after coldgirdling source leaves. Planta 195:313–323. Krezdorn, A. H., and H. D. Brown. 1970. Increasing yields of the ‘Minneola’, ‘Robinson’ and ‘Osceola’ varieties with gibberellic acid sprays and girdling. Proc. Fla. Sta. Hort. Soc. 83:29–34. Krezdorn, A. H., and W. J. Wiltbank. 1968. Annual girdling of ‘Orlando’ tangelos over an eight-year period. Proc. Fla. Sta. Hort. Soc. 81:17–23.

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2 Irrigation Water Quality and Salinity Effects in Citrus Trees* Yoseph Levy Agricultural Research Organization Department of Fruit Tree Sciences Gilat Research Center, Mobile Post Negev, 85-280 Israel Jim Syvertsen University of Florida, IFAS, Citrus Research and Education Center 700 Experiment Station Road Lake Alfred, Florida 33850-2299, USA

I. INTRODUCTION II. MANAGING SALINITY A. Irrigation and Salinity B. Rootstocks and Scions III. EXPERIMENTAL METHODS IN SALINITY RESEARCH A. Leaf Analysis B Juice Analysis C. Seed Mineral Content D. Biochemical Indicators E. Seed Germination F. Solution Culture vs. Soil Culture G. Seedling Rootstocks vs. Budded Trees H. Greenhouse vs. Field Studies I. Tissue Culture vs. Whole Plant IV. PHYSIOLOGICAL RESPONSES A. Amino Acids Accumulation B. Net Gas Exchange of Leaves C. Salinity Interactions with Physical Environmental Factors *We thank Drs. G. Albrigo and M. Talon for helpful comments. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 37

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D. Osmotic Stress E. Toxic Ions F. Vegetative Growth G. Fruit Yield and Quality H. Phytochemicals V. SALINITY AND BIOTIC STRESSES A. Phytophthora B. Rio Grande Gummosis C. Nematodes D. Mycorrhizae VI. BENEFITS OF MODERATE SALINITY A. Chilling and Freezing Tolerance B. Leaching C. Increase Flowering, Yield VII. SUMMARY LITERATURE CITED

I. INTRODUCTION Most worldwide citrus production at least partially depends on irrigation for economic production (Shalhevet and Levy 1990). Irrigation is inevitably associated with the deterioration of water quality of run-off or ground water, especially due to increases in soluble salts. Poor water quality unavoidably leads to increased soil salinity. Excess salts from irrigation water must be removed from the root zone by leaching from rainfall or irrigation if agriculture is to be sustainable (Shannon 1997). Citrus trees, and most other fruit trees with the exception of date, pistachio, pomegranate, and perhaps olive trees (Gucci and Tattini 1997), are relatively sensitive to salinity stress. Unlike deciduous fruit trees, world citrus production is limited to a relatively small climatic belt where frosts are not too severe. The best citrus is produced, however, where winter cold is adequate to induce uniform flowering and the development of good fruit color. Human immigration to these mild-climate zones and concomitant urban development competes with citrus for both land and water resources. This trend began in Southern California and is now also evident in the citrus producing areas of Arizona, Texas, Florida, and the Mediterranean coasts. Increased consumptive use of water also results in the degradation of ground water quality all over the world (Jensen et al. 1990). In many coastal areas, demand for water exceeds the annual renewable supply and this over-exploitation of groundwater can lead to salt water intrusion into aquifers (Bosch et al. 1992). Any future rise in sea level may further threaten coastal ground water quality. However, salinization is caused not only by overuse of ground water, but also from slowing the

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rate of natural drainage to the sea. This process increases salts in ground water, that is already being replenished by increasingly saline irrigation water. Such salinization of the aquifer is not only limited to arid areas but is also evident in higher rainfall humid regions, such as parts of Florida, where salinity of well water increased at a rate of 12 mg L–1 per year (Calvert 1982) long before the more recent drought years. Urban requirements for high-quality water will ultimately require citriculture to depend on alternate poorer-quality water sources, including recycled wastewater and brackish water. The quality of domestic wastewater is also likely to deteriorate. Ironically, as water conservation reduces per capita domestic water use and increases water-use efficiency, effluent is diluted with less fresh water even though the total salt output may not change. The toxic ion content of domestic wastewater can be reduced by replacing the Na+ with K+ in water softeners and cleaning agents and also by limiting the use of boron (B) in cleaning agents. The quality of industrial wastewater can be improved by modifying industrial processes to use less-harmful pollutants. The amount of NO3– and/or NH4+ can be reduced by effluent treatment procedures. Soluble chlorides will continue to be a problem since it is not possible to significantly reduce Cl– in domestic effluent, nor is there an effective way of removing Cl– from solution apart from expensive desalination of wastewater. This review summarizes effects of irrigation water quality and salinity on citrus trees. We have tried to focus on cultural practices that are used to deal with poor-quality irrigation water, especially with respect to salinity, along with physiological responses of rootstocks and scions to salinity stress. Although this review concentrates on information that has become available since the review by Maas (1993), it was often necessary to review older work to develop the appropriate context in which to discuss experimental results. Conclusions about negative and positive aspects of salinity stress and their interaction with other environmental stresses are developed along with contrasting different experimental approaches in the laboratory, greenhouse, and field.

II. MANAGING SALINITY A. Irrigation and Salinity. All irrigation water contains salts; moderately saline water containing 200 mg Cl– L–1 will add 1000 kg Cl– ha–1 when applied at 500 mm per annum. If only part of that amount accumulates from year to year, soil

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will become non-productive. Even if the overall salt content does not increase from year to year because of adequate leaching, salinity may become high enough to cause damage during rain-free periods, between irrigations, or in portions of the soil that are inadequately leached. Leaching, of course, requires good drainage. In poorly drained soils, finetextured soils, or when the ground-water table is shallow, leaching requirements may necessitate the construction of an effective drainage system. The effects of irrigation and salinity on perennial tree crops are cumulative (Hoffman et al. 1989), particularly for citrus (Shalhevet and Levy 1990). In humid areas with high rainfall, injury symptoms on citrus trees from saline irrigation water may be transitory. However, even temporarily affected trees may remain stunted compared with trees not exposed to saline water, especially if young trees are salinity-stressed. The concentration of salts in a soil is a function of the total salts present and the soil water-content. Soil salinity is related to the electrical conductivity of standard saturated aqueous extract (ECe). Managing irrigation and fertilization with high-salinity irrigation waters requires routine monitoring of the electrical conductivity of the irrigation water (ECi) and ECe. If excess salts accumulate in the soil, it is best to keep the soil near field capacity moisture content so as not to further concentrate the salts. Without adequate rain, it may become necessary to apply irrigations with excess water in order to leach salts from the root zone (leaching fraction). The required frequency of leaching varies with the degree of salinization and evaporative demand. Leaching may be required no less frequently than every other week in some environments and irrigation must be excessive. Areas with compacted soils or poor drainage may need special attention when managing salinity, such as flood leaching or other ways to handle slow percolation and poor aeration. The method of irrigation and its interactions with the amount of rainfall throughout the season have important effects on responses of citrus trees to salinity. The amount of leaching depends on the amount of rainfall during the wet season and on the volume of soil wet by the irrigation water. Under dry summer conditions in Mediterranean climates, most of the active roots concentrate in the soil volume that is wet by the irrigation water since roots cease to develop at low soil temperatures when the soil is wet by winter rains. In summer-rainfall areas, however, roots grow beyond the irrigated zone. ECe measurement standardizes the amount of salts in the soil to conditions when the soil is saturated, but depending on soil moisture content, the actual salinity level in the vicinity of the tree roots may be several times greater than the ECe. In sandy soils where salts are easily

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leached, using ECe alone to evaluate soil salinity may not be sufficiently accurate. The ECe of these soils is only an indication of soil salinity at the time of measurement and can change rapidly following irrigation or rainfall. Without proper water and nutrient management, citrus irrigated with high-salinity water can suffer reduced growth and production. Salt concentrations in the soil solution can be monitored effectively with ceramic suction cups or soil salinity probes after proper calibration to approximate ECe (Boman 2000). Monitoring of soil solution is important where saline conditions may result from intentional deficit irrigation (Gonzalez-Altozano and Castel 1999) or from water-conserving irrigation scheduling based on soil moisture sensors (Boman et al. 2000) such as tensiometers or capacitance sensors (Fares and Alva 2000). When irrigation amounts do not exceed evapotranspiration, all the dissolved salts in the irrigation water that are not taken up by roots will remain in the root zone. Since the decreasing soil osmotic potential (Ψπ) reduces water uptake by roots, soil moisture sensors will indicate that the soil water content is high, thereby reducing the amount of water per irrigation. Such a scenario can result in a spiraling increase in soil salinization even with comparatively good-quality water. The soil ECe, which is linearly correlated to Ψπ, should be monitored to prevent such problems from developing. Microirrigation, especially drip irrigation, results in a relatively small soil volume that is routinely wet and leached by irrigation water. In arid climates, this comparatively small soil volume may be surrounded by a saline border and can be underlain by a salinized soil zone. Although drip irrigation can be beneficial for leaching salts away from localized root zones, a light rain may move the salts that accumulated on the surface or at the border of the wetted zone into the root zone. This necessitates the operation of drip irrigation (even during an initial rain event) until adequate rains have occurred to leach out accumulated salts. Salts can also accumulate in the periphery of furrows that are irrigated with saline water. 1. Irrigation Methods Gravity Irrigation. If adequate water is available, flood or basin irrigation can have an advantage over microirrigation due to the high downward movement of soil water. This leaching depends on soil permeability, drainage, and on the depth to ground water. The interval between irrigations is usually relatively long with these methods, so when the water tables are shallow, ground water salinity can affect soil salinity if the net flow of water is upward for a significant period of time in the absence

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of sufficient irrigation or rainfall to maintain downward water flow (Boman 2000). This method usually will depend on skilled labor to maintain uniform irrigation. Thus, basin irrigation is becoming less popular in new large-scale plantings because of the soil grading and skilled labor needed to maintain the system and because it requires a high volume of water. With good drainage, flood irrigation is still an excellent way to leach saline soils before planting. Furrow irrigation with saline water may cause salt buildup in the periphery of the wetted zone as mentioned above. The necessary soil grading, greater need for weed control, and skilled labor to operate such systems make it less feasible than other methods for many locations. Sprinkler. Overhead irrigation is still practiced in some parts of the world. This method requires comparatively high pressure, high volume, and good-quality water. If used with reclaimed water, there is also the hazard of biological contamination of the fruit. Citrus leaves easily absorb Cl– and Na+ from direct contact with water droplets (Eaton and Harding 1959; Ehlig and Bernstein 1959). Salt accumulation is a function of the evaporation rate, which increases the salt concentration of the water film on leaves. Damage can also develop from windblown salt water near the sea. Severe damage to leaves located in low canopy positions of under-thecanopy sprinkler-irrigated trees or in canopies of overhead-irrigated citrus has been described (Harding et al. 1958; Lundberg 1971; Nakagawa et al. 1980; Spurling 1981; Calvert 1982). Nighttime irrigation was recommended for overhead irrigation with comparatively high salinity (1200 mg L–1 TDS; Tucker 1978), since the accumulation of dissolved salts is greater from daytime than nighttime irrigation because of the different evaporative demand. Pulsed irrigation is dangerous, since salt absorption is greater from intermittent than from continuous wetting. The sensitivity of a citrus scion/rootstock combination to injury through direct foliar contact bears no relationship to its general tolerance to soil salinity that will be discussed later. Leaf Cl– and Na+ toxicity from direct contact with saline water has different symptoms from toxicity of Cl– that was absorbed by roots. Contact damage, consisting of burned necrotic, or dry-appearing tips on leaves, is one of the most common visible salt injury symptoms. In some cases, overhead irrigation, particularly at low humidity, will cause ring-shaped lesions on fruit where irrigation water evaporated. There are reports of Cl– and Na+ concentrations in leaves from low positions in the canopy that were about four times greater than those of the upper leaves (of grapefruit, ‘Valencia’ and ‘Washington

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Navel’ orange). The lowest concentration of either Na+ or Cl– generally associated with leaf burn is about 0.25% of leaf dry weight. Young trees (1–2 years) on ‘CTRM’ (see Table 2.1 for rootstock abbreviations) seem to be more susceptible to saline irrigation water spray and can develop brown “blisters” of dead tissue on their trunks (Boman 1999). Using overhead irrigation with poor-quality water for evaporative cooling (Brewer et al. 1979) during conditions of high evaporative demand can be especially dangerous and can lead to rapid concentration of the remaining salt solution on the leaves. Under-the-canopy sprinklers, especially microsprinklers, lessen the danger of salt damage to wetted leaves. The use of microsprinklers has become popular in Florida due to water-use restrictions, and because it prevents frost damage better than overhead sprinklers or drip irrigation (Boman and Parsons 1999). Microirrigation systems usually do not wet the entire soil volume. This occurrence is a benefit in arid climates, since more leaching of water usually occurs during irrigation of the limited volume and salts will not accumulate on the soil surface. However, the same increased leaching may also leach nutrients from the soil and increase nitrate concentration in ground water, especially in rainy areas with sandy soils.

Table 2.1. CARZ CLEO CTRM CTRN FA13 FA5 MACR RANG RL SB812 RT803 GT SO SwL SwO TRIF TROY VOLK X639

Abbreviations for names of Citrus and Citrus relatives. Carrizo citrange (C. sinensis [L.] Osbeck. × Poncirus trifoliata L.) Cleopatra mandarin (C. reshnii Hort ex Tan.) Swingle citrumelo (C. paradisi × P. trifoliata) citron (C. medica L.) Cleopatra mandarin (C. reshnii × P. trifoliata) Cleopatra mandarin (C. reshnii × P. trifoliata) Alemow (C. macrophylla Westr.) Rangpur lime (C. limonia Osbeck.) rough lemon (C. jambhiri Lush.) Sunki × Beneke (C. sunki × P. trifoliata L.) RANG × TROY [C. limonia × (C. sinensis × P. trifoliata)] Gau Tau (C. aurantium × ?) sour orange (C. aurantium L.) sweet lime (C. aurantifolia L.) sweet orange (C. sinensis [L.] Osbeck.) trifoliate orange (Poncirus trifoliata L) Troyer citrange (C. sinensis × P. trifoliata) Volkameriana (C. volkameriana Chapot) CLEO × TRIF (C. reshni × P. trifoliata)

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Drip. This irrigation method has become common in arid areas and Mediterranean climates. The popularity of drip is not only due to the water savings gained by reducing evaporative losses, but also due to the advantage of this system for irrigation with saline water that was described above. Successful use of a drip system depends on good water filtration and water treatment to prevent bacterial or mineral clogging. The utility of a drip system can be improved by fertigation. Dripper improvement and chemical prevention of root penetration into the drippers make underground drip systems feasible in citrus orchards. The advantage of this system over regular drip is that the water does not usually reach the surface, so it does not leave salts behind. This system is also advantageous when using reclaimed water that may be contaminated with harmful bacteria. Additionally, underground systems are less prone to damage from orchard operations and from pests like rodents or woodpeckers. Among the disadvantages of subsurface drip systems is the difficulty in monitoring the proper operation of the system. Also, if water does wet the soil surface by capillary action, salts may accumulate there. 2. Fertilizer and Salinity. The frequency of applying fertilizer has a direct effect on the concentration of total salts in the soil solution. A fertilization program that uses frequent applications with relatively low concentrations of salts will normally result in less salinity stress than programs using only two or three applications per year. As described above, light rain can aggravate salinity damage by the leaching of any residual dry fertilizer that was applied in the non-irrigated soil areas between the rows. Relatively expensive controlled-release fertilizers or frequent fertigations are ways to minimize salt stress when using highsalinity irrigation water. Selecting nutrient sources that do not add potentially harmful ions to already high levels in irrigation water can also avoid compounding salinity problems. The Cl– in KCl or Na+ in NaNO3 materials adds more toxic salts to the soil solution. Repeated fertilizer application with sources like (NH4)2SO4 can alter soil pH and cause soil nutrient imbalances. Specific ions can also add to potential nutrient imbalances in soil and trees. For example, Na+ can displace K+ and lead to K+ deficiencies. The displacement of Ca2+ by Na+ in the soil cation exchange complex can lead to decreased permeability and destroy soil structure. Such nutrient imbalances can compound drainage problems and aggravate the effects of salinity stress. Salinity problems can be minimized if sufficient soil nutrient concentrations are maintained, especially those of K+ and Ca2+. Preliminary results suggest that continuous application of nitrates like

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KNO3 under saline conditions can reduce Cl– accumulation in scions grafted on susceptible rootstocks, and can increase yield (Bar et al. 1996, 1997; Levy et al. 1999a, 1999c, 2002; Levy and Lifshitz 2000a, 2000b). This effect might be due to competitive exclusion of Cl– by NO3– at the soil-root interface, or, in young trees, a dilution effect due to increased growth. There are marked differences in the salt index (the salt content per unit nutrient) of particular formulations of fertilizer nutrients. Choosing nutrient sources with a relatively low salt index can reduce salinity problems from fertilizer salts. With high-salinity irrigation water, fertilizer formulations should have low salt index. It may be necessary to increase the frequency of fertilizations, thereby making it possible to reduce the salt content of each application and aid in preventing excess salt accumulation in the root zone. The nutrient storage capacity of citrus trees tends to buffer the different seasonal demands for nutrients associated with specific growth demands. Leaf or fruit analysis should be used to detect excessive Na+ and Cl– concentrations, or deficient concentrations of other elements caused by nutrient imbalances from salt stress.

B. Rootstocks and Scions 1. Rootstock Abbreviations. The abbreviations for different rootstocks (Table 2.1) are based on nomenclature of Hodgson (1967). 2. Salt Tolerance. It has been known for many years that citrus rootstocks differ in their ability to absorb the toxic ions, Cl–, Na+, and B, and to translocate ions to the canopy (Oppenheimer 1937; Cooper et al. 1951, 1952; Cooper and Gorton 1952; Cooper 1961; Embleton et al. 1973; Wutscher et al. 1973). Most of these studies were from short-term, comparatively high salinity trials, but results have been corroborated more recently for many rootstocks under field conditions (Levy and Shalhevet 1990, 1991; Garcia Lidon et al. 1998; Levy et al. 1999a,b,c). Because of the relative importance of Cl– toxicity in citrus (detailed below), salinity tolerance of rootstocks is most often based on the ability of the root system to limit the transport of Cl– to the leaves. In general, the decreasing order of salinity tolerance (most tolerant to most sensitive) in citrus rootstocks is: ‘CLEO’, ‘RANG’, ‘SB812’, ‘X639’, ‘GT’, ‘VOLK’, ‘SO’, ‘MACR’, ‘CTRM’, ‘RL’, ‘CARZ’, and ‘TROY’, ‘C35’ citrange, ‘CTRN’ (see Table 2.2 for details). The above ranking may differ somewhat, however, depending on the specific ions, effects of scion,

46 Table 2.2.

Ranking of rootstock tolerance to Cl– in different studies.

Susceptible

Medium

Tolerant

Scion

500

Reference

SwL

SO

CTRN>CTRM>RL

SwO>SO

CLEO>RANG

grapefruit

1800

Cooper and Gorton 1952

SO

CLEO

grapefruit

1200

Cooper et al. 1958

MACR>CARZ>TROY

SwL>SO>CTRM

CLEO>RANG>SUNKI

grapefruit

1200

Peynado and Young 1962

CARZ

CLEO

FA5=FA13

seedlings

4690

Forner et al. 2000

RL>TRIF

CARZ>TROY>SwO

RANG>CLEO>MACR

seedlings

1775

Grieve and Walker 1983

MACR

SO*

CLEO*

lemon

1490

Nieves et al. 1990

RL

SwO

Max Cl– Range

SO>CLEO

grapefruit

SO

VOLK

MACR

lemon

3550

Garcia Legaz et al. 1992

TROY

SO>CITR

CLEO

grapefruit

3400

Boman 1994

CARZ=TROY

RL

VOLK

seedlings

1147

Combrink et al. 1995

SO

CLEO

RANG>VOLK

seedlings

3000

El Hammady et al. 1995

SO

SB812

RT803>GT>CLEO

seedlings

1680

Levy et al. 1999

TROY

SO>SB812>GT

VOLK>RANG>CLEO

grapefruit

880

Levy et al. 2000

*SwO interstock

680

Oppenheimer 1937

Levy and Shalhevet 1990

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conditions of incompatibility, and with disease status (viruses, viroids, root infections, or pests). Many citrus rootstocks with low growth vigor have good Cl– exclusion characteristics, whereas some of the vigorous citrus rootstocks exhibit poor Cl– tolerance (Castle and Krezdorn 1993). Since faster-growing trees always use more water than slower-growing trees, leaves on highvigor trees would be exposed to relatively more Cl– in the transpiration stream from saline water than low-vigor trees. Thus, at least part of the mechanism underlying the accumulation of relatively low leaf Cl– in some citrus rootstocks may be related to their low growth vigor (Moya et al. 1999). However, there are many exceptions to this rule: ‘RANG’ is a fast-growing rootstock with good salt tolerance and ‘VOLK’, another fast-growing rootstock, exhibits some salt tolerance, at least as a young tree (Levy and Lifshitz 2000a). It is important to remember that due to osmotic effects, growth and yield of citrus trees can be reduced by excessive salts regardless of rootstock. The critical salinity level for salt damage varies with the buffering capacity of the soil (soil type, organic matter), climatic conditions, and the soil moisture status. Salinity-induced symptoms such as nonspecific chlorosis, smaller leaf size, and impaired shoot growth are often difficult to assess. Cl– toxicity can be diagnosed by leaf analysis (taking care to sample leaves that were not wet by irrigation water, when only a part of the canopy is wet by irrigation water) and at harvest time by juice analysis (Levy and Shalhevet 1990). Na+ toxicity symptoms such as tip-burn seldom distinctly appear. Boron toxicity symptoms are usually visible in leaves. Without leaf ion analysis, however, boron toxicity can be confused with other microelement deficiency or herbicide damage symptoms. Salinity interacts with many horticultural issues when choosing a rootstock. The comparatively high salinity tolerance of ‘SO’ and its other desirable horticultural characteristics make it a good rootstock to choose to cope with salinity problems. This fact places growers all over the world in a dilemma because trees grafted on ‘SO’ are susceptible to tristeza. Many tristeza-tolerant rootstocks such as ‘RL’, ‘TRIF’, ‘CARZ’, and ‘CTRM’ are sensitive to salinity. In addition, recent research indicates that drip-irrigated young trees on ‘SO’ may be more susceptible to salinity than mature trees (Hamou et al. 1999; Levy et al. 2000). A goal of many plant breeding programs is to develop a substitute rootstock for ‘SO’ that has similar growth, fruit quality, disease tolerance, and salinity tolerance, but is also tolerant to tristeza. Poncirus sp. and its hybrids are popular rootstocks in many areas but are susceptible to lime-induced chlorosis in calcareous soils. When

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salinity is also a potential problem, the grower is presented with an additional dilemma. Deficit irrigation can prevent lime-induced chlorosis (Levy 1998; Boman et al. 1999), but since these rootstocks are also very susceptible to salinity, it increases the hazard of salinity damage if leaching is reduced with reduced irrigation. The fact that rootstocks differ in their ability to extract water from saline soil affects the leaching pattern in the soil. For example, salinity stress increased N leaching (Lea-Cox and Syvertsen 1993). Since salinity reduces water use and transpiration differently in different rootstocks, rootstocks can actually affect soil salinity (Levy and Shalhevet 1991). Most of the breeding work done on citrus rootstocks is aimed at producing dwarfing and disease tolerance (tristeza, phytophthora, and nematode), but not for salinity tolerance (J. R. Furr and J. B. Carpenter, pers. commun. 1975; Hutchison 1985; C. M. Anderson, pers. commun. 2000; G. W. Grosser, pers. commun. 2001). Some new rootstocks have been evaluated for salinity tolerance. Rootstocks released by Forner et al. (2000) include ‘F&A13’ (‘CLEO’ × ‘TRIF’) that accumulated half the amount of Cl– compared with ‘CLEO’ and only 16% of the amount of Na when irrigated for 7 months with saline water in the greenhouse. The hybrid rootstock ‘FA517’ (C. nobilis Lour × ‘TRIF’), was similar to ‘CLEO’ and much better than ‘CARZ’ in the same experiment. Two other hybrids, ‘020324’ (‘TROY’ × ‘CLEO’) and ‘030131’ (‘CLEO’ × ‘TRIF’) were also noted as Cl– and Na+ excluders. ‘CLEO’, which is one of the best Cl– excluding rootstocks, was recognized as a salt-tolerant rootstock even though it was never selected intentionally because of its salt tolerance, but rather as an ornamental (Chapman 1968). Future research should evaluate citrus crosses that were produced in different parts of the world and evaluated for disease tolerance or cold hardiness (Hutchison 1985; Dunaway and Dunaway 1996). There is hope that crosses of ‘CLEO’ with ‘RANG’ or ‘VOLK’ or even ‘TRIF’ may produce a rootstock that is better than ‘CLEO’ in terms of salt tolerance, vigor, and yield. Another direction to take may be to try to induce beneficial mutations in ‘CLEO’. 3. Ranking of Salinity Tolerance. Table 2.2 summarizes the Cl– tolerance ranking reported in different studies during the last seven decades. 4. Effect of Scion Cultivars. Just as growth and yield responses of citrus scions and rootstocks differ in sensitivity to salinity (Cooper et al. 1951, 1961; Levy 1986, 1997; Levy and Shalhevet 1990, 1991; Levy et al. 1992, 1999a,b; Levy and Lifshitz 2000a), there are scion differences in salt sensitivity of leaf gas exchange physiology that may be attributed to genetic

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differences. Net gas exchange of CO2 in ‘Marsh’ grapefruit leaves was more sensitive to salt stress than in ‘Navel’ or ‘Valencia’ orange regardless of the rootstock on which they were grafted (Lloyd et al. 1990). This observation was attributed to the higher accumulation of Na+ in grapefruit leaves than in orange leaves even though grapefruit leaves also accumulated the most Cl–. However, salinity experiments with mature grapefruit and ‘Washington Navel’ oranges also indicated that grapefruit growth and yield were more susceptible than orange to salinity (Levy and Shalhevet 1991). In this case, salinity effects were manifested by Cl– accumulation in the leaves and yield reduction of grapefruit grafted on salt-sensitive ‘RL’ (Levy and Shalhevet 1991; Levy et al. 1992). There are also differences in the susceptibility of different citrus scions to salt damage from overhead irrigation. Similar to the report above, ‘Marsh’ grapefruit had more leaf damage than ‘Temple’ or ‘Valencia’ orange trees when irrigated with water containing 2800 mg L–1 total salts (about 1000 mg Cl– L–1; Calvert and Reitz 1965). This may be related to differences in cuticular permeability to Cl–, as well as to the sensitivity of the different cultivars to salinity. Such genetic differences of scion types may also be attributable to different sensitivities to Cl– or to an ability of salt-tolerant types to compartmentalize toxic ions in the vacuoles away from the physiologically active cytoplasm. However, x-ray analysis could not detect such compartmentation in citrus under salinity stress (M. Talon, pers. commun. 2001). It is interesting to note that leaves containing high Cl– levels from saline foliar sprays did not have the same reductions of photosynthetic assimilation of CO2 that would be expected from similar leaf Cl– levels that accumulated from salinized soil (Romero-Aranda and Syvertsen 1996). Future research should focus on such potential differences (and others) with a goal to achieve an understanding of the underlying mechanisms of salinity tolerance. This understanding may lead to breeding salt-tolerant scions that will continue to yield commercial crops in spite of Cl– or Na+ accumulation in their leaves. Breeding of such halophytic-like cultivars, however, seems to be a distant prospect today (Yeo 1998; Barkla et al. 1999).

III. EXPERIMENTAL METHODS IN SALINITY RESEARCH Reliable data on the yield response of citrus or any other commercial crop to salinity can be obtained only from carefully controlled and wellreplicated field experiments conducted across a range of salinity treatments (Shannon 1997). Tests should include mature yielding trees during a long time span (years) in order to evaluate possible cumulative

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effects of salinity on tree development and yield. Such experiments are expensive and thus rare (Hoffman et al. 1989). Young seedlings often provide indications as to the anticipated response of the trees to salinity and, as such, seedlings as early indicators may be tools in testing new breeding materials and cultural practices even though in many cases they may fail as rootstocks for mature trees. A. Leaf Analysis Leaf analysis was developed as a tool for assessing the nutritional needs of citrus. Some of the standards developed in Riverside, California (Chapman 1968; Embleton and Jones 1964; Embleton et al. 1973) were based on hydroponics along with some actual nutrition field experiments and field observations. The work of Cooper et al. (Cooper et al. 1951, 1955; Cooper and Gorton 1952; Cooper 1961) also contributed to the establishment of tolerances for Cl–, Na+, and B concentrations in citrus leaves. There are some disadvantages in using leaves for assessment of salt accumulation. Mineral concentrations depend on leaf age, so leaves should be sampled carefully to ensure that they are of the same age (Embleton et al. 1962a). Leaves exposed to saline irrigation water may absorb salt directly through the epidermis (Stolzy et al. 1966) or have non-washable salt residues adsorbed on the leaf surface. Therefore, leaf analysis may not always be indicative of ion uptake by roots. Another serious problem is the tendency of leaves most affected by salinity to abscise before the usual summer/autumn sampling date, resulting in the sampled leaves not being representative. B. Juice Analysis Juice analysis can give a better ranking of the susceptibility of citrus rootstocks to salinity (Levy and Shalhevet 1990; Levy et al. 1992, 2000; Levy and Lifshitz 1995, 2000a). Juice analysis has several advantages over leaf analysis. A much more uniform tissue is used and the sample can be much larger. There can be 3 to 6 kg fresh weight of fruit per juice sample vs. about 50 g for leaves. As a rule, in most citrus cultivars (except summer lemon) all the fruits are of a similar calendar age and it is easy to eliminate surface contaminants from the juice. There is no need for extensive preparation of juice samples for analysis since fresh citrus juice can be analyzed directly for Cl–, Na+, and K+. Analysis results can be obtained shortly after the juice is extracted (Levy and Shalhevet 1990). The concentration of Cl– and particularly Na+ in juice is often lower than that of

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tap water, so care should be exercised to prevent contamination of juice with tap water during juice extraction. Since variability is lower than with leaf analysis, juice analysis can give a better ranking on the uptake of Cl– and Na+ by the different rootstocks (Levy and Shalhevet 1990; Levy et al. 1992, 2000; Levy and Lifshitz 1995, 2000a). C. Seed Mineral Content Seed tissue of eleven citrus species revealed significant differences in Cl– concentration calculated on a dry weight basis (Altman and Goell 1970). This result correlated well with the Cl– concentrations in the leaves of the same plants. However, there was no significant difference in Cl– concentrations of seeds from 10-year-old ‘Clemantine’ mandarin grafted on different rootstocks and watered with non-saline water. Increasing the Cl– concentration of irrigation water from 130 to 1800 mg L–1 did not affect the Cl– concentration of the seeds of ‘Shamouti’ orange trees grafted on salt susceptible ‘Palestine SwL’ rootstock. Thus, it does not appear that seed Cl– concentrations can be a reliable indicator of salinity tolerance, nor is it conveniently sampled tissue. D. Biochemical Indicators An intriguing possibility is to identify an indicator of membrane permeability to Cl– and, thus, an indicator Cl– tolerance. Treatment with high salinity increased free sterols in the young fibrous roots of salttolerant ‘RANG’, and reduced free sterols in the non-tolerant ‘Kharna khatta’ rootstock of India (C. karna Raf.) (Douglas and Walker 1983). A significant correlation was found between the ratio of the “more planar” cholesterol and campesterol to “less planar” sterols in the free sterol fraction. In the absence of salt stress, this ratio was lowest in ‘RANG’, intermediate in ‘Kharna khatta’, and highest in ‘Etrog’ citron, correlating to their Cl– exclusion. This finding was interpreted as a potentially useful indicator of membrane permeability of the different genotypes. Another study suggested that the phospholipid to free sterol ratio could be used to assess Cl– exclusion ability in citrus (Douglas and Sykes 1985). Unfortunately, these studies have not been continued. E. Seed Germination Salinity reduces seed germination initially through the osmotic effect of the solution, but there was no evidence that the tolerance to salinity during germination was correlated with the tolerance of the plant to

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salinity (Zekri 1993). This finding was confirmed in a recent study (Zekri 2001). ‘CARZ’, which is a Cl– accumulator, was the first to germinate at high salinity, ‘SO’ the last, and ‘CLEO’, the best Cl– excluder, was intermediate. The author suggested that stem analysis of seedlings germinated at high salinity could serve as an indicator of Cl– tolerance. F. Solution Culture vs. Soil Culture Much of the early work on the salt tolerance of citrus rootstocks to salinity was based on hydroponics or sand culture. These studies ranked ‘RL’ and ‘SO’ as moderately tolerant to salinity (Cooper et al. 1952; Bernstein 1969, 1980). Later, under field conditions, it was found that ‘SO’ could tolerate salinity (Bielorai et al. 1983, 1985) and that ‘RL’ was much more sensitive to salinity than ‘SO’ (Shalhevet and Levy 1990; Levy and Shalhevet 1990, 1991). Thus, ion uptake by roots in solution culture can be different from that by roots growing in soil. Irrigation method can also interact with the response of field-grown rootstocks to salinity (Wutscher et al. 1973). Roots growing in an aqueous environment encounter entirely different solute gradients than roots in soil. In soil, the mass flow of solution toward the root by transpiration is much greater than the diffusion away from the root unless there is continuous leaching of salts by rainfall or irrigation (Yeo 1998). If a root in soil excludes Na+ or Cl– ions, they will not move away from the root. Thus, roots may actually increase soil salinity by salt exclusion. In addition, salinity-tolerant citrus rootstocks can increase the soil salinity because they do not limit water uptake as salinity increases compared with non-selective rootstocks (Levy and Shalhevet 1991). This condition is very different from flowing or stirred hydroponic solutions. In this respect, sand culture may be similar to hydroponics since sand is usually frequently irrigated with an excess of nutrient solution. Roots also interact with soil microflora such as vesicular arbuscular mycorrhizae (VAM), that are missing in water culture and may be altered or absent in sand culture. Roots develop a different anatomy when grown in solution-culture than when grown in soil. In addition, since nutrient solutions have different aeration and usually a different pH than the soil, salinity responses of solution culture plants are usually different from that of trees in soil. There are examples, however, of short-term, high-salinity hydroponic culture of citrus hybrids where leaf analysis was coupled to plant development and gave a rapid indication of their possible Cl– tolerance when used as rootstocks under real field situations (Sykes 1985).

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G. Seedling Rootstocks vs. Budded Trees The majority of commercial citrus trees are composed of a rootstock and a scion, which are two different Citrus (or Poncirus) species or their hybrids. Exceptions may be lime trees (C. aurantifolia L.) that are vegetatively propagated from cuttings or ‘Emperor’ (‘Empress’) mandarin trees grown as seedlings. The rootstock develops the root system that absorbs water, nutrients, and salts from the soil; the scion develops the branch system and leaves, transpires water, fixes CO2, flowers, and develops the fruit. It is the scion that suffers most from the stress caused by salinity. Many rootstocks behave differently when scions are budded on them than when grown as unbudded seedlings. For instance, ‘MACR’ as a rootstock produces a large and prolific tree for virus-free scions in Israel (Levy et al. 1980; Levy and Lifshitz 1995), Arizona (Fallahi and Rodney 1992; Wright 1999), and Spain (A. Garcia Lidon pers. commun. 2001), but on its own roots, ‘MACR’ will remain a relatively small tree with only a few fruit. To have practical significance, studying physiological processes in un-budded rootstock seedlings should be augmented by studies with grafted scions in order to distinguish between the effect of the rootstock as a root system and the possible effects of shoot anatomy and physiology. Shoot and leaf characteristics of a seedling of a rootstock species have no practical significance once it is grafted. Physiological responses of shoots and leaves (including photosynthetic responses) of rootstock seedlings, however, can yield valuable information about physiological functions of the root system that can have practical significance for understanding underlying mechanisms in the root systems of commercial trees. The compound genetic system of a citrus tree presents other potential complications that do not occur in seedlings. The specific scion can influence ion uptake by the rootstock (Cooper et al. 1952). The budunion itself may affect the transfer of nutrients and toxic elements from root to canopy. This is especially true of some specific rootstock/scion combinations that are partially incompatible. In addition, the bud-union is the part of the grafted tree that may be first affected by several virus diseases, further complicating the response of the whole tree to the environment variables.

H. Greenhouse vs. Field Studies Most of the knowledge about the salinity tolerance of rootstocks comes from water-culture or container experiments. These experiments are usually short-term, and comparatively high salinities are used in order

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to measure results quickly. Often the response of mature, grafted trees was different from that of young seedlings in pots (Levy et al. 1992). As with seedlings vs. budded tree studies, pot experiments with confined root systems should be corroborated in long-term orchard experiments before recommendations based on results are adopted in commercial practices. Obviously, long-term field experiments are more difficult and less common than shorter-term pot experiments in fruit trees (Hoffman et al. 1989). I. Tissue Culture vs. Whole Plant Much of our physiological knowledge at the molecular level comes from bacterial or animal systems, which are very different from whole plants. Animal cells and respiring plant tissues absorb O2 and release CO2. The O2 concentration in air is about 21%, while the CO2 that the green plant tissues combine with water to make sugars is only present at a concentration of about 0.03%. Plant leaves unavoidably transpire a relatively huge volume of water while acquiring CO2 for photosynthesis. Plant cell suspensions do not transpire and in vitro plants from tissue cultures transpire very little water, so there is relatively little exchange of water and ions with their environment. Toxic ions that are not absorbed by cell or tissue cultures will remain uniformly distributed in the culture media and not accumulate in the media near cells (Yeo 1998). This situation is very different from the accumulation of excluded ions in the rhizosphere of roots growing in soil. Thus, in vitro cultured cells and tissues can tolerate much higher external salinity in the media than a transpiring plant growing in soil. Variant cell lines selected from cultured somatic cells can exhibit a level of tolerance to salinity (Ben Hayyim and Kochba 1983; Ben-Hayyim and Goffer 1989; Kochba et al. 1982). As stated by Kochba et al. (1982), the salt tolerance of selected cell lines will be of agronomic value only if the tolerance achieved is maintained in all stages of plant development. The major limitation of tissue culture is that the selected salinity tolerance character often cannot be maintained during the regeneration process and tolerance mechanisms that depend on the integrated function of the differentiated tissues cannot readily be identified in cell culture (Shannon 1997; Yeo 1998). Thus, salinity tolerance for terrestrial agriculture is a whole plant function that can best be studied in intact plants in the field. Induction of natural genetic mutations may offer improvements in salinity tolerance. Flowers and Yeo (1995) state that mutation works best with factors likely to be controlled by a single gene. Tolerance to abiotic stresses is usually a function of a group of complex quantitative genetic

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characters and, thus, very few successes have been reported in breeding plants with increased stress tolerance. Garcia-Agustin and Primo-Millo (1992, 1995) treated unfertilized TROY ovules with the mutagen ethylmethyl-sulphonate, and selected three lines that accumulated little Cl– and Na+ along with high concentration of K+ in leaves when subjected to increasing NaCl in the culture medium. However, two of the selected lines partially lost this characteristic when they were vegetatively propagated from cuttings and grown in the absence of saline selection pressure. Since only a true mutant continues to carry a stable trait in the absence of selection pressure (Garcia-Agustin and Primo-Millo 1992, 1995), these lines apparently were only phenotypically acclimated to salinity and lost this characteristic when propagated. Cervera et al. (2000) transformed plants of ‘CARZ’ with the halotolerance gene HAL2, which confers Li+ and Na+ tolerance in yeast and so was implicated in salt-tolerance mechanisms. The transgenic nature of these plants was confirmed by Southern and Northern analyses, and was the first time that a gene from yeast had been stably integrated and expressed in citrus plants. However, when whole plants were tested in the greenhouse, the transformed ‘CARZ’ plants did not differ in their susceptibility to salinity from control ‘CARZ’ plants (L. Peña and M. Talon, pers. commun. 2001). These contrast with results with tomato plants that were transformed with the HAL1 gene from yeast (Gisbert et al. 2000), which reduced both root and leaf Na+ and increased K+. Cervera et al. (2000) concluded that salt tolerance is a multigenic and quantitative trait, and both improvement and evaluation of this characteristic is difficult. This is especially true for Cl– toxicity tolerance in citrus, which is not well understood and apparently is not governed by a single gene. Introduction of transgenic genes for salinity tolerance into commercial rootstocks or preferably directly into commercial scion cultivars could result in the production of “halophytic” citrus. This prospect seems remote at the present time due to our lack of basic knowledge about salinity tolerance in citrus. However, progress is rapid in yeast molecular genetics for improvement of salt tolerance in plants (Matsumoto et al. 2002) and a breakthrough is possible.

IV. PHYSIOLOGICAL RESPONSES A. Amino Acids Accumulation Non-protein amino acids like proline, often reported as a stress metabolite, increase with drought stress (Levy 1980; Yelenosky 1979) and also with salt stress (Dunn et al. 1998). Proline has been reported to have a

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role in stressed plants (Syvertsen 1984; Syvertsen and Smith, Jr. 1984), where it acts as an osmoticum and/or a storage source of N. Arginine concentration in ‘VOLK’ feeder roots (percent of total amino acids) was doubled by salinity, while phenylalanine ammonia lyase (PAL) was reduced (Dunn et al. 1998). These may reduce the chemical defenses of the plant to nematodes as discussed below. Free proline increased with salinity in the leaves of lemon grafted on the relatively salt-tolerant ‘SO’, but not when grafted on the more salt-susceptible ‘MACR’ (Nieves et al. 1991). In another study (Walker et al. 1993), proline increased significantly only in lemon leaves on ‘RANG’ exposed to Na2SO4 but not when irrigated with NaCl. Its increase with salt stress supports its role in stressed plants where it acts as an osmoticum. Betaine levels in leaf tissues of ‘CARZ’ were also positively related to soil salinity (Duke et al. 1986). These compounds are considered as osmo-protectants, which may be “engineered” into citrus for better total salt (osmotic and drought) tolerance (Nolte et al. 1997) but not for reduction of specific mineral toxicity. B. Net Gas Exchange of Leaves There have been several studies comparing stomatal conductance (gs) and photosynthetic assimilation of CO2 (ACO2 ) in leaves from salinized trees with gas exchange values from non-salinized controls. It is clear that salt stress reduces water use and ACO2 but the underlying mechanisms are still debatable. Much of the controversy surrounding salinityinduced limitations on net gas exchange follows the same argument as the relative importance of osmotic stress vs. toxic ion stress of Na+ and Cl–. Osmotic stress from saline soils undoubtedly reduces water use and gs, but the magnitude of this reduction depends on the rate at which salinity stress develops and the duration over which it exists. Leaf proline concentration (Syvertsen and Yelenosky 1988) and proline-betaine levels (Lloyd et al. 1990; Banuls and Primo-Millo 1992) increased with salinity-induced osmotic stress. Potentially negative osmotic shock effects on plant-water relations usually do not occur if there are ample cations available to gradually allow leaf tissues to lower osmotic potential (Ψπ) to compensate for losses of turgor. For example, long-term moderate salinity stress lowered leaf Ψπ such that turgor was maintained and leaves suffered little or no drought stress-like symptoms (Syvertsen et al. 1988). Turgor can be even higher in salt-stressed trees than in nonstressed control trees (Behboudian et al. 1986). This is why controlled salinity studies often gradually build up salt concentrations in the irrigation water to avoid osmotic shock and defoliation.

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Patterns in gs usually follow patterns in ACO2, which has caused some researchers to mistakenly link declines in ACO2 to salinity-induced reductions in gs. This speculation is probably not the case, however, since low gs probably only directly limits ACO2 at very low leaf water potential (Ψw) or at large vapor pressure deficits (Farquhar and Sharkey 1982). In most cases, including moderate salinity stress, changes in ACO2 cause changes in gs. Lloyd et al. (Lloyd and Howie 1989b; Syvertsen and Lloyd 1994) examined effects of salinity on the relationship between ACO2 and internal CO2 concentrations and concluded that reductions in ACO2 were due to a direct biochemical inhibition of mesophyll photosynthetic capacity followed by reductions in gs. Thus, other than osmotic shock responses, most decreases in net gas exchange attributable to salinity are probably caused by ion toxicity responses. Since the most common source of salt stress is NaCl and both ions often accumulate together, it is difficult to determine the relative importance of Na+ vs. Cl– ions in reducing ACO2. There are many reasons why decreases in the net gas exchange of leaves in response to salinity are complicated by salinity-induced variations in leaf nutrition and by leaf chlorophyll. Increases in leaf Na+ interact with Ca2+ and K+, whereas leaf Cl– interacts with the anions NO3– and SO42–. Many problems associated with toxic levels of Na+ are probably due to deficiencies of K+ and Ca2+. These deficiencies explain why salinity effects can be ameliorated with Ca amendments (Cooper et al. 1958; Banuls et al. 1991; Banuls and Primo-Millo 1992). Ca2+ amendments also help remove Na+ from soil colloids and free Na+ to be leached. There can also be direct effects of leaf Cl– on other ions. For example, high Cl– reduces N uptake (Syvertsen et al. 1993) and decreases NO3– N use efficiency (Lea-Cox and Syvertsen 1993). There are direct effects of salinity on leaf chlorophyll concentrations that are reflected in variations in ACO2. In the field or in high-light greenhouses, leaf chlorophyll concentration usually decreases with salinity stress in well-watered trees (Syvertsen et al. 1988; Romero-Aranda et al. 1998). Interestingly, surviving leaves from drought-stressed salinized trees did not suffer losses of chlorophyll. In low-light growth chamber studies, however, leaf chlorophyll is affected little by salinity (Lloyd et al. 1987a) and can even be higher in salinized leaves than in nonsalinized control leaves (Lloyd et al. 1987b). Several studies describe decreases in citrus leaf ACO2 in response to elevated leaf Cl– (Syvertsen and Lloyd 1994; Storey and Walker 1999). Although citrus has been considered to be sensitive to Cl– toxicity, Syvertsen et al. (1988) found no effect of salinity on gas exchange of remaining leaves on ‘Valencia’ orange trees on both ‘SwO’ and ‘TRIF’ rootstocks despite foliar concentrations (cell sap basis) of Cl– as high as

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400 mol m–3 (mM). These trees had already sustained some salinityinduced defoliation such that whole tree-water relations were dramatically affected. Defoliation can actually increase ACO2 of the surviving leaves (Syvertsen 1994; M. Talon, pers. commun. 2001). As leaf canopies became thinner, salinity responses of retained leaves were affected little. The inhibition of citrus leaf photosynthesis by high Cl– concentrations (Walker et al. 1982; Lloyd and Howie 1989a) appears especially prominent when rates of Cl– entry into foliage are rapid. If rapid salinity stress in the field induces leaf abscission, physiological responses to salt stress can only be characterized in the remaining relatively young leaves, that have relatively low concentrations of Cl–. This occurrence can lead to a misinterpretation of the relative importance of leaf Cl– relative to leaf Na. Nonetheless, high correlations between net gas exchange and salinity in two orchard sites in Australia (Syvertsen et al. 1988; Lloyd and Howie 1989a) were attributed to a Na+ rather than a Cl– effect on citrus leaf gas exchange. Reductions in ACO2 can be attributed to high Na+, especially when there are relatively low Ca and K+ concentrations in leaves. Although leaf injury can be correlated with Cl– concentrations, studies have shown that reductions in ACO2 depend on the relative sensitivity of the scion type rather than on the absolute concentration of Na+ or Cl– (Banuls and Primo-Millo 1995). Salinity caused a progressive loss in variable fluorescence under strong irradiance. Adaxial (upper) surfaces were especially vulnerable to this apparent photoinhibitory damage, which coincides with the apparent bronzing that is typical of Cl toxicity. Predawn increases in maximal fluorescence correlated with leaf Cl– (Lloyd et al. 1986). Rootstock differences in Cl– exclusion characteristics also are reflected in salinity effects on ACO2 (Lloyd et al. 1987a,b). ‘Valencia’ orange trees on TRIF rootstock had a less rapid decline in leaf gas exchange when exposed to 1775 mg Cl– L–1 (50 mol m–3) NaCl than did equivalent foliage on ‘CLEO’ despite much higher Cl– concentrations in leaves on scions budded to ‘TRIF’. Although this rootstock effect was attributed to higher Na+ levels in scion foliage budded on ‘CLEO’, underlying levels of leaf Cl– were much higher in trees on ‘TRIF’ than in those on ‘CLEO’. In spite of high levels of Na+ in NaNO3 treated leaves, there were no reductions in ACO2 that could be attributed to Na+ (Banuls et al. 1997). C. Salinity Interactions with Physical Environmental Factors 1. High Temperature and Evaporative Demand. There are direct interactions between salinity, leaf water relations, irradiance, leaf temperature, and atmospheric evaporative demand that are impossible to

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separate in the field. Physiological mechanisms underlying environmental interactions with salinity can only be studied in controlled environments. Such studies may provide insights into cultural practices or environmental conditions that can improve production under salinity stress. Citrus leaves growing in full sun can experience temperatures that exceed air temperature by as much as 10°C (Syvertsen and Albrigo 1980). Leaf temperatures up to 45°C not only exceed optimum temperature for photosynthesis, but also lead to large vapor pressure differences (VPD) between leaves and air. Since citrus stomata are sensitive to evaporative demand, a large VPD can reduce gs and ACO2. Transpirational water use is also a function of VPD, and large VPDs can result in very low water use efficiency (WUE). Decreasing VPD by lowering leaf temperature or increasing humidity can increase gs, ACO2, and WUE. Misting tree canopies with high-quality water may improve salinity tolerance and decrease accumulation of toxic ions as found in tomatoes (RomeroAranda et al. 2001). Since salinity stress is greater for sun-exposed than for shaded leaves, additional shade may improve salinity tolerance. Artificial shade screens during the warmest season reduced citrus leaf temperature and improved WUE (Jifon and Syvertsen 2001) and likely would decrease salt stress. 2. Elevated CO2. Growing plants at elevated CO2 usually increases growth and ACO2 but at the same time, high CO2 decreases stomatal conductance. Elevated CO2 almost always leads to higher WUE, so it can disconnect rapid tree growth from high water use. Thus, elevated CO2 offers a tool to study mechanisms of salinity tolerance. If salt uptake is coupled with water uptake, then leaves grown at elevated CO2 should have lower salt concentrations than leaves grown at ambient CO2 (Ball and Munns 1992). In greenhouse studies using twice ambient elevated CO2, all citrus rootstock species studied increased growth and WUE in response to CO2, but ‘RANG’ and ‘CLEO’ were less affected by salinity stress than were ‘SO’ and ‘SwO’ (Syvertsen and Grosser, unpublished). Generally, the salinity-induced accumulation of Na+ in leaves was less when seedlings were grown at elevated CO2 than at ambient CO2, implying that the lower Na+ accumulation was linked to increased WUE. Na+ accumulation, however, was unaffected by elevated CO2 in ‘RANG’. In addition, ‘RANG’ also had the lowest leaf Cl– concentrations. The accumulation of leaf Cl– in salinized ‘SO’ was greater at elevated CO2 than at ambient CO2. Cl– concentrations were less at elevated CO2 in ‘CLEO’, but unaffected by CO2 in ‘RANG’. The decrease in Cl– accumulation at elevated CO2 in ‘CLEO’ was related to the increase in WUE, whereas the

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increase in leaf Cl– in ‘SO’ was not. Thus, relationships between salt ion accumulation and water use differed depending on the specific ions and citrus species. The growth increases in response to elevated CO2 in salt-tolerant ‘RANG’ were less under salt stress than without salt stress and there was little interaction between CO2 level and salinity for growth responses of ‘SO’ and ‘CLEO’. Seedlings of these three Citrus species, therefore, differed from other C3 non-halophytic species in which the enhancement of growth in response to elevated CO2 was greater when plants were exposed to salt stress (Ball and Munns 1992). Non-salinized plants were relatively less responsive to elevated CO2 than salt-stressed plants because non-salinized plants were growing near their maximum growth capacity, whereas salt-stressed plants had a greater potential for growth. This result differed for relatively slow-growing, salt-tolerant ‘SO’ and ‘CLEO’, where growth was enhanced by elevated CO2 similarly at high and low salinity (Syvertsen and Grosser, unpublished). In ‘RANG’, the adverse effects of salinity on growth were worse at elevated CO2. Thus, the salinity tolerance of ‘RANG’ may be reflected in the near maximum growth response of salinized seedlings at elevated CO2, whereas nonsalinized seedlings at elevated CO2 may have a greater potential for growth. D. Osmotic Stress Salinity affects citrus in two ways: osmotic stress and toxic ion stress. Dissolved salts exert an osmotic effect that reduces the availability of free (unbound) water through physical processes. This situation is analogous to drought stress and is discussed in detail below. The effect of osmotic stress is different when stress increases gradually and the plant can adjust to it compared with the situation when the Ψπ of the soil solution decreases abruptly. 1. Gradual Osmotic Stress. The osmotic effect from dissolved salts in the soil solution reduces the availability of free (unbound) water through the physical processes of lowering the energy of the soil solution. More free energy is required to overcome the lower Ψπ exerted by salts in solution, so there is less water available to roots. The energy required for roots to extract that water is referred to as osmotic stress. Osmotic stress can result in a reduction in root growth followed by a decline of canopy development and yield. When salinity stress is gradual, salt-tolerant rootstocks, that limit the translocation of the toxic ions Cl– and Na+ into the leaves, will acclimate

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to the lower Ψπ in the root zone by closing stomata and reducing transpiration (Syvertsen and Smith, Jr. 1983; Nieves et al. 1991). Ψπ can decrease in the plant by accumulating sugars and other osmoticum such as proline (Banuls and Primo-Millo 1992). Under saline conditions, Ψw reached values near –1.8 MPa. This reduction was offset by a decrease in the leaf Ψπ so that turgor was maintained at or above control values. The changes in Ψπ were closely correlated with changes in leaf proline concentration (Syvertsen and Smith, Jr. 1983; Rabe 1990; Eissenstat 1998; Nolte et al. 1997). Under osmotic stress caused by high nutrient concentrations (Syvertsen and Yelenosky 1988), ‘CLEO’ accumulated more proline than ‘SwO’ and ‘TRIF’ seedlings. This response may contribute to the relatively high tolerance of ‘CLEO’ to salinity. Enhanced accumulation of proline was considered to be a good indicator of superior salinity stress tolerance in breeding programs (Deng et al. 1993; Nolte et al. 1997), especially if the new lines also limit the uptake of Cl– and Na+. 2. Osmotic Shock. Osmotic shock can occur from excessive fertilization and from a drastic increase in water salinity in the soil solution. A rapid shock can occur as a result of light rain leaching accumulated salts into the root zone. The first apparent symptom of such an osmotic shock is abrupt leaf abscission, which may occur within days after the rain event or application of the salt. Typically, the lamina (leaf blade) separates at the abscission zone between the lamina and the petiole. The petiole may remain green and attached to the stem for some time. Leaf analysis of the abscised leaves may not reveal an increase in their Cl– or Na+ content. Such leaf drop can be prevented by irrigation during the initial rain period until sufficient rain leaches the previous accumulated salts. Similar leaf abscission is common for situations of sudden drought stress such as that caused by desiccating winds (Schneider 1968). Typically, citrus leaves will not abscise during drought but abscise only when irrigation (or rain) follows a severe drought. Ethylene production may be involved, since elevated ethylene is produced within 2 hours after rehydration (Tudela and Primo Millo 1992). Osmotic shock, induced either by a sudden salt increase or severe drought stress, increased abscisic acid (ABA) and aminocyclopropane1-carboxylic acid (ACC) in roots, xylem fluid, and leaves (GomezCadenas et al. 1996, 1998). Under salinity, the pattern of change of ABA, ACC, and proline followed a two-phase response: an initial transient increase (10 to 12 days) overlapping with a gradual and continuous accumulation. This biphasic response appears to be compatible with the proposal that the transitory hormonal (ethylene) rises are first induced

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by the osmotic component of salinity and then by Cl– accumulation (Gomez-Cadenas et al. 1998). Thus, osmotic shock induced ABA, ethylene production, and leaf abscission. E. Toxic Ions In addition to osmotic stress, part of the salt sensitivity in citrus is related to the specific toxic effects of accumulation of Cl–, Na+, B, and other ions in leaves (Bernstein 1980). One of the main differences between the effect of salinity on annual plants and trees is the gradual accumulation of toxic elements in the leaves and other plant parts in trees. These elements are transported by the transpiration stream and remain in the plant after transpired water has evaporated. 1. Chloride. Chloride toxicity in woody species is generally more severe and observed in a wider range of species than is Na+ toxicity (Shannon 1997). Citrus provides a good example. Since Cl– ion is more toxic to citrus than Na+, the concentration of Cl– in water is an important parameter in deciding the suitability of water for citrus irrigation (Bernstein 1980; Shalhevet and Levy 1990; Levy and Shalhevet 1991; Levy et al. 1992; Maas 1993; Storey and Walker 1999). Cl– can reduce leaf chlorophyll concentration (Zekri 1991), and cause bleaching or bronzing of sunlit leaves. There is ample evidence that Cl– can reduce photosynthesis in citrus leaves as discussed previously. Under warm, dry, summer conditions in Australia, a yield decrease of about 20% was calculated for each increase of 35.5 mg L–1 (1 mol m–3) of Cl– concentration in the irrigation water above a threshold concentration of about 152 mg L–1 Cl– (4.3 mol m–3). The yield decrease was attributable to Cl– toxicity rather than osmotic stress (Cole 1985). A similar negative correlation was found between leaf Cl– and yield under similar climatic conditions in Israel (Levy et al. 1992). 2. Sodium. Na+ is a toxic element that is perhaps a greater salinity problem in other plant species than it is in citrus. The significance of Na+ toxicity in citrus and other fruit trees is often overshadowed by the effect of Cl–. Na+ can be harmful through its effect on the absorption of other nutrients, especially K+. The amount of Na+ found in citrus leaves and juice is comparatively low; in lemon juice, it amounts to 0.1 g kg–1 fresh weight compared with 10 g kg–1 for K+ and 6 g kg–1 for Ca++ (Sinclair 1984). The application of NaNO3 was compared with Ca(NO3)2 for 9 years. The NaNO3 increased leaf Na+ concentration from 0.1 to 0.2 g kg–1 and reduced the yield of ‘Washington Navel’ orange by 25%. In the

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same experiment, feeder root Na+ concentration increased from 0.2 to 0.7 g kg–1. However, it is not clear if all the Na+ was inside the roots or just adsorbed on the root surface (Jones et al. 1952). In most situations, salinity problems are almost always caused by NaCl. The relatively greater importance of Cl– than Na+ is not unique to citrus. In stone fruits, Cl– was found to be the main damaging ion, whereas Na+ accumulated in leaves only after membranes had already been damaged by Cl– (Shannon 1997). This is probably true also for citrus, however, in situations where salinity is caused by non Cl– salts (mainly sulfates), Na+ toxicity can appear. As described for Cl–, rootstocks can have a significant effect on the amount of Na+ absorbed from the soil and transported to the leaves. Among the rootstocks, ‘CLEO’ absorbed more Na+ than most other rootstocks (Cooper et al. 1958; Taylor and Dimsey 1993; Azab 1998; Levy 1998; Levy et al. 2000). Poncirus sp. and its hybrids usually absorb less Na+ than other rootstocks. 3. Boron. A toxic element of great concern for citriculture is boron. Boron is unique among the toxic elements since the range between deficiency and toxicity is narrow; B deficiency and toxicity can appear in the same orchard. Leaf concentrations of B of 50 to 200 mg kg–1 dry weight was considered optimum, and above 200 mg kg–1 (Chapman 1968) or 250 mg kg–1 (Embleton et al. 1973) was considered to be in the excess range. Toxicity can be caused by high concentrations of available B in the soil, even when the total B concentration is low, such as in some desert sandy soils (Elseewi et al. 1977). Salinity caused an increase in leaf injury of cucumber due to B toxicity (Alpaslan and Gunes 2001). High B soils can be found in some semi-arid regions, including the lower Rio Grande Valley of Texas (Cooper and Gorton 1952), around the Mediterranean, in some fine-textured soils in Victoria, Australia (Penman and McAlphin 1949) and the internal valleys of Israel. Boron excess can occur in some natural water sources. It is usually higher in reclaimed water (Reboll et al. 2000) and may increase in desalinized water produced by reverse-osmosis of seawater. Natural seawater contains 4 to 5 mg L–1 B, but the water that is desalinized by reverse osmosis may still contain more than 1.8 mg L–1 B (Nadav 1999) and membranes cannot deliver less than 1 mg L–1 B (Taniguchi et al. 2001). Such a level of B may prohibit the utilization of reclaimed water derived from desalinized water for the irrigation of citrus or other Bsensitive plants. A multistage reverse osmosis membrane sea desalination process and a low pressure reverse osmosis process can be recommendable for B management with a reasonable additional cost in drinking water supply (Magara et al. 1998). Scofield and Wilcox (1931)

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concluded that irrigation waters containing more than 0.5 mg L–1 of B might injure sensitive crops such as lemons or walnuts. Since irrigation water containing more than 1 mg L–1 may injure other plants, the 1 mg L–1 threshold is probably a safe upper level for B in irrigation water for citrus (Parsons et al. 2001). Under severe B toxicity, typical symptoms appear in the summer, with leaf abscission in winter leading to completely leafless trees, before they flush in the spring. This can result in branch dieback and sun damage to branches. B toxicity is often accompanied by Cl– toxicity. The orange-yellow mottling of B toxicity is often difficult to distinguish from the bronzing symptoms of Cl– toxicity (Cooper et al. 1955). The nutrition status of the tree has an effect on the appearance of B toxicity symptoms. High rates of N fertilizer, especially Ca (NO3)2 (but not (NH4)2SO4), reduced the severity of the B-toxicity symptoms, although the concentration of B in leaves was not reduced (Cooper et al. 1958; Cooper and Peynado 1959). CaSO4 had no effect on B-toxicity. In high-B soils in Israel, a common practice has been to apply chicken manure to sprinklerirrigated citrus to counteract B toxicity. The chicken manure may act like a high organic, slow-release fertilizer, thereby improving overall mineral nutrition. The shift from high volume sprinkler to microirrigation along with continuous proportional fertigation also mitigated B toxicity. This effect was probably because of better N and P fertilization and because of increased leaching of the smaller soil volume with water low in B. Swietlik (1995) described a link between the appearance of B-toxicity symptoms and Zn deficiency. Apparently, Zn-deficient citrus seedlings were more sensitive to B toxicity, as only Zn-deficient seedlings reduced growth in response to high B. The B toxicity symptoms could be reduced with foliar applications of chelated Zn even though the B concentrations in leaves, stems, and roots of the foliar-sprayed seedlings were not reduced. This observation is important since B toxicity and Zn deficiency may occur simultaneously in some soils and Zn deficiency is relatively easy to correct by foliar application. The susceptibility of different rootstocks to B toxicity and their interaction with scions has a large effect on the development of B toxicity. In grapefruit grafted on different rootstocks, the highest B levels recorded for ‘ SwL’, ‘SO’ and ‘RL’ were intermediate, and ‘SwO’ had the lowest B uptake (Embleton et al. 1962b). In a rootstock trial for ‘Nova’ mandarin, B was highest in trees on ‘Yuma citrange’ and C. taiwanica and lowest on ‘SO’ (Georgiou 2000). Outstanding tolerance to B was reported for grapefruit and ‘Valencia’ orange grafted on Severinia buxifolia (Poir)

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Tenore (Cooper et al. 1955). Graft incompatibility may rule out this combination, which also causes abnormal concentrations of other leaf nutrients. ‘MACR’ was also among the most tolerant rootstocks to high B (Embleton et al. 1962b; Peynado and Young 1962). This may be associated with the fact that scion leaves on this rootstock usually have higher N concentration than other rootstocks (Caro et al. 1977; Levy et al. 1993). ‘SO’ was much more tolerant to B than ‘SwL’ and ‘RL’ in the Negev area of Israel (Levy et al. 1980). Among the scions, lemon was more sensitive than other cultivars, and ‘Shamouti’ orange was more sensitive than ‘Valencia’ orange to B toxicity. ‘Emperor’ mandarin had the lowest B levels regardless of rootstock (Taylor and Dimsey 1993). 4. Lithium. There are some reports that excessive lithium can become toxic in arid areas of California and Arizona (Aldrich et al. 1951; Bradford 1961; Hilgeman et al. 1970). Symptoms included necrotic lesions in grapefruit leaves and defoliation. Injury became evident after the trees were 10 years old and increased in severity as the trees aged. Hilgeman et al. (1970) reported marked differences between citrus species and varieties in either tolerance to Li+ or their influence on Li+ uptake. Grapefruit and lemon seem to be more susceptible than orange, and ‘Kinnow’ mandarin topworked on severely affected grapefruit did not show any symptoms. Toxicity may be linked to the effect of Li on Ca uptake (Epstein 1960) or to an inhibition of myo-inositol monophosphatase (IMP) that is required for de novo inositol synthesis (Gillaspy et al. 1995). This compound has been related to salinity tolerance in plants (Nelson et al. 1998). The threshold for toxicity was estimated to be 12 mg kg–1 in leaf dry weight (Bradford 1961) or between 50 and 90 mg kg–1 in leaf dry weight (Embleton et al. 1973). Such a high range may be related to the fact that Li+ may concentrate at lesions in leaves (Hilgeman et al. 1970). Bradford (1961) noted that Li+ toxicity symptoms were similar in many respects to B symptoms and soils that have an excess of Li+ usually are also high in B. There are no recent reports on Li toxicity in citrus. 5. Interaction between Salinity and Nutrient Ions. Salinity can cause nutrient imbalances in various ways. K+ can be leached from the soil exchange complex if excessive Na+ is present, and Na+ may also compete with K+ at the soil-root interface. This can result in K+ deficiency under saline conditions. Interestingly, some of the Cl–-tolerant rootstocks, such as ‘CLEO’, ‘Sunki’, and ‘Emperor’ mandarins, tend to suffer

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from K+ deficiency coupled with an increase in tissue Na+ content under saline conditions (Behboudian et al. 1986). One way to observe the interrelations of Cl– and Na+ is to use these ions with different anion combinations. Banuls and Primo-Millo (1992) compared the effect of NaCl, KCl, and NaNO3 on citrus photosynthesis, and concluded that NaCl and KCl increased Cl– leaf content and reduced photosynthesis. NaNO3, however, did not affect photosynthesis though it increased leaf Na+ content. These results were confirmed by RomeroAranda et al. (1998), who found that decreases in photosynthesis were highly correlated with increases in leaf Cl–. F. Vegetative Growth Growth of all plants is reduced by decreased leaf water potential (Maas 1986). The effect of salinity on plant growth is not always related to the accumulation of toxic elements in citrus leaves if toxic concentrations are not reached. For example, the growth of ‘SO’ and ‘CLEO’ was similar even though ‘SO’ accumulated more Cl– (Zekri 1991). Salinity also increases the succulence of citrus leaves (Cerda et al. 1977) and the thickness of the leaf lamina. Comparative anatomical observations indicated that the mesophyll increased in volume by simultaneous division and expansion of the cells as spongy parenchyma cells became larger and more rounded (Romero-Aranda et al. 1998; Nastou et al. 1999). In a short-term experiment, Sykes (1985) reported that salinity increased leaf water contents acropetally in only some of the rootstocks tested. G. Fruit Yield and Quality 1. Yield. Many salinity tolerance comparisons have been based on relative reductions in fruit yield. ‘Verna’ and ‘Fino’ lemons, on ‘SO’ and ‘MACR’ rootstocks, had reduced yields as salinity increased (Nieves et al. 1992). Fruit yields decrease about 13% for each 1.0 dS m–1 increase in electrical conductivity of the saturated-soil extract (ECe) once soil salinity exceeds a threshold ECe of 1.4 dS m–1 (Maas 1993). In Australia (Cole and McCloud 1985), regression analysis during the period 1945–1979 on data from irrigated orchards showed that yield was negatively associated with salinity at the locations with highest salinity. Fruit yield of ‘Washington Navel’ orange decreased with increasing salinity due to a reduced number of fruits per tree rather than reduced average fruit weight (Haggag 1997). Increased salinity of ground water caused by seawater intrusion reduced the yield of ‘Satsuma’ mandarins

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grafted on trifoliate orange rootstocks in Western Turkey (Aksoy et al. 1996). ‘Shamouti’ orange on ‘SO’ did not absorb much Cl– after 6 years of salinization (up to 0.44% Cl leaf dry weight) with water up to 462 mg Cl– L–1 (13 mol m–3 Cl–). The 14% reduction in yield was mainly due to osmotic stress (Dasberg et al. 1991). However, continued exposure to salinity could have caused accumulation of Cl– to toxic levels. 2. Internal Quality. Although drought stress can have a profound effect on citrus internal quality, the effect of salinity is usually very subtle. Most salinity studies report a slight increase in juice solids, sometimes accompanied with a similar increase in acidity, which causes the TSS to acid ratio to remain unchanged (Boman 2000; Levy et al. 1978, 1979). This observation implicates a reduced water movement into the fruit due to the osmotic effect of salinity. The production of more solids in fruit may have a significant importance in fruit for processing. H. Phytochemicals Citrus fruits contain several phytochemicals and/or nutraceuticals such as carotenoids (lycopene and β-carotene), limonoids, flavonones (naringin and naringin rutinoside), folate, and vitamin C that have important medical benefits in human diets. Phenolic compounds have been used to establish taxonomic relationships among fruit cultivars (Berhow et al. 1998) and many phytochemicals vary with rootstocks (Kefford and Chandler 1970). This fact implies that the accumulation of these materials in fruit is subject to variations in water relations, mineral nutrition, and/or plant growth regulators that are attributable to rootstock. There are data indicating that several phytochemicals can be enhanced by preharvest factors such as cultivar and season (Patil 2000). Red and pink grapefruit cultivars have higher lycopene and total carotenoids than white-fleshed ones and concentrations of most phytochemicals change as seasonal maturity progresses. In addition, there are a few studies on effects of soil moisture status, temperature, and freezing on juice constituents (Kefford and Chandler 1970). Flavonones and liminoids increase during post-harvest storage (Patil et al. 2000). Undoubtedly, such responses in fruit are related to dehydration and/or dilution of juice. It is tempting to speculate that just as rootstocks affect salinity tolerance, salinity stress may affect the accumulation of phytochemicals. Controlled salinity stress might enhance the concentration of phytochemicals in juice. We know of no data, however, to support this speculation, but this is an area that may merit future research work.

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V. SALINITY AND BIOTIC STRESSES A. Phytophthora Multiple stresses can have synergistic effects on plants. Much of the work on interactions between salinity and pathogens has been done using seedlings. In field trees, however, the scion can affect the susceptibility of the rootstock to root rot (Shaked et al. 1984). In greenhouse experiments, irrigation with high-salinity water with a Cl– concentration of 1670 mg L–1 predisposed citrus rootstocks to attack by root pathogens (Combrink et al. 1996). Rootstock seedlings of ‘TROY’, ‘CARZ’, ‘VOLK’, and ‘RL’ were most affected by the treatment consisting of three root pathogens in combination (Phytophthora nicotianae, Fusarium solani, and Tylenchulus semipenetrans) under saline conditions. Growth of these seedlings subjected to both Phytophthora and salinity together was significantly less than that of seedlings subjected to the pathogens either singly or with Cl– stress alone. Phytophthora infection and Fusarium root rot were always more severe in combination with Cl–. ‘VOLK’ and ‘RL’ were more severely affected by the three pathogens than ‘TROY’ and ‘CARZ’. In addition, ‘TROY’ and ‘CARZ’ citranges, with known tolerance to P. nicotianae and T. semipenetrans, became more susceptible to these pathogens when irrigated with high-salinity water. Salinity also affected stem infection. Stems of ‘SO’, ‘RL’, and ‘TROY’ were inoculated with a fungus identified as P. citrophthora, and regardless of rootstock, NaCl (but not Na2SO4) increased stem gummosis (El Guilli 2000), pointing again to the detrimental effect of the Cl– ion on citrus. Increased disease could have resulted from increased tissue susceptibility in response to salinity stress, inhibition of plant defense (Afek and Sztejnberg 1993), and/or decreased root regeneration. Phytophthora isolates cultured from diseased citrus growing in the saline soils of the Coachella valley in California tolerated salinity more than a culture isolated from citrus growing in non-saline soil (Blaker and MacDonald 1985). The ability of Phytophthora to tolerate high levels of salinity could significantly diminish the resistance of Phytophthora-tolerant rootstocks such as ‘TROY’ under saline conditions (Blaker and MacDonald 1986).

B. Rio Grande Gummosis Rio Grande gummosis, a disease of unclear etiology, was attributed to irrigation with high-salinity water and to applications of KCl or CaCl2 but not to K2SO4 (Childs 1978). Although the Cl– levels in the leaves were

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similarly normal in infected and non-infected locations, Cl– levels in the bark and wood were about 10 times higher than those in the roots and almost four times higher in an orchard infected with Rio Grande gummosis than in the non-infected orchard (Russo et al. 1993). However, analysis of grapefruit trees on different rootstocks in Florida indicated no relationship between rootstock tolerance to salinity and incidence of Rio Grande gummosis (Sonoda and Pelosi 1990). In a long-term salinity experiment at Gilat, Israel (Y. Levy and J. Shalhevet, unpublished results), there was no correlation between the salinity of the irrigation water and appearance of Rio Grande gummosis in ‘Marsh’ grapefruit. There was adequate disease pressure present, however, as trees at different salinities were infected at random. In Israel, Rio Grande gummosis commonly affects grapefruit trees on ‘TROY’ or on ‘SO’ that suffer from lime-induced chlorosis. The problem can be corrected by the application of chelated iron and by modifying the irrigation system from sprinkler to drip. This occurrence leads us to the conclusion that Rio Grande gummosis may be related to soil aeration, to lime-induced chlorosis, or to just general stress that may be caused by different factors and not only salinity. C. Nematodes The citrus nematode (Tylenchulus semipenetrans) can reduce the salt tolerance of citrus roots and increase Cl– uptake (Willers and Holmden 1980). Leaf Cl– levels of severely affected trees varied between 1.75 and 2.00% compared with 0.50–0.90% in less-infected trees under the same conditions; this was true for salinity-tolerant rootstocks and for salinitysensitive rootstocks, however. At the same experiment, nematodes increased more than three-fold the Cl– concentration in leaves but decreased the Cl– concentration in roots (Mashela and Nthangeni 2002). Salinity increased nematode egg production, with the largest number of eggs recovered from ‘CLEO’ and ‘SO’ roots, where salinity doubled the number of eggs. Salinity also increased the number of nematode eggs and females on rootstocks with better tolerance to nematodes, such as ‘TRIF’, ‘CTRM’, and ‘TROY’. However, the nematode number remained small, suggesting that salt-tolerant rootstocks are more susceptible to nematodes and nematode-resistant rootstocks lack salt tolerance (Mashela et al. 1992a). On the other hand, sudden reductions in soil salinity by rain or irrigation offered nematodes a suitable non-osmotic habitat that increased their population densities (Mashela et al. 1992b). Soil salinity increased the susceptibility of citrus roots to attack by the citrus nematode (Dunn et al. 1998). Thirty days of a high-salinity (0.1 M

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NaCl) treatment 6 months after inoculation with nematodes, increased the nematode infection rate by 54%. Phenylalanine ammonia lyase (PAL) activity was inversely correlated with salinity level and with increase in arginine concentration, suggesting that salinity caused a breakdown in root chemical defenses. D. Mycorrhizae Citrus trees interact with microorganisms that belong to various groups, including bacteria, fungi, and nematodes. Soil-borne pathogens constitute only a very small fraction of the total population of soil organisms (Katan 1996). These range from true parasites that always harm the roots to microorganisms that may exist in harmony with the plant or even benefit the plant. Citrus is very dependent on vesicular arbuscular mycorrhizae (VAM) colonization, especially under conditions of low soil P concentration or sterilized soils (Kleinshmidt and Gerdemann 1972; Krikun and Levy 1980; Menge et al. 1978). The ability of VAM to increase tree growth particularly under saline conditions and thus alleviating salinity stress has been reported. However, there have been some reports that VAM can increase Cl– uptake by plants, just as VAM increases P uptake. VAM plants of ‘CARZ’ and ‘SO’ accumulated more Cl– in leaves than non-mycorrhizal plants. Cl– was higher in non-mycorrhizal roots of ‘SwO’ and ‘CARZ’ than in mycorrhizal roots (Hartmond et al. 1987). Graham and Syvertsen (1989) reported that VAM increased the concentrations of Cl– in leaves and roots of ‘SwO’ and ‘SO’ seedlings irrigated with high-salinity water. This increase could not be attributed to increased transpiration in the VAM plants. Na+ concentrations, on the other hand, were not affected by VAM. There were no significant growth or physiological interactions between mycorrhizae and salinity. Natural VAM in relatively saline soils may be sensitive to salinity and its population decreased with increased soil salinity (Levy et al. 1983). VAM strains that originated in soils of different salinities may differ in this respect (Copeman et al. 1996; Juniper and Abbott 1993).

VI. BENEFITS OF MODERATE SALINITY Other than the benefits from moderate applications of fertilizer salts, salinity is usually not beneficial for citrus in the long run. Since citrus can tolerate moderate salinity and produce a profitable yield using

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proper cultural practices and tolerant cultivars, there may be some shortterm benefits from salinity. A. Chilling and Freezing Tolerance Moderate salinity at levels of 1065 to 2130 mg Cl–1 L–1 (30 to 60 mol m–3 of NaCl) applied for 2 months, reduced growth and total plant transpiration but enhanced cold hardiness of ‘SwO’ and ‘CLEO’ seedlings (Syvertsen and Yelenosky 1988) even though leaf Ψπ and leaf proline concentration did not change significantly. Thus, controlled salinity stress under greenhouse conditions can substitute for cool temperature-induced freeze tolerance in seedlings by reducing physiological activity and growth. However, when freeze injury was determined for young grapefruit trees on different rootstocks, trees with high Cl– content were more susceptible to freeze injury than those with low Cl– (Peynado 1982). B. Leaching Du Plessis (1985) suggested that reduced transpiration from salinity stress could potentially be a benefit in reducing the accumulation of soil salinity, since the lower water uptake should increase the leaching fraction. This scenario implies that an increase in the leaching fraction occurs when irrigating with increasingly saline water when water applications are scheduled similarly to those for non-saline conditions. However, soil salinity can increase proportionally to the salinity in the irrigation water and thereby reduce growth and yield. C. Increase Flowering, Yield Just as drought stress can substitute for cool wintertime temperatures to enhance flower induction (Nir et al. 1972; Southwick and Davenport 1986), it is possible that moderate salinity stress will also increase flowering. In a warm, wet climate with inadequate chilling or drought stress to maximize flower induction, controlled salinization might offer a substitute to induce flowering as is practiced for inducing flowering of litchi in Thailand (E. Tomer, pers. commun. 2001). If saline irrigation water could be applied during induction followed by adequate rainfall or irrigation with good-quality water during fruit set, yields might be increased. The successful economic use of such a practice, however, remains to be tested. As discussed above, effects of moderate salinity on fruit quality are usually subtle (Boman 2000).

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VII. SUMMARY Since decreases in the quality of the world’s water resources are inevitable, it is important that growers continue to improve production practices and genetic varieties to deal with poor-quality water to sustain production. Citrus can use reclaimed water better than other crops since fruit are either processed for juice or thoroughly washed and disinfected in the packinghouse prior to peeling (Parsons et al. 2002). However, reclaimed waters are higher in salinity than unused water and salinity will increase as urban water use efficiency improves. There are many things citrus growers can do to ameliorate problems associated with salinity stress, from choosing the best rootstock and scion cultivars to appropriately managing irrigation and fertilizer application methods. To help citrus growers cope with salinity problems, researchers should not only understand the mode of action of salinity stress but also understand the underlying mechanisms of salinity tolerance. Salinity reduces water use thorough osmotic effects but the gradual accumulation of Cl–, Na+, and B to toxic levels are equally or even more important in citrus trees. Fortunately, the different species of Citrus and their relatives differ in susceptibility to salinity, and future breeding may produce better rootstocks than are available today. Salinity tolerance is a whole plant phenomenon that requires an appreciation of citrus rootstock/scion interactions in the field. Such relationships are complicated by interactions between salinity and physical environmental factors as well as between salinity, pests, and diseases. The study of interactions between salinity, drought, and elevated CO2 can yield insights into salt exclusion/uptake, growth, and plant water use. New rootstocks or even salttolerant cultivars, together with improved cultural practices, such as nutrition, irrigation, drainage, and perhaps altering the physical environment, such as shading or raising humidity, may enable future citriculture to utilize lower-quality water. Not all effects of salinity are negative, however, as moderate osmotic stress can reduce physiological activity and growth, allowing citrus seedlings to survive cold stress. Short-term salinity can even enhance flowering after the salinity stress is relieved. LITERATURE CITED Afek, U., and A. Sztejnberg. 1993. Temperature and gamma irradiation effects on scoparone, a citrus phytoalexin conferring resistance to Phytophthora citrophthora. Phytopathology 83:753–758.

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Gomez-Cadenas, A., F. R. Tadeo, M. Talon, and E. Primo-Millo. 1996. Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol. 112:401–408. Gonzalez-Altozano, P., and J. R. Castel. 1999. Regulated deficit irrigation in Clementina de Nules’ citrus trees. I. Yield and fruit quality effects. J. Hort. Sci. Biotechnol. 74: 706–713. Graham, J. H., and J. P. Syvertsen. 1989. Vesicular arbuscular mycorrhiza increase chloride concentration in citrus seedlings. New Phytol. 113:29–36. Grieve, A. M., and R. R. Walker. 1983. Uptake and distribution of chloride, sodium, and potassium ions in salt-treated citrus plants. Austral. J. Agr. Res. 34:133–143. Gucci, R., and M. Tattini. 1997. Salinity tolerance in olive. Hort. Rev. 21:177–214. Haggag, L. F. 1997. Response of Washington Navel orange trees to salinity of irrigation water. Egypt. J. Hort. 24:67–74. Hamou, M., Y. Levy, O. Sagee, D. Hisdai, A. Dahan, J. Lifshitz, and A. Shaked. 1999. Effect of salinity and rootstock on the easy peeling cultivar ‘Winola’ (in Hebrew). Alon Haotea 53:242–247. Harding, R. B., M. Miller, and M. Fireman. 1958. Absorption of salts by citrus leaves during sprinkling with water suitable for surface irrigation. Proc. Am. Soc. Hort. Sci. 71:248–256. Hartmond, U., N. V. Schaesberg, J. H. Graham, and J. P. Syvertsen. 1987. Salinity and flooding stress effects on mycorrhizal and nonmycorrhizal citrus rootstock seedlings. Plant Soil 104:37–43. Hilgeman, R. H., W. H. Fuller, L. F. True, G. C. Sharples, and P. F. Smith. 1970. Lithium toxicity in Marsh grapefruit in Arizona. J. Am. Soc. Hort. Sci. 95:248–252. Hodgson, R. L. 1967. Horticultural varieties of Citrus. p. 431–591. In: W. Reuther, H. J. Webber, and L. D. Batchelor (eds.), The citrus industry, Vol. 1. Univ. California, Berkeley. Hoffman, G. J., P. B. Catlin, R. M. Mead, R. S. Johnson, L. E. Francois, and D. Goldhamer. 1989. Yield and foliar injury response of mature plum trees. Irrig. Sci. 10:215–229. Hutchison, D. J. 1985. Rootstock development screening and selection for disease tolerance and horticultural characteristics. Fruit Var. J. 39:21–25. Jensen, M. E., W. R. Rangeley, and P. J. Dieleman. 1990. Irrigation trends in world agriculture. p. 31–67. In: A. R. Stewart, and D. R. Nielsen (eds.), Irrig. Agr. Crops, Vol. 30. Am. Soc. Agron., Crop Sci. Soc. Am. Soil Sci. Soc. Am., Madison. Jifon, J. and J. P. Syvertsen. 2001. Effects of moderate shade on citrus leaf gas exchange, fruit yield and quality. Proc. Fla. State Hort. Soc. 114:177–181. Jones, W. W., H. E. Pearson, E. R. Parker, and M. R. Huberty. 1952. Effect of sodium fertilizer and irrigation water on concentration in leaf and root tissues in citrus trees. Proc. Am. Soc. Hort. Sci. 60:65–70. Juniper, S., and L. Abbott. 1993. Vesicular-arbuscular mycorrhizas and soil-salinity. Mycorrhiza 4:45–57. Katan, J. 1996. Interaction of roots with soil-borne pathogens. p. 811–822. In: Y. Waisel, A. Eshel, and U. Kafkafi (eds.), Plant roots: The hidden part, 2nd ed. Marcel Dekker Inc., NY. Kefford, J. F., and B. V. Chandler. 1970. The chemical constituents of citrus fruits. Acad. Press, NY, p. 246. Kleinshmidt, G. D., and J. W. Gerdemann. 1972. Stunting of citrus seedlings in fumigated nursery soils related to the absence of endomycorrhizal. Phytopathololy 62:1447–1453. Kochba, J., G. Ben-Hayyim, P. Spiegel-Roy, S. Saad, and H. Neumann. 1982. Selection of stable salt-tolerant callus cell lines and embryos in Citrus sinensis and Citrus aurantium. Z. Planzenphysiol. 106:111–118.

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3 Red Bayberry: Botany and Horticulture* Kunsong Chen, Changjie Xu, and Bo Zhang Department of Horticulture Huajiachi Campus, Zhejiang University Hangzhou, 310029, P. R. China Ian B. Ferguson The Horticulture and Food Research Institute of New Zealand Private Bag 92 169 Auckland, New Zealand I. INTRODUCTION A. History B. Distribution C. Commercial Production II. BOTANY A. Taxonomy B. Morphology and Anatomy III. PHYSIOLOGY A. Vegetative Growth B. Flowering and Fruit Set C. Fruit Development IV. ENVIRONMENTAL REQUIREMENTS A. Temperature B. Water C. Soil D. Light E. Elevation and Exposure *This review was supported by the State Key Basic Research and Development Plan (G2000046806), the National Natural Science Foundation of China (30170660), and Zhejiang Natural Science Foundation (ZD0004), and was also a part of a cooperative program between The Horticulture & Food Research Institute of New Zealand and Zhejiang University. We thank Dr. Grant Thorp for critically reading the manuscript. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 83

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V. HORTICULTURE A. Propagation B. Field Cultivation C. Pests and Diseases D. Harvest and Handling E. Storage and Transportation F. Processing VI. CONCLUDING REMARKS LITERATURE CITED

1. INTRODUCTION Red bayberry (Myrica rubra Sieb. & Zucc., Myricaceae) is a subtropical fruit tree native to China and other Asian countries, bearing a delicious, berry-like fruit (Fig. 3.1). Gengmin Wu, founder of modern Chinese horticulture, praised it as a “precious Southern Yangtze fruit of early summer ” (Wu 1995). The fruit ripens in June and early July in the main Chinese production areas of Zhejiang and Jiangsu provinces, earlier than most other local fruits. The rich red colors and appealing flavor make this juicy fruit popular with consumers; it is eaten like a cherry.

Fig. 3.1. Red bayberry (Myrica rubra) fruit and trees. A and B: mature fruit showing (B) the segmented juicy flesh and the hard stone. C: fruit growing on the outer space of the canopy. D: trees growing on hillsides, a common cultivation practice in China. Photos by Jiangguo Xu.

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In addition to being consumed fresh, various products such as juice, canned fruit, jam, wine, sweets and salted fruit are produced. Presentday commercial cultivation is still largely restricted to China. The fruit and roots of red bayberry have been used as important components of traditional Chinese medicines for more than 2000 years (Li 1578), the fruit being beneficial for treating congestion, coughs, digestive problems, and diarrhoea. The root also has wound healing properties. In recent years, a number of pharmaceutically active compounds have been identified from the various plant parts (Zhang et al. 1993; Chi et al. 2000; Yi and Liu 2000; Zhong et al. 2000). The evergreen tree has a bushy, round canopy and grows well in soils of low fertility, having an association with the nitrogen-fixing bacterium Actinomyces frankia. The tree is used in China to increase the organic matter content of soil, reduce soil erosion, and to enhance the landscape (Wang and Chen 1989). Red bayberry is often interplanted with existing vegetation such as pine or other natural forest trees (Wang et al. 2001). While the fruit is well known throughout China, where there is a considerable body of literature on various aspects of production, it is little known elsewhere. There is a short general review on red bayberry available in English (Li et al. 1992), and a review of research progress in China has recently been published (Li et al. 1999). This review will cover the botany and horticulture of red bayberry, most of it based on Chinese publications. A. History In China, red bayberry has been known by a variety of names. Yangmei is the most common name in Chinese. Shizheng Li, in Compendium of Materia Medica (1578), wrote: “The shape of the tree is similar to poplar (Yang), and the taste of the fruit is somewhat like mume (Mei), thus it is named Yangmei.” Shumei (strawberry tree) is used in Taiwan. Zhuhong is a common name in Fujian province and, elsewhere in China, names such as Shanyangmei and Zhurong are used. The English names for this fruit include red bayberry, Chinese bayberry, and waxberry. The fruit has a very long history in Chinese civilization. The earliest records come from the Neolithic site at Hemudu, Zhejiang province, indicating that the fruit has existed as a foodstuff for more than 7,000 years (Yu 1979; Wu 1984). Red bayberry fruit and stones have also been found in the Mawangdui tumulus of the Western Han Dynasty (206 B.C.E.–25 C.E.) in Hunan province and the Luobowan tumulus in Guangxi Zhuang Autonomous Region (Yu 1979). Nan Fang Cao Mu Zhuang, a book on the properties of various plants from southern China, written by Ji Han during the Jing Dynasty (265–420), recorded the cultivation of red bayberry

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and its use in wine making (Ji 304). By the Song Dynasty (960–1279), the Wu-Yue area (Jiangsu and Zhejiang provinces today) was well known for red bayberry production and the fruit recognized for its quality and quantity; locations close to Ningbo and Taizhou in Zhejiang province are still the most important production areas. B. Distribution Red bayberry originated in southeastern China, where it is still found in the wild and is the source of seed for rootstocks. It is now distributed south of the Yangtze River and north of Hainan Island, approximately 97° to 122°E longitude, and 20° to 31° N latitude. This distribution is similar to that of citrus, loquat, tea, and bamboo, except that red bayberry can withstand lower temperatures (Maio and Wang 1987; Maio et al. 1995). The major commercial production area is concentrated in Zhejiang, Fujian, Jiangxi, Jiangsu, Guangdong, and Guizhou provinces. There is some production in Yunnan, Guangxi, Sichuan, Hunan, Shanxi, and Taiwan, from semi- or wholly wild trees (Wang 1995). Outside of China (Yu 1979; Wang 1987) the crop is grown in Thailand, although fruit quality is often poor and the area limited. In Japan, it is grown in Tokushima, Kochi, Ehime and the western part of Honshu. In Europe and America, red bayberry trees are used mainly for ornamental purposes. There are a number of closely related species (described below) that are cultivated. Myrica integrifolia Roxb. is distributed in India, Sri Lanka, Burma, and Vietnam, where it is confined to home gardens, producing small and acid fruit, usually used for jam or medicine. Myrica esculenta Buch.-Ham. is found in India, Nepal, and Vietnam as well as in southwest China. Myrica faya Ait. has fruit suitable for fresh consumption and is grown in the Canary Islands. C. Commercial Production Production of red bayberry has increased dramatically; the cultivated area in China in 1995 was 130,000 ha. The crop has become one of the most important fruit tree crops in south China (Liu 2000; Wang et al. 2001). In Zhejiang province, the cultivated area and production were 4,400 ha and 26,500 tonnes (t) in 1959, 17,500 ha and 46,200 t in 1985, and 38,378 ha and 129,750 t in 2000 (Wang et al. 2001). As a result, red bayberry is second only to citrus among the fruit crops of the province, and the yield is expected to continue to increase. Most production is consumed locally, but an increasing proportion is being exported both within and outside of China.

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II. BOTANY A. Taxonomy 1. Species. The Myricaceae are widespread in tropical, subtropical, and temperate areas of the world. They consist of two genera, Comptonia and Myrica, both of which are cultivated. The genus Myrica Linn contains more than 50 species of which six are found in China (Yu 1979; Maio and Wang 1987; Qu and Sun 1990; Wang 1995; Li et al. 1999). More recently, RAPD (Random Amplified Polymorphic DNA) markers have been successfully used in classification and identification of Myrica species (Lin et al. 1999). Myrica cerifera L. originating from North America was clearly distinguished from three Chinese species (Myrica adenophora Hance, Myrica esculenta Buch. -Ham, and Myrica rubra Sieb. & Zucc.), which clustered together. Myrica rubra Sieb. & Zucc. Red bayberry (2n = 16) is an evergreen tree growing to a height of 5 to 10 m, distributed in southern China, but also found in Japan, South Korea, and The Philippines. The bark of young trees is smooth and yellow-green, while that of old trees is grey-brown with white spots and narrow cracks. The canopy is uniform and round or slightly flattened. The branches are frail and easily broken, and the leaves alternate and simple, with blades 5–14 cm long and 1–4 cm wide, usually with smooth margins, although sometimes serrated. The upper and lower leaf surfaces are smooth without hairs, the upper lustrous and dark green and the lower light green. The plant is dioecious, although occasionally monoecious, with the inflorescence forming in axillary buds. The staminate inflorescence is a compound catkin, 1–3 cm long, columnar, and yellow-red; the pistillate inflorescence is a simple catkin and shorter and thinner, filaceous, bright red, with two longitudinal grooves along the stigma. The fruit is a small drupe and consists of a fleshy pericarp comprising individual segments and a hard endocarp protecting a single seed. It is red, purple, white, or pink when ripe, depending on the cultivar. Flowers bloom during February to April and fruit ripen during May to July. Myrica esculenta Buch.-Ham. This is also known as Yangmei Dou in Guizhou. It is mainly distributed in mountains at elevations of 1,500–2,500 m in southwest China (Sichun, Yunnan, Guizhou, Guangdong, and Guangxi), and in India, Nepal, and Vietnam. The tree is 4–15 m high, with light-colored bark. The shoots are thin and covered with numerous hairs. The leaves are thick, hairless, and oval, 3–12 cm long

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and 1.2–4.5 cm wide, with few or no marginal indentations and sparse yellow glands on the lower surface. The petiole is covered with white hairs. The plant is dioecious and the inflorescences are catkins, the flowers having two bright red, thin stigmas. The fruit are ovoid, about 1 cm long and 0.8 cm in diameter, with an average weight of about 0.5 g, and with red flesh. The edible portion constitutes about 80% of the fruit weight and, when ripe, the soluble solids concentrations are about 12.5% and total acids 1.3%. Flowers bloom during September to October and fruit ripen during the following March to April. There are seven subspecies or variants of this species, which can endure high humidity and temperatures down to –6°C, and which will also grow well in dry areas. Myrica nana Cheval. This species is variously known as Yunnan Yangmei and Dian Yangmei and is mainly distributed in subtropical and temperate zones of Yunnan, Guizhou, and Xizhang in China. The plant is a shrub 0.5–1.0 m high, with thick, strong shoots. The bark is rich in tannin, and the olive green leaves are narrowly obovate or occasionally elliptic. The upper leaf surface usually has small depressions associated with yellow glands and sunken venation; the lower leaf surface has glands and protruberant venation. Petioles are short and covered with short soft hairs. Fruit are round to oblate, about 2 cm long and 2 cm in diameter, with an average weight of 3.5–5 g. Ripe fruit are red, with an 80% edible proportion and soluble solids levels of 9–10% and total acids of nearly 4%. Flowering may last 1 month from February to March, and fruit normally ripen about 4–6 months after flowering. The species has four variants and two derivatives: M. nana var. integra Cheval., M. nana var. luxurians Cheval., M. nana Cheval, var. humifusa N. Liu et Z. F. Li, var. sp. nov., M. nana Cheval, var. alba N. Liu et Z. F. Liu et Z. F. Li var. sp. nov., M. nana cheval, f. cerea N. Liu et Z. F. Li, f. niv. and M. nana Cheval, f. gracilifolia N. Liu et Z. F. Li, f. onv. Myrica integrifolia Roxb. This species is mainly distributed in the mountains of South Asia at an elevation of 900–1,400 m in countries such as India, Sri Lanka, Burma, and Vietnam, and also in the western part of Yunnan in China. It is a large evergreen shrub or tree, 8–10 m high with dense shoots covered with dense soft hair. Leaves are lanceolate, bright green, with smooth margins, but sometimes undulate. The plant is dioecious, with oval, red, acid fruit when ripe, weighing about 2.4–3 g, with 10.5% soluble solids and an edible portion of about 85%. Flowers bloom during February to March, and fruit ripen from April to May. The species prefers an acid soil and high humidity, and usually grows in forests together with deciduous plants.

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Myrica arborescens. S. R. Liet X. L. Hu, sp. nor. The species is distributed in the south and southwest part of Yunnan in China, and in Burma, growing in the mountains at an elevation of 900–1,400 m. Plants prefer an acid soil and humid climate. It is an evergreen tree, about 15 m in height, with a trunk of more than 300 cm in circumference. Shoots have long white hairs and few glands, and the leaves are larger than for other species, with blades 8–19 cm long and 2–4 cm wide, elongated lanceolate or ellipsoidal in shape, and having obvious sharp sawtooth edges on the abaxial sides. The upper venation of young leaves is covered with white soft hair, while yellow glands cover the lower surface, and the secondary veins are also covered with long white soft hair. Plants are dioecious, with an ovary surrounded by long hairs and the fruit are round or ovoid, 2.5–3 cm in diameter and yellow-white or green-white when ripe. Flowers bloom during February to March, and the fruit ripen from April to May. Myrica adenophora Hance. Known variously as Xiyeyangmei, Pomei, and Qingmei, it is mainly distributed in Hainan province, the southern part of Guangdong province and southwestern Guangxi province. The variant M. adenophora var. kusanoi Hayata is grown in Taiwan. It is a shrub or small tree, 1–6 m high. The bark is gray and the young thin shoots are covered with short soft hair and yellow glands. Leaves are obovate, both sides with numerous glands. The medial vein has short soft hair, as does the petiole. Staminate and pistillate inflorescences form in axillary buds. The red fruit are oval, small, and less than 1 cm in diameter. Flowers bloom from October to November, and the fruit ripen during February to May. 2. Cultivars. There is little agreement on cultivar classification. Fruit color and ripening date have been used to identify different groups of cultivars (Yu 1979; Wu 1984; Maio and Wang 1987; Qu and Sun 1990). Guo and Li (1994) sorted the cultivars into five groups and nine types based on physical characters of the stone, fruit, and leaves, while Chen (2000) divided them into two types based on soft and hard fruit flesh. The Chinese Red Bayberry Cooperation Association has established three types based on the fruit ripening date (Chen 2000). Recently, peroxidase isozyme analysis, chromosome banding, and karyotypic analysis have been introduced into varietal classification (Lin et al. 1999). Ripe fruit color is one of the more useful criteria used (Qu and Sun 1990; Li et al. 1992), and this has resulted in four cultivar groups described as follows:

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Wild. This group, also called wild black, is found growing in the wild and is used as rootstocks. The fruit are red and acid, with small flesh segments, and ripen earlier than other types, in Zhejiang at about the beginning of June. Red. Fruit of this group are red when ripe, and usually larger and of better quality than other types. Representative cultivars include ‘Shuimei ’, ‘Chise’ , ‘Dongkui’ in Zhejiang, and ‘Dayexidi ’ in Jiangsu. Black. This group has the best fruit quality, with large flesh segments and a stone that can be easily separated from the flesh. The fruit turns from red to red-black during ripening. Representative cultivars include ‘Biqi’ in the Cixi-Yuyao district, ‘Wandao Yangmei’ in Dinghai, ‘Ding-ao Mei’ in Wenzhou, ‘Datanmei’ in Yuhang in Zhejiang, ‘Wumei’ in the Dongting area in Jiangsu, and ‘Shanwu’ and ‘Wuhesu’ in the Chaoyang area in Guangdong. White. The ripe fruit of this group are various shades of white. Yield and fruit quality is less than for fruit of the black or red groups, and it is not so widely planted. ‘Shuijing Yangmei’ (crystallooking) in Shangyu is the best cultivar of this type grown in Zhejiang province. Zhang and Miao (1999) distinguished 268 cultivars in China. Fruit characteristics vary widely among these cultivars, as shown by the percentage of cultivars in different groups on the basis of ripening date, fruit color, and fruit weight (Table 3.1). The cultivars in Zhejiang province can be sorted by ripening date into three groups (Table 3.2).

Table 3.1. Distribution of fruit attributes among different Chinese cultivars of red bayberry. Source: Zhang and Miao (1999). Ripening Date

Month April May Early June Mid June Late June Early July

Distribution (%) 1.1 6.3 13.7 18.7 47.8 12.4

Flesh

Fruit Size

Color

Distribution (%)

Weight (g)

Distribution (%)

White Pink Red Deep red Purple Deep purple Purple black Jet black

9.3 5.6 17.2 7.8 37.3 3.4 13.8 5.6

<6 6.1–9 9.1–13 13.1–15 >15

6.3 25.8 46.6 14.9 6.3

Table 3.2. Ripe fruit attributes of early-, medium-, and late-maturing cultivars of red bayberry grown in Zhejiang. Data are averages from unpublished sources. Fruit Characteristics

Ripening date Early (<June 20) Mid (June 20–July 5) Late (>July 5)

Cultivar

Width (cm)

Length (cm)

Weight (g)

Zaodamei Zaoqimimei Biqi Ding-aomei Dongkui Wandaoyangmei Wanqimimei

3.2 2.6 2.7 2.7 3.7 2.8 2.8

2.9 2.5 2.6 2.9 3.9 2.7 2.7

15.7 9.7 10.7 20–25 11.20 12.50

Edible portion (% wt)

Soluble solids (%)

Total sugars (%)

Acidity (%)

Stone (g)

94 94 95 94 96 95 95

11.7 11.5 12.5 11.7 12.7 12.7 12.8

8.7 9.7 9.5 9.7 9.5 9.7 10.7

1.1 1.7 0.9 0.9 1.4 0.9 0.9

1.7 0.5 0.6 0.6 0.8 0.6 0.6

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B. Morphology and Anatomy 1. Roots and Nitrogen Fixation. The trees have a shallow, fibrous root system, usually occupying the top 5 to 40 cm of the soil, and typically one- to twofold greater than the diameter of the canopy. The plants form an association with Actinomyces frankia, a nitrogen-fixing bacterium. The nodules are usually greyish yellow, fleshy, and randomly distributed on the roots (Miao and Wang 1987; Wang 1995). In transverse section, the nodules are round and symmetric, and their color changes from oyster white to yellow brown with maturation, and dark brown with senescence (Wang and Huang 1990). Nitrogenase activity of mature nodules is higher than that of the young ones, with two peaks of activity observed in June and October. The lowest activity is found in January, and can be inhibited by nitrate (Wang and Huang 1990; Wu and Gu 1994). Measurements by Z. Li et al. (1993) have shown that the average nodulation mass in a 7-year-old red bayberry sapling was 52 g/tree with 460 kg/ha of nitrogen fixed per year. There are clear advantages in this nitrogen-fixing capacity in terms of fertilizer use and soil fertility. 2. Shoots. The bark color varies with development stages, from pale yellow-green in young trees to grey-brown in mature trees. The mature branches, which have very visible lenticels, are weak and easily broken by wind. There are four types of shoots: rapidly growing extension shoots (water shoots), vegetative shoots, bearing shoots, and staminate flowering shoots (Miao and Wang 1987; Wang 1995). Water shoots are usually longer than 30 cm and vegetative shoots shorter than 30 cm, with longer internodes. Well-developed axillary buds on vegetative shoots are the potential fruiting shoots. New leaf and shoot growth generally arises from buds near the shoot apex (Miao and Wang 1987). The season of growth affects leaf size: The spring leaves are the biggest, followed by those produced in the summer, and then the autumn. Leaf color also varies with the season; the spring leaves are deep green, in the summer a lighter green, and autumn leaves are pale green. These characters are also used to estimate nutritional status. Leaves remain on the tree usually for 12–14 months, with a marked peak in abscission just prior to the spring growth flush. 3. Flowers. Flower buds of red bayberry are simple, forming in axillary buds and never in terminal buds, where only vegetative (leaf) buds occur. The flower bud is larger than the leaf bud, and can be distinguished in winter before budbreak. New growth in spring occurs from axillary buds on shoots grown in the previous season. Flower bud differentiation has been well studied, mainly on ‘Xiyeqing ’and ‘White’ cul-

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tivars (Li and Dai 1980). Only apical buds and 4–5 axillary buds can develop into leaf or flower primordia; the other buds remain latent for quite some time and can be stimulated to develop into shoots. This character is useful when replacement of the canopy and fruiting shoots is needed. Leaf buds break about 20 days later than flower buds, and leaf unfurling occurs about 15 days after that. Red bayberry is a typical dioecious fruit tree, but it is difficult to identify sex before flowering. G. Li et al. (1993) established a method based on isozymes patterns and composition of phenolic compounds. The flower is small, unisexual, without perianth, and is wind-pollinated. Each staminate flowering shoot can contain 2–60 inflorescences, normally between 15 and 20, and is part of a compound inflorescence that bears 15–36 catkins, each catkin composed of 4–6 staminate flowers. Staminate inflorescences form in the leaf axil, and are cylindrical or long conical in shape, with the color changing from garnet in young flowers to yellow-red or bright red in mature ones. The distal staminate flowers open first, and the flowering period can be as long as 40–50 days for a whole tree. Staminate flowers are arranged as a corymb, without pedicel or receptacle, and are surrounded by greenish white bracts. Each staminate flower has two stamens, and unequal filament length (Fig. 3.2). The filaments are yellowish red or bright red, and usually bear anthers at the apex. Anthers are kidney-shaped, bright red, fused at the base, and

Fig. 3.2.

Morphology of staminate floral structure of red bayberry (from Wang 1995).

1. Staminate flowering shoot. 2. Staminate compound catkin. 3. Individual staminate catkin. 4. Bract for compound catkin. 5. Bract. 6. Stamen.

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release yellow pollen through longitudinal splits. The pollen grains are small (20 µm diameter) and can be carried as far as 1000 m by wind (Miao and Wang 1987). Each anther holds more than 7,000 pollen grains, and each staminate inflorescence contains 200,000–250,000 pollen grains. Each pistillate flower shoot has 2–60 pistillate inflorescences, the average being 15 to 20. The catkins contain 7–26 flowers (average 14). The ovary is unilocular, and the style bright red, 0.5–1 cm in length, with a Y-shaped stigma with 2, sometimes 3–4 sites of dehiscence. Terminal flowers of the pistillate inflorescence usually flower earlier than others (Fig. 3.3), and the flowering period for a whole tree may last for about 30 days. Occasionally, mixed inflorescences occur with pistillate flowers at the top and staminate flowers at the base (Fig. 3.4). Staminate flowers open after 2–3 pistillate flowers have opened in the same inflorescence. However, pistillate flowers in a staminate inflorescence have only been reported once (Miao and Wang 1987). 4. Fruit. The fruit have stones like peach and plum, with an edible part more like a berry (Fig. 3.1). The fruit is usually spherical, and the skin has a waxy coat (Miao and Wang 1987). Fruit size varies among cultivars (Table 3.2), generally being greater than 2 cm in diameter, with some reaching 3 cm or more. Fruit of the wild types are less than 2 cm in diameter, and fruit of Myrica nana Cheval grown in Guizhou, China, are the smallest, measuring less than 1 cm in diameter.

Fig. 3.3.

Morphology of pistillate floral structure of red bayberry (from Wang 1995).

1. Pistillate flowering shoot. 2. Pistillate inflorescence. 3. Pistillate flower. 4. Bract for inflorescence. 5. Bract. 6. Pistil. 7. Longitudinal section of fruit. 8. Flesh segment.

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Inflorescences of red bayberry (from Liu 2000).

1. Staminate inflorescence. 2. Bisexual inflorescence. 3. Pistillate inflorescence.

The epicarp of the fruit consists of thin-walled parenchyma cells, in which the vascular bundles are arranged like a cup. The parenchymatous mesocarp makes up the edible portion. The endocarp consists of a hard stone with small, round, thick-walled sclerenchyma cells, most of which are flattened. The stone includes a seed coat, embryo, and large, soft, waxy cotyledon (Fig. 3.5). The epicarp and mesocarp (flesh segments) develop from the outermost layers of endocarp and usually consist of 1,100–1,300 flesh segments. The length, thickness, pointedness, and hardness of the flesh segments varies with cultivars. Tree age, yield, soil nutrition, humidity, degree of maturation, and position of fruit on the tree influence fruit quality (Li et al. 1992). More mature trees, heavier fruit loads, more abundant nutrition, drier climates, and sun exposure will result in fruit with more pointed flesh segments. In some cultivars, a single fruit may contain both round and pointed segments. The former would be located

Fig. 3.5.

Morphology of the fruit of red bayberry (from Miao and Wang 1987).

1. Epicarp. 2. Mesocarp (flesh segment). 3. Endocarp. 4. Seed coat. 5. Seed (cotyledon).

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in the middle of the fruit, with the latter in the outer parts. Fruit with round flesh segments are usually more succulent and taste better, while those with sharper flesh segments tend to have a longer storage life. III. PHYSIOLOGY A. Vegetative Growth Root growth usually commences in late February, and the root system has three major growth peaks, in late May, mid-July, and early October (Miao and Wang 1987). Vegetative growth has up to three growth flushes each year. Summer shoots are the most abundant, accounting for 60–70% of the total shoots each year, and these make up most of the bearing shoots in the following season; spring shoots, summer shoots, and sometimes autumn shoots will become flowering branches. Winter shoots can develop into bearing shoots depending on weather and nutrition (Miao and Wang 1987). Spring shoots occur from late March to late June, developing from the spring shoots or summer shoots of the previous year; summer shoots, from June to August, developing from the spring shoots of the same year and bearing shoots of the previous year; autumn shoots, from early August to October, developing mainly from the spring and summer shoots of the same year (Li 2001). Except for the cultivars ‘Biqi’ and ‘Ding-ao’, autumn shoots do not become bearing shoots, as they form too late (Miao and Wang 1987). As might be expected, spring shoots are the longest and autumn shoots the shortest. Leaves unfurl during late March to early April, and develop rapidly in May. Old leaves begin to abscise at the beginning of May, and reach an abscission peak when spring shoots stop growing. Leaf abscission is influenced by both the growing environment and the cultivar. Trees growing on clay soils, attacked by pathogens, or generally weak trees, usually shed leaves earlier, and abscission is postponed in late maturing cultivars such as ‘Wandao Yangmei’. B. Flowering and Fruit Set Flower-bearing shoots develop from the strong spring and summer shoots of the previous year. Although spring shoots are the best shoots for bearing fruit, they are not sufficient for adequate crop loads, and since summer shoots are the most abundant, they become the most important source of fruit and the key factor influencing yield in the next year (Li 2001). The fruit capacity of a bearing shoot varies with shoot length, and shoots are divided by length in the ‘Biqi’ cultivar into four types: extended, long,

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medium, and short shoots (Miao and Wang 1987). Extended shoots are more than 30-cm long with limited flower buds at the end and most of the buds will be shed after flowering. Long shoots are thin, 20–30 cm in length, with 5–6 flower buds at the end, and a low rate of fruit set. Medium shoots are 10–20 cm long, with a heavy load of flower buds except at the apex; these shoots bear the highest fruit load. Short shoots, 1–10 cm in length, some as short as 1–2 cm, carry many flower buds, with high rates of fruit set. When flowering shoots constitute about 40% of the total shoots, a high, steady yield can be predicted (Chen et al., pers. comm.), but when this ratio is more than 60%, alternate bearing may develop. Flower bud differentiation begins shortly after the cessation of summer shoot growth (Li and Dai 1980). Physiological differentiation of inflorescence primordia of the ‘Xiyeqing’ and ‘White’ cultivars occurs in early or mid-July. During the early stage of flower bud differentiation, abortive pistillate inflorescences emerge and these will be shed rather than open in the next spring. Inflorescences that differentiated after early August normally develop fruit. Morphological differentiation of the primordia of pistillate inflorescences begins in mid-July, and the first small flower primordium forms in late July. The formation of primordia of the staminate inflorescences begins at the end of the same month. Flower bud differentiation stops at the beginning of December. Physiological differentiation of the flower buds develops 2–4 weeks earlier than morphological differentiation, and takes about 3 months to complete. Autumn shoots are unable to develop flower primordia in time for the normal flowering period. Flowering date varies according to cultivar and growing conditions (Miao and Wang 1987). Some staminate flowers open in late January, some during February and March, reaching full bloom in March to April. This also happens with pistillate flowers and, as a result, individual pistillate inflorescences commonly carry fruit and opening flowers at the same time. Flowering can be divided into six stages: bud break, inflorescence break, first bloom, full bloom, end of bloom, flower drop (Miao and Wang 1987). Usually, the first bloom stage is when 5% of anthers or stigmas are exposed, full bloom stage is at 75%, and end of bloom when the anther exposes pollen and becomes yellowish-brown or the stigma wilts (Miao and Wang 1987). The period of flowering can span 39 days for staminate flowers and 27 days for pistillate flowers. Though pistillate flowers open later and last for a shorter time than the staminate ones, full bloom stage is longer (13 days) than that of the staminate flowers (5–7 days), and this benefits pollination (Miao and Wang 1987). The highest fruit set occurs in the uppermost five inflorescences on bearing shoots, but the first inflorescence is the predominant one, bearing

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20–45% of the total fruit. The rate of fruit set is only 2–4% for the whole tree (Wang 1995). The main peak in abscission of inflorescences and fruitlets is late April to early May. Additional peaks occur in the middle of May and just prior to harvest in some cultivars such as ‘Shuimei’ and ‘Hunanzhong’, but not in the cultivars ‘Dongkui’ and ‘Wandao Yangmei’ (Miao and Wang 1987). C. Fruit Development The time from fruit set to maturation is 60–70 days (Miao and Wang 1987). The fruit of leading cultivars in Guangdong and Fujian ripen during late May to early June, the early-maturing cultivars in Zhejiang and Jiangsu during middle to late June, and the late-maturing cultivars in early July. Fruit on trees in inland areas ripen earlier than in coastal areas because of greater diurnal temperature differences in inland climates. Fruit growth follows a double sigmoid curve in both fruit size (diameter; Fig. 3.6) and fruit weight. For example, ‘Biqi’ and ‘Dongkui’ fruit (Miao and Wang 1987; Gong 1995) develop rapidly and reach the max-

Fig. 3.6. Changes in length, diameter, and ratio of length to diameter during fruit development of ‘Donkui’ red bayberry (from Gong, 1995).

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imum of the first growth stage (about 20 days) just after the first peak of fruit abscission in early May. This period of rapid growth is followed by a pit hardening stage (15–20 days) and a second burst in fruit growth, characterized by increases in water content, weight, and color of fruit just prior to fruit ripening on the tree. Fruit size increases synchronously with fruit weight and there is a strong correlation between the size of the seed and the fruit. Water content of the fruit increases from the fruitlet to the pit hardening stage, then decreases gradually, before increasing again as the fruit matures (Miao and Wang 1987). The daily increment in fresh weight of the fruit flesh during the maturation stage is three times that at the first rapid growth stage; there is no similar difference in dry weight increase. The length of the pit hardening stage is influenced by fruit size as well as cultivar—the bigger the fruit, the shorter the length of the stage. Total soluble solids (TSS) contents increase with fruit maturation to the point of harvest, with sugars accumulating rapidly during the final 2–3 weeks (Chen et al. 1992). Larger fruit are commonly sweeter than smaller ones, and there is a positive correlation between TSS content and degree of pigmentation. Citric acid is the most abundant of the fruit organic acids, accounting for 97% of the total, with malic, oxalic, succinic, isocitrate, fumaric and other acids making up the remaining 3%. Chen et al. (1992) found that total acidity increased rapidly from about 40 days before harvest, but then decreased as the fruit began to ripen on the tree. Smaller fruit tend to have higher acidity than larger ones (Chen et al. 1992). The pigments responsible for the fruit flesh color (red, and purple to black) are anthocyanins, the levels of which vary with cultivar, fruit development, and environmental factors, especially light. Cyanidin-3glucoside has been identified as the principal fruit pigment, with pelargonin-3-monoside and delphinidin-3-monoside as minor components (Lin 1984; Ye et al. 1994). Chlorophyll contents decrease during fruit maturation.

IV. ENVIRONMENTAL REQUIREMENTS A. Temperature The tree performs well in tropical, subtropical, and temperate zones, with optimum temperatures of 15–20°C. It can endure winter freezing with average temperatures of more than 2°C and an absolute minimum

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above –9°C. However, the trees can be damaged and the yield for the following year reduced by more than 20% if the minimum temperature falls below –9°C and a maximum temperature of less than 0°C lasts longer than about three consecutive days. Because the flowering period is quite late, unlike peach and apricot, flower or fruit freezing seldom occurs. To get high yields and quality, the growing conditions should include an annual average temperature >14°C and accumulated temperature (>10°C) of more than 4,500 degree days. Outside these conditions, small, very acid and poor-tasting fruit are likely to be produced. High temperatures during May and June, during the second fast growth phase, also may result in fruit with high acid and low sugar contents. For example, one study has shown that when the mean May–June temperature was 20–22°C, the acid content was 0.7–1.3% and the ratio of soluble solids to acids was 9–16, but when the mean temperature was raised by 2°C, the acid content increased to 1.4–1.9% and the ratio decreased to 6–7 (Miao and Wang 1987). High temperatures (e.g., a mean temperature higher than 28°C) can cause damage, particularly to young, newly transplanted trees, and affect the development of flower buds and fruit-bearing shoots. The optimum temperature for photosynthesis of red bayberry is less than 20°C (Ruan and Wu 1991). B. Water High humidity and a plentiful water supply assures high cropping and high-quality fruit (Chen et al. 1992). In China, most trees are planted on hills and slopes without artificial irrigation (Fig. 3.1). Annual precipitation and its seasonal distribution are the most important factors influencing tree growth and fruit production. In Zhejiang, precipitation of more than 1000 mm is usually required (Li et al. 1992), and the optimum is between 1300–1700 mm. Low humidity results in poor pollination and reduced yields. Rainfall of more than 260 mm during February and April favors the growth of the root system, leaf development, blossoming, and fruit set. The period May to June is of particular importance for fruit maturation, warmth and light being needed to enhance fruit color. Rainfall of more than 160 mm is required in June, since less than 100 mm will result in small, poor-quality fruit, and a reduction in yield. Having sunny days during late summer to early autumn is beneficial for the accumulation of carbohydrates and flower bud differentiation. Most of the important commercial areas of red bayberry production in China do not have extremes of temperature and humidity.

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C. Soil A deep, fertile, acid soil with a pH of 4–5.5 is the optimum for cultivation. In mountainous areas, successful growth of plants such as Dicranopteris pedata (Houtt.) Nakaike, Rhododendron simsii Planch., pines, firs, bamboos, Cyclobalanopsis glauca (Thunb.) Oerst., Quercus acutissima Carruth., or Castanopsis sclerophylla (Lindl.) Schott. indicate suitable conditions for bayberry cultivation (Li et al. 1992). Red bayberry is tolerant of shade and can be planted in less-fertile soils and fine sandy loams. Planting in clay or sandy soils can result in weak and/or dwarfed trees. The presence of nitrogen-fixing root nodules allows the trees to perform well on infertile but well-drained slopes. In fertile flat soils, trees may have excess vegetative growth and consequently shed flowers and fruit. The species is susceptible to boron deficiency, which can result in small leaf size. D. Light Although tolerant of shade, sufficient light is needed for cropping. Ruan and Wu (1991) found that the tree had significant winter photosynthetic rates, although the net rate was usually below 1.5 mg CO2 d–1m–2. Fruit of poor quality and small size may be produced on south-facing slopes where direct light and heat is excessive (Li et al. 1992). E. Elevation and Exposure Flowering and fruiting have been shown to be delayed by up to 20 days with an increase in elevation from 50 to 600 m (Chen et al. 1989). Trees grown at between 200 and 400 m produce fruit of high quality, with soluble solids levels of 9.9–10.1% and acidity 1.8–1.55% (Chen et al. 1992). Elevations greater than 500 m are unsuitable for cultivation since annual temperatures are usually below 15°C. The trees are not tolerant of strong winds because of a shallow root system, dense branches and leaves, large canopy, and brittle shoots. V. HORTICULTURE A. Propagation The most widely used methods for propagation include seeds, grafting, and layering (Wang 1995). Propagation from seed has been the traditional practice in many areas in China, especially for rootstocks. Seeds need to

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be stratified, and are generally sown in November. The soil should be deep, well drained, and with reasonable organic matter. Soils previously used for citrus, peach, pine, cypress and red bayberry itself are usually unsuitable for sowing, probably because of nutrient depletion, with soils used for annual crops such as rice, vegetables and leguminous plants being preferred. The seeds are sown at a density of about 1.2–1.5 kg⋅m–2, and they germinate in the following spring. In April, seedlings can be transplanted to nurseries when about 7 cm high. By the time of the next spring after transplanting, the saplings are suitable for grafting. Seedlings with a stem diameter over 0.5 cm can be used as rootstocks for grafting. For scions, one- to two-year-old shoots are cut from trees over 10 years old with a history of good yields, and these are cut into several 7-cm segments after removing the leaves. The optimum time for grafting is between late March and early April in Zhejiang. A survival rate of over 70% can be achieved with cleft grafting. The growers in Xiaoshan and Lanxi in Zhejiang province often propagate red bayberry by layering, which is usually performed before bud break in spring. This method speeds up the time to production of a fruiting tree. However, the root systems of such plants are often shallow, and the growth weak. B. Field Cultivation Red bayberry is a long-lived tree and can remain productive for more than 30 years (Wang 1995). The optimum time for planting varies with regions. To avoid freezing injury in winter, planting takes place during late February to mid-March in Zhejiang, Jiangsu, Hunan, and Jiangxi. In regions with a relatively warm winter, such as in Guangdong, Fujian, Yunnan, Guizhou, and Sichuan, planting is carried out during early October to early December or from mid-February to mid-March. Planting density is about 600 trees/ha. Since the tree is dioecious, it is necessary to interplant staminate trees, at a frequency of about 1–2% (Wang 1995). Pollen grains are small and can be carried some distance by wind, and if an orchard has staminate plantings nearby, then interplanting is not always necessary. Organic fertilizer applications are commonly made in October, and green manure crops, usually leguminous plants, are often interplanted with young trees to improve soil structure and provide another source of income. For plantings on slopes, mounding up can prevent exposure of roots and promote root growth. According to Zhang (1999), a tonne of ‘Dongkui’ fruit contains 1.4 kg N, 0.07 kg P, 1.8 kg K, 0.06 kg Ca, and 0.28 kg Mg, with a ratio of N: P:

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K=20:1:26. The nutrient contents of fruit (Table 3.3) are generally lower than in many fruit crops, especially levels of P and Ca. Since nodulated roots supply part of the N requirements of the tree, K is the most important major nutrient that must be supplied from the soil. Excess P application can be harmful because of possible boron, zinc, and molybdenum deficiencies. The kinds of fertilizers used and application rates are related to plant age and soil nutrient status. For example, at a density of 270 trees/ha, fertilizers applied annually to young trees (5 years old) should contain 3.5 kg N, 0.9 kg P, and 3.0 kg K, and for adult trees (12 years old) 9.2–10.6 kg N, 2.3 kg P, and 12.3 kg K. Fertilizers should be applied three times a year: during February or March to promote spring flush growth, blossoming, and fruit set; late May for promoting fruit development; and a further application just after harvest. The trees are upright and will grow too tall if not trained, and the recommended practice throughout China is to create a tree with a low canopy and open center (Fig. 3.1). Pruning is carried out in February to March (spring) and September to October (autumn). Unwanted branches are removed or cut back to allow light penetration into the canopy to promote fruit set and increase fruit quality. For example, training of ‘Dongkui’ trees involves establishing a trunk with 3–4 primary scaffold limbs, with angles between the trunk and the limbs greater than 45°, and the height of the canopy less than 2.5–3.0 m. Groups of fruiting branches, rather than secondary scaffold limbs, should be allowed to develop on the main limbs, and these should be replaced by new groups about every 4 years (Wang 1999).

Table 3.3. The content of mineral elements in different organs of red bayberry trees (data from Zhang 1999). Fruit Nutrient Content (% dry weight) Tree age Non-bearing (5 year old)

Bearing (12 year old)

Organs

N

P

K

Ca

Mg

Leaves Shoots Roots

1.33 0.31–0.67 0.57

0.08 0.03–0.04 0.03

0.95 0.24–0.76 0.53

0.46 0.12–0.31 0.15

0.14 0.02–0.08 0.07

Leaves Fruit Shoots Roots

1.27 1.01 0.24–0.82 0.55

0.07 0.02 0.02–0.03 0.03

1.02 1.10 0.25–0.08 0.57

0.38 0.03 0.11–0.28 0.17

0.13 0.12 0.02–0.09 0.06

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Alternate bearing has been the target of recent research. Li et al. (2001) showed that spraying bayberry trees with 250 g/L GA3 in June and July inhibited the activities of PAL, POD, and PPO, and hence slowed down the biosynthesis of lignin, suppressed the differentiation of flower buds, and as a result, greatly reduced flowers in the following year. These results confirm those of Lavee (1989), who found that phenylalanine ammonia lyase (PAL), peroxidase (POD), polyphenol oxidase (PPO), and lignin were related to formation of flower buds. GA3 treatment promoted the emergence of spring shoots by 133%, increased the size of flower buds on spring shoots, and increased fruit weight by 3.8 g, soluble solids by 3.4%, and advanced maturity by 3 days (Liang et al. 2000). Paclobutrazol (PP333), an inhibitor of GA biosynthesis, applied in autumn or spring to arrest the vigorous growth of young trees, accelerates the formation of flower buds. However, Luo and Huang (1997) reported that spraying trees with PP333 at 500 mg/L in spring decreased fruit size and sugar content while increasing acid levels. Trunk spiral girdling also effectively promotes flower formation (Luo et al. 1999). In China, growing red bayberry in greenhouses was first carried out in Wenzhou, Zhejiang in 1999–2000 with ‘Ding-ao’ (Huang and Zhao 2001). The system has proved to be profitable, with fruit in the market early in the season realizing higher prices. The plastic house, 20 m × 10 m × 4.5 m, resulted in average temperatures being increased by 4.5°C, humidity by 7.5%, the ripening date being advanced by 14–16 days, and yields being increased by 11.5%. However, the time from fruit set to full maturation did not change, remaining at about 106 days. C. Pests and Diseases There are important disease and pest problems in red bayberry (listed in Table 3.4), and although studies on these are generally limited, there is some information available in the literature. Pseudomonas syringae pv. myrigae is one of the most widely distributed pathogens, infecting 2- to 3-year-old shoots and resulting in a tumor-like growth known as red bayberry ulcer or sore (Li 2002). Smooth, milky tubercles arise at the infected sites, and then develop into larger, rough, brown or black tumors, 1.5–2 cm in diameter. The symptoms become apparent about 30 days after infection. The disease develops in late April to May, and protective methods involve removal and burning of infected shoots followed by a 0.5% Bordeaux spray. Brown leaf spot results from infection of Mycosphaerella myricae Saw. The round or irregular spots are 4–8 mm in diameter, with brown

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Table 3.4. Major pathogens and pests of red bayberry (data from Chen 1994; Cai 2000; Rao et al. 2001). Disease or pest Disease Brown leaf spot Root rot Rust Tumor-like growth Red mould Stem blight Shoot rot Nematode Root-knot Insect Leaf wilt moth

Scale insect Leaf rolling moth Scale insect Fruit fly White ant White ant

Affected tissue

Production area

Mycosphaerella myricae

Leaves

Zhejiang

Botryosphaeria dothidea Caeoma makinoi Kusano Pseudomonas syringae pv. myricae Corticium saimonicolor Myxosporium corticola

Roots Leaves Shoots, trunk

Valsa coronata

Cortex of shoot

Zhejiang Fujian Zhejiang, Japan Zhejiang All producing areas Zhejiang

Meloidogyne spp.

Roots

Fujian

Lebeda nobilis

Leaves

Lepidosphes cupressi Homona spp.

Spring leaves Young leaves

Jiangsu, Zhejiang, Fujian Zhejiang Zhejiang

Fiorinia myricae Drosophila melanogaster Odontotermes formosanus Macrotermes barneyi

Fruit Fruit Trunk, root Trunk, root

Japan Japan Zhejiang Zhejiang

Binomial

Branches Trunk

or greyish-brown borders and reddish-brown or greyish-white centers. The spots can coalesce and may result in leaf wilting and abscission. Control is through use of fungicides such as a 0.5% Bordeaux spray, and 70% thiophanate methyl and 50% carbendazol wettable powders, sprayed onto foliage one month before full fruit ripening, two weeks prior to harvest, and after harvest (Li 2002). Root rot is an important disease in Zhoushan Island of Zhejiang Province. The pathogen has been identified as Botryosphaeria dothidea (Moung ex Fr.) Ces. & de. Not. (Li et al. 1995), with infection spreading through the root system, resulting in wilting and tree death. Control is through soil applications of carbendazol at 0.25–0.5 kg/tree or thiophanate at 0.25–0.5 kg/tree (Ren et al. 2000).

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Scale insects are common and important pests resulting in severe yield losses and decline in fruit quality; they include Lepidosaphes cupressi Borchsenius in Zhejiang and Jiangsu areas of China, and Fiorinia myricae Targioni in Japan (Xu et al. 1995; Mao 2000). Lepidosaphes cupressi feed on foliage and have two reproductive cycles per year, egg-laying being in mid-April and late July. Insecticides such as buprofezin are used for control, in combination with agriculture practices and native predators such as Chilocorus kuwanae Silvestri and Prospaltella spp. (Xu et al. 1995). D. Harvest and Handling Bayberry fruit are picked when eating ripe. Fruit maturation and time of ripening on the tree varies greatly with growing region. The fruit ripen in early April in Guizhou, from mid- to late May in Fujian, Guangdong, and Sichuan, and from early June to mid-July in Zhejiang, Anhui, Jiangsu, Hunan, and Jiangxi. In most regions, high temperatures and rain are common at the time of fruit ripening, making them susceptible to preharvest drop and rots, resulting in a comparatively short harvest time (Liu 2000). Fruit maturation also varies with cultivars, and since unripe fruit are excessively acid, estimation of maturity and the appropriate harvest time is important. Flesh color is a useful indicator of ripeness and is used as a harvest index. For example, color changing from red to purple or black indicates ripeness for the black type, from bluish green to white for the white type, and from green to deep red for the red type. The soluble solids contents increase in the fruit with ripening, while total acid levels decrease. The optimum acid content for harvest is between 1–1.2% for ‘Biqi’ fruit (Miao and Wang 1987). Individual fruit on a tree ripen at different times, and fruit often have to be picked as frequently as every day. Since the fruit are susceptible to mechanical injury, careful handling is necessary. The optimum times for picking are early morning and evening, when the field heat is least. The flesh is susceptible to damage from pickers, and current recommendations are that fruit should be picked with stalk attached, and packed in 3–5 kg bamboo baskets with leaves or weeds to reduce damage. Fruit shaken from the trees can only be used for processing. E. Storage and Transportation Red bayberry is a delicate fruit and has a short storage life, made shorter by enhanced flesh softness resulting from high temperatures and rain at harvest. The storage life of the fruit is 9–12 days at 0–2°C, 5–7 days at

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10–12°C, and 3 days at 20–22°C (Xi et al. 1993). There is a need for more research on extending the storage and shelf life of the fruit, particularly if it is to be used more widely as an export crop. As the fruit ripens, the total soluble solids (TSS) contents increase and acid levels decrease, resulting in higher ratios of TSS to acids. Sugars are the main constituents of TSS, and sucrose is the principal sugar, accounting for about 60% of the total. Citric acid is the predominant acid, with oxalic acid as the next most abundant; acetic and malic acids are minor components. Fruit quality declines rapidly during storage. For example, after storage at 0–2°C for 12 days, fruit TSS decreased by 10.5%, total acids by 41.4%, sucrose by 49.1%, and vitamin C by 36%, from 432 µmol/L to 277 µmol/L (Xi et al. 1993). These decreases can be retarded by treatment with salicylic acid, an inhibitor of plant senescence (Gao et al. 1989). Cell membrane permeability, measured by changes in electrical conductivity of tissue, increases during fruit storage, and is greater at higher temperatures (Xi et al. 1994). These permeability changes, along with increased respiration and ethylene production, increase under vibrational stress, such as may occur during postharvest handling and transport (Ying et al. 1993; Zheng et al. 1996). There are different views on the respiration pattern of ripening red bayberry fruit. Xi et al. (1994) classified it as nonclimacteric, whereas Hu et al. (2001) regarded it as climacteric because they detected a small ethylene production peak both at 21°C and 1°C. Ethylene production during storage may be dependent on fruit maturity at harvest, since less mature ‘Biqi’ fruit (picked at the pink stage) showed some increase in ethylene production after harvest (Fig. 3.7; K. Chen et al., unpublished data). The activity of superoxide dismutase (SOD), a free radical scavenger and thus a protectant against oxidative stress, gradually increases in the fruit during the first 6 days after harvest, and then decreases rapidly, following a pattern familiar in senescing tissues. High storage temperatures and vibration stress accelerate this decline in SOD activity (Xi et al. 1994; Zheng et al. 1996). The levels of SOD in vibration-stressed fruit were less than those in control fruit, supporting the observation that such stress can promote fruit senescence (Zheng et al. 1996). Malondiadehyde (MDA), a product of membrane peroxidation, which itself can further damage membrane structure and function, has been followed during storage. Fruit stored at 1°C or under high nitrogen (85%) had substantially lower contents of MDA and a longer storage life (Xi et al. 2001). Another group of metabolites, polyamines including spermidine, spermine, and putrescine, share the same precursor as ethylene in their biosynthetic pathway. In a study of vibration stress on bayberry

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Fig. 3.7. Changes in ethylene production of ‘Biqi’ red bayberry fruit of different maturity (K. Chen et al., unpublished data).

fruit, synthesis of spermidine increased whereas ethylene production decreased during the initial post-vibration storage period, suggesting a possible protective metabolic system (Zheng et al. 1996). At a later stage, spermine content decreased while ethylene was produced at a higher rate than in control fruit, suggesting that vibrational stress ultimately accelerated the overall senescence process. Putrescine accumulated during the final storage period, and may be detrimental to fruit storage. Storage life of the fruit can be extended up to two weeks if fruit are stored at 0–1°C, with a relative humidity of 85–90% (Xiao et al. 1999; Xi et al. 2001). Postharvest treatments such as sodium sorbate, 1% salicylic acid, or 0.5% CaCl2 together with 7.5 mg/L NAA (Liu 2000) increased storage life, although 1-MCP (the inhibitor of ethylene reception) had little effect (K. Chen et al., unpublished data). Modified atmosphere packaging and controlled atmospheres have not been studied to any great extent.

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In China, red bayberry is traditionally picked from the tree directly into bamboo baskets, and then transported to the market. Because of the increasing commercial production and value of the crop, packaging of the fruit has greatly improved. Fruit are graded by size and color to provide uniform packs. In Yuyao, Zhejiang province, high-quality ‘Biqi’ fruit are selected and packed in 500-g plastic boxes, then in 3-kg cartons, and shipped to Hong Kong. ‘Dongkui’ fruit, being larger and of higher quality, are packed 10 to a plastic box. Good results have also been achieved with other cultivars by changing the number of fruit in a box (Lu et al. 1999). In Japan, red bayberry are packed in 400-g polyethylene bags and then into 1.6-kg wooden or plastic boxes (Miao and Wang 1987). Because they are susceptible to rots, fruit should be precooled before packing and transported carefully to avoid vibration and high temperatures. Since the short storage life limits the period of supply to the market, there are benefits in freezing. Fresh fruit can be blast-frozen at –25 to –30°C for 15 minutes, and then stored and transported at –18°C. F. Processing Red bayberry fruit can be processed into jam, juice, wine, or as candied products, and canned red bayberry fruit is exported from China, particularly to Southeast Asian countries. Recent annual production of the canned product in Zhejiang has reached 1,800 t, about a third of which is exported. Ye and Zhang (2000) have shown that the fruit pigments can be used as food additives, although they are readily affected by pH, ultraviolet light, and reducing agents. Rapid and simple carbon dioxide supercritical extraction technology is needed for pigment extraction. The pigments have good potential uses so long as stability can be assured. Juice can be extracted with 2% saline at 70–80°C, and the preferred product contains 40% original extract, 10.5% sugar, and 0.45% acid (Zheng and Chen 2000). Red bayberry wine is also an important product of the fruit. Relatively high pectin and cellulose contents are largely responsible for the existence of methanol in the wine, and this needs to be kept at levels less than 0.08 mg/100 ml (Huang 1999). The composition of red bayberry fruit is summarized in Table 3.5. In addition, three flavonoids have been isolated from the fruit stone and identified by spectral analysis as quercetin, myricetin, and quercetin-3-O-αD-glucopyranosyl-(6→1)-α-α-L-rhamnopyranoside (Zou 1995). These compounds, especially quercetin and myricetin, are active antioxidants.

110 Table 3.5.

K. CHEN, C. XU, B. ZHANG, AND I. FERGUSON Chemical composition of ripe red bayberry fruit. Content (fresh weight basis)

Component

Reference

Total soluble solids Total sugars Sucrose Glucose Fructose Total acids Citric acid

11.6–13.4% 9.8–11.7% 46.6 mg/g 13.5 mg/g 13.8 mg/g 0.42–1.28% 0–10.3 mg/g

Tartaric acid Malic acid Succinic acid Acetic acid Oxalic acid Minerals Potassium Trace elements (Fe, Mn, Zn, Cu, Mg) Vitamins Vitamin C (ascorbic acid) Vitamin B1 Vitamin B6 Vitamin E Vitamin A Protein

1.2–4.5 mg/g 1.3–1.7 mg/g 1.2–3.1 mg/g 0.5–2.0 mg/g 1.9 mg/g

Wang et al. 2001 Wang et al. 2001 Zhang et al. 1991 Zhang et al. 1991 Zhang et al. 1991 Wang et al. 2001 Zhang et al. 1991; Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Zhang et al. 1991

1.41 mg/g 0.075 mg/g

Wang et al. 2001 Miao and Wang 1987

0.11–1.14 mg/g

Wang et al. 2001

0.054 mg/g 0.008–0.016 mg/g 0.0007–0.0016 mg/g 0.00004–0.0005 mg/g 0.33%

Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Zhang et al. 1991

There are also some unknown compounds in the stones that can arrest the growth of cancer cells or induce cell death (Zhang et al. 1993).

VI. CONCLUDING REMARKS China has a rich genetic resource in red bayberry, with a wide range of cropping and fruit properties that should be exploited for breeding purposes. Some wild species fruit early, resist high temperature, are dwarfing, and have excellent postharvest properties. Many contain compounds of medical importance. These resources are in danger of being destroyed; species such as Myrica esculenta Buch are on the edge of extinction.

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There are 268 cultivars planted in China, of which about two-thirds ripen in mid- to late June (Zhang and Miao 1999). There are some earlymaturing cultivars such as ‘Zaoxingmei’ grown in Huangyan and Wenling, Zhejiang province, that ripen in May, but the fruit is small and acid. The storage life of almost all cultivars is very limited, resulting in severe losses each season. It is imperative that further breeding work be carried out to create new early-maturing cultivars of high fruit quality and longer storage potential. Only 9.3% of total cultivars are white fleshed (Miao and Wang 1987), and only one, ‘Shuijingyangmei’ or ‘Crystal’, has been commercially planted, in Shangyu, Zhejiang province, its place of origin. There is a need for more effort in breeding new white-fleshed cultivars adapted to different climates. Alternate bearing has a major impact on production; in years of high yield, the price of fruit may be low, while in low years there may be insufficient fruit to meet consumer demand. Furthermore, compared with other fruit crops, the yield of red bayberry is quite low. This means that there is a need to increase yield and reduce cropping variability. The short storage life, together with other cultivation, harvesting, and handling problems has inhibited the development of the crop. Red bayberry is a candidate for international markets provided that storage and shelf life of the fruit can be extended. The crop has potential outside of China in warm-temperate and sub-tropical growing conditions. With current limitations on storage life, production would need to be aligned with easily accessible markets.

LITERATURE CITED Cai, H. 2000. Occurrence and control of rust on red bayberry (in Chinese). South China Fruits 29:28–29. Chen, F. Y. 2000. Survey, evaluation and utilization of bayberry resources in Zhejiang (in Chinese). Guangxi Hort. 31:16–17. Chen, Y. B. 1994. Study of advances in occurrence and control of diseases and pests on red bayberry (in Chinese). Subtrop. Plant Res. Commun. 23:64–68. Chen, Z. Y., S. Y. Li, M. E. Ye, and S. C. Qin. 1992. A study on the relationship between climatic ecological factors and fruit quality of red bayberry (in Chinese). J. Zhejiang Agr. Univ. 18:97–103. Chen, Z. Y., S. Y. Li, M. E. Ye, and Z. W. Yu. 1989. Effects of altitude on flowering and fruit quality of red bayberry (in Chinese). J. Zhejiang Agr. Univ. 15:302–304. Chi, W., J. Xu, L. Y. Guo, and Y. S. Zheng. 2000. Effects of polyphenols from red bayberry on protection of blood cells and hemopoietic tissues from injuries (in Chinese). Traditional Chinese Drug Research & Clinical 11:20–22.

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Gao, J. C., M. Y. Yuan, W. L. Gu, and R. J. Xu. 1989. Effects of salicylic acid (SA) on physiological processes and quality of red bayberry fruit (in Chinese). Food Sci. (6):42–43. Gong, J. Q. 1995. An investigation on growth of fruit and shoots of ‘Dongkui’ red bayberry (in Chinese). Fujian Fruits (1):24–25. Guo, S., and S. Y. Li. 1994. Preliminary study on utilization of karyotype analysis in classification of red bayberry (in Chinese). Shu Guo’s Corpus on Citrus Research. p. 129–137. Hu, X. Q., X. Yu, and L. G. Chen. 2001. Studies on some physiological characters of Chinese bayberry fruit during storage (in Chinese). J. Zhejiang Univ. (Agr. & Life Sci.). 27:179–182. Huang, J. Z., and Y. G. Zhao. 2001. Studies on protected culture of Ding-ao Yangmei (in Chinese). South China Fruits 30:33. Huang, Y. D. 1999. The formation of methanol in red bayberry wine and the analysis of the toxicity of methanol (in Chinese). Liquor-making Sci. & Technol. 92:60–61. Ji, H. 304. Nan Fang Cao Mu Zhuang (A prospect of the plants and trees of the southern regions). Commercial Press, Beijing, P. R. China. (Printed in 1955.) Lavee, S. 1989. Involvement of plant growth regulators and endogenous growth substances in the control of alternate bearing. Acta Hort. 239:311–322. Li, G. L., B. N. Lin, and D. X. Shen. 1993. Sex identification of horticultural dioecious plants by phenolic analysis (in Chinese). Acta Hort. Sin. 20:397–398. Li, H. Y., R. B. Gao, and Y. M. Hu. 1995. The symptoms and pathogen of the bayberry (Myrica rubra) root rot (in Chinese). J. Zhejiang Agr. Univ. 21:398–402 Li, J. 2001. Practical techniques of pruning and top grafting of South China fruits (in Chinese). China Agr. Press, Beijing, P. R. China. Li, S. Y. 2002. Encyclopedia of Zhejiang agriculture—Red bayberry (in Chinese). China Agr. Sci. & Technol. Press, Beijing, P. R. China. Li, S. Y., and S. Z. Dai. 1980. A study on flower bud differentiation of red bayberry (in Chinese). Acta Hort. Sin. 7:9–16. Li, S. Z. 1578. Compendium of Materia Medica (in Chinese). People’s Medical Publishing House. Beijing, P. R. China. (Printed in 1978.) Li, X. J., J. L. Lu, and S. Y. Li. 1999. Advances in bayberry research in China (in Chinese). J. Sichuan Agr. Univ. 17:24–229. Li, X. J., S. Y. Li, J. L. Lu, and G. Y. Wang. 2001. Effects of gibberellic acid on leaf lignin levels, related enzymes and flower formation in bayberry (in Chinese). Acta Hort. Sin. 28:156–158. Li, Z. L., S. L. Zhang, and D. M. Chen. 1992. Red bayberry (Myrica rubra Sieb. & Zucc.): A valuable evergreen tree fruit for tropical and subtropical areas. Acta Hort. 321:112–121. Li, Z. Z., J. B. Huang, L. C. Yang, Z. Q. Li, and F. G. Xie. 1993. Nitrogen-fixing activities of Myrica rubra root nodules and evaluation of the amount of nitrogen-fixation (in Chinese). Fujian Res. Inst. Forestry 20:36–38. Liang, S. M., S. L. Miao, and B. S. Jin. 2000. Effects of gibberellins on flowering control in red bayberry (in Chinese). Acta Agr. Zhejiang 12:147–150. Lin, B. N., L. J. Xu, and C. L. Jia. 1999. Studies on identification and classification of genomic DNA in Myrica by RAPD analysis (in Chinese). Acta Hort. Sin. 26:221–226. Lin, D. Y. 1984. Study on the pigments of red bayberry (in Chinese). China Fruits 4:47–49. Liu, Q. 2000. Handbook for cultivation of special local fruits in South China (in Chinese). China Agr. Press. Beijing, P. R. China. Lu, D. H., X. Z. Lin, and Z. G. He. 1999. Study on fruit storage of red bayberry (in Chinese). Fujian Fruits 100:11–12.

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Luo, Z. Y., and J. H. Huang. 1997. Effects of PP333 on growth and fruit set of young trees of ‘Dongkui’ red bayberry (in Chinese). J. Hubei Inst. National (Nat. Sci. Ed.) 15:13–16 Luo, Z. Y., J. H. Huang, T. Y. Xiang, and D. H. Wang. 1999. Effects of spiral girdling on maintaining flowers and fruit of ‘Dongkui’ red bayberry (in Chinese). South China Fruits 28:25–26. Mao, Q. M. 2000. Main pests endangering Myrica rubra in Ningbo and their prevention and control (in Chinese). J. Zhejiang Sci. & Technol. 20:66–68. Miao, S. L., S. B. Huang, S. M. Liang, and Y. J. Zhang. 1995. Study on ecological regionalization of Myrica rubra in China (in Chinese). J. Zhejiang Agr. Univ. 21:366–372. Miao, S. L., and D. X. Wang. 1987. Red bayberry (in Chinese). Zhejiang Sci. & Technol. Press, Hangzhou, P. R. China. Qu, Z. Z., and Y. W. Sun. 1990. Fruit species (in Chinese). China Agr. Press, Beijing, P. R. China. Rao, J. S., C. G. Ding, L. H. Chen, and Y. C. Zhu. 2001. Occurrence and control of Corticium saimonicolor on red bayberry (in Chinese). Plant Protect. Technol. & Exten. 21:23–33. Ren, R. H., Y. M., Hu, H. Y. Li, and L. B. Cao. 2000. Studies on red bayberry root rot and control. South China Fruits (in Chinese) 29:32–33. Ruan, Y. L., and L. M. Wu. 1991. Studies of photosynthetic characteristics of wintering loquat and bayberry (in Chinese). Acta Hort. Sin. 18:309–312. Wang, B. B., Y. P. Zheng, Z. J. Li, and W. W. Yu. 2001. Utilization of Myrica rubra resources in Zhejiang and their ecological effects (in Chinese). J. Zhejiang Forestry College 18:155–160. Wang, D. X. 1987. Cultivation of red bayberry in Japan (in Chinese). China Fruits 32:57–59. Wang, H. Y., and W. N. Huang. 1990. Observations on the structure and ultrastructure of root nodules and nitrogenase activity in Myrica rubra (in Chinese). Acta Phytophysiol. Sin. 16:152–157. Wang, J. B. 1995. Pomology of individual fruits (for Southern China, Second Edition) (in Chinese). China Agr. Press, Beijing, P. R. China. Wang, P. L. 1999. Growth characters of ‘Dongkui’ red bayberry and techniques for high yield (in Chinese). Fujian Fruits 1:45–47. Wang, W. M., and Y. B. Chen. 1989. Effects of planting red bayberry on infiltration and erosion control of deteriorated soil (in Chinese). Sci. & Technic. Info. Soil & Water Conserv. 1:18–20. Wu, G. M.1984. Taxonomy of temperate fruits in China (in Chinese). Agr. Pub. House, Beijing, P. R. China. Wu, G. M. 1995. Precious southern Yangtze fruits (in Chinese). Dept. Hortic., Zhejiang Agr. Univ., Hangzhou, P. R. China. Wu, X. L., and X. P. Gu. 1994. A study on the characteristics of nodulation and nitrogen fixation in Myrica rubra (in Chinese). Forest Res. 7:206–310. Xi, Y. F., Z. S. Luo, D. Cheng, X. Cheng, and Y. G. Wang. 2001. Effect of CA storage on active oxygen metabolism in Chinese bayberry fruit (Myrica rubra) (in Chinese). J. Zhejiang Univ. (Agr. & Life Sci.) 27:311–313. Xi, Y. F., Y. H. Zheng, D. M. Qian, and T. J. Ying. 1993. Effects of storage temperature on changes in nutritional composition and decay rates in fruit of red bayberry (in Chinese). Bul. Sci. Technol. 9:254–256. Xi, Y. F., Y. H. Zheng, T. J. Ying, J. F. Ying, and Z. L. Chen. 1994. Senescence physiology of Chinese bayberry fruit during storage (in Chinese). Acta Hort. Sin. 21:213–216. Xiao, Y., J. C. Huang, and H. B. Li. 1999. Study of the effect of calcium and NAA treatments on the storage of red bayberry (in Chinese). J. Southwest Agr. Univ. 21:307–310.

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Xu, C. M., D. R. Zhou, and X. Y. Wu. 1995. Studies on occurrence and control of Lepidosaphes cupressi Borchsenius on Myrica rubra. J. Nanjing Agr. Univ. 18:57–62. Ye, R. Y., and J. Zhang. 2000. The analysis of physical and chemical characters of red bayberry (in Chinese). Exploit. Agr. & Pastur. Product. 1:11–12. Ye, X. Q., J. C. Chen, and P. Shu. 1994. Identification of the constituents of Yangmei (Myrica rubra cv. Biqi) (in Chinese). J. Zhejiang Agr. Univ. 20:188–190. Yi, Y., and N. Liu. 2000. Comparison of the quercetin contents in leaves of different types of Myrica nana Cheval (in Chinese). J. Plant Resour. & Environ. 9:59–60. Ying, T. J., C. R. Chen, Y. F. Xi, and Y. H. Zheng. 1993. Respiration reactions and cell membrane permeability changes in red bayberry (Myrica rubra) fruit under vibration stress (in Chinese). J. Zhejiang Agr. Univ. 19:80–81. Yu, D. J. 1979. Taxonomy of fruits in China (in Chinese). Agr. Pub. House, Beijing, P. R. China. Zhang, W. M., L. M. Wang, S. R. Zhang, and J. Y. Xu. 1993. A preliminary study on use of red bayberry stones to kill or constrain gastric cancer cells (in Chinese). Acta Chin. Medicine & Pharmacol. (3):38. Zhang, Y. J. 1999. The analysis of mineral nutrient absorption of Chinese bayberry (Myrica rubra) Dongkui over a whole year (in Chinese). Acta Agr. Zhejiang. 11:208–211. Zhang, Y. J., and S. L. Miao. 1999. Resources of red bayberry and its utilization in China. South China Fruits (in Chinese) 28:24–25. Zhang, Y. J., S. L. Miao, D. X. Wang, X. J. Qi, S. M. Liang, and Z. L. Chen. 1991. Alteration of pigments and the major endogenous components of fruits of colored bayberry (Myrica rubra) varieties during pigment development stage (in Chinese). J. Zhejiang Agr. Univ. 3:198–201. Zheng, M. F., and X. H. Chen. 2000. Red bayberry fruit extraction and the production of its juice (in Chinese). Light & Textile Indust. Fujian 130:9–11. Zheng, Y. H., T. J. Ying, Y. F. Xi, L. C. Mao, and Z. L. Chen. 1996. Effects of vibrational stress on postharvest senescence physiology of Chinese bayberry fruit (in Chinese). Acta Hort. Sin. 23:214–234. Zhong, Z. X., J. P. Qin, X. F. Chen, and G. F. Zhou. 2000. Hypoglycemic effect of ampelopsin on diabetic rats induced by steptozotocin (in Chinese). Guangxi Sci. 7:203–205. Zou, Y. H. 1995. Study on the antioxidant ingredients of edible oils in the fruit kernel of Myrica (in Chinese). Chem. & Indust. Forest Product. 15:13–17.

4 Protected Cultivation of Horticultural Crops in China* Weijie Jiang, Dongyu Qu, and Ding Mu Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences 12 Zhongguancun S. Street, Beijing 100081 China Lirong Wang Zhengzhou Fruit Research Institute Chinese Academy of Agricultural Sciences Zhengzhou, Henan Province 450009 China I. INTRODUCTION II. THE ENERGY-SAVING GREENHOUSE A. General Information B. Structure C. Advantages and Disadvantages III. VEGETABLE CROPS A. Mechanization of Vegetable Seedling Production B. Soil-less Systems C. Nutrient Solution and Substrate D. Disease and Insect Control IV. FLORICULTURE A. Present Situation B. Facilities and Equipment C. Commercial Flower Production V. FRUIT TREES A. Present Situation B. Cultivars C. Cultural Techniques VI. FUTURE DEVELOPMENT OF PROTECTED HORTICULTURE LITERATURE CITED *Acknowledgment: The authors thank Professor Guanghua Zheng for his valuable contribution to the preparation of the manuscript. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 115

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I. INTRODUCTION Protected horticulture production has a long history in China. In the Hanshu, a history written in the Han Dynasty (206–23 B.C.E.), China had begun to grow alliums such as Welsh onion and leek in heated structures during the winter. In the Tang Dynasty (618–907 C.E.), natural hot springs were used for vegetable growing in winter. In the Song Dynasty (960–1279 C.E.), a simple greenhouse covered with translucent paper had been developed to grow vegetables, and flowers, and in the Ming Dynasty (1368–1644 C.E.), these greenhouses were used to grow flowers during winter around Beijing (Fig. 4.1). Horticultural production within glass greenhouses occurred in Shanghai at the end of the 19th century, and commercial greenhouses for special pot production for species such as Gloxinia and Begonia tuberosa had started at the beginning of the 20th century (Zhang 2001). Windbreaks (Fig. 4.2) and solar, lean-to greenhouses (Fig. 4.3) were constructed in Northern China in the 1950s. At the beginning of 1960, polyvinyl chloride (PVC) and polyethylene (PE) film were produced for agricultural use in the Beijing and Shanghai areas, which promoted the development of medium-high (0.8–1.5 m) and low (<0.8 m) tunnels. In 1965, a 700 m2 plastic high tunnel (>2.0 m high) was built to grow spring cucumber very successfully in Jilin province, where winter temperatures reach –30°C. In 1980, low-density polyethylene film was produced and galvanized steel pipe was used to build plastic high tunnels in the Beijing area, but the area of primary protected horticulture was only 16,000 ha. Protected horticulture developed very rapidly in China after 1981, especially during the 1990s. The total area of protected horticultural crops reached 1,401,000 ha in 1999. China is now the leading country in the world for protected horticulture, including multi-span greenSunlight Roof

Paper Ground Wall

Figure 4.1 A special type of greenhouse for growing flowers during the Ming Dynasty. Oiled paper is also used.

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Figure 4.2

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Windbreak used in China in the 1950s.

houses, solar, lean-to greenhouses, and plastic tunnels (Zhang and Li 1999; Jiang et al. 2000). Solar, lean-to greenhouses, with or without heating systems, and large, plastic high tunnels developed very rapidly in China. In 1995, solar, lean-to greenhouses and large high tunnels accounted for about 45% of the total area of protected horticulture, and by 1999 the proportion had increased to 59%. Low tunnels decreased from 55% to 41% of total area from 1995 to 1999 (Zhang and Li 1999) due to low production efficiency, inconveniences, and a higher labor input requirement. Plastic high tunnels and low tunnels are widely used for commercial horticultural crop production all over China (Fig. 4.4). In the north, where winter is cold, plastic tunnels are used mainly in early spring and late autumn. In the south, where winter is mild, plastic tunnels can be used all year (Zhang 2001). In the mid-1980s, a new type of “energy-saving, solar, lean-to greenhouse” was developed in Liaoning province of Northeast China that was adapted for producing cucumber, tomato, eggplant, and watermelon without heating during the winter season. This “energy-saving” greenhouse has been extended to the whole of North China from latitude 33°N to 47°N, and has made a great contribution to the vegetable supply of cities. The area of energy-saving greenhouses was 104,413 ha in 1995 and 200,000 ha in 1999, a 92% increase (Zhang and Li 1999; Chen 2001). All types of protected horticulture have developed rapidly since 1990,

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Figure 4.3

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Solar lean-to greenhouse used in China in the 1950s.

especially in the last 5 years, but the proportion of each type has changed (Table 4.1). Modern greenhouses in China started in the late 1970s, with 21 ha of metal-frame greenhouses imported from 1978 to 1994. On the basis of this introduced technology, China developed its own technology in the late 1980s. This includes large-size tunnels, single-span glasshouses, and double-pitched glasshouses, mainly with a gate-type steel frame structure. In the 1990s, and especially after 1995, the large-scale introduction of foreign greenhouse facility and cultivation technology stimulated

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Figure 4.4

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Plastic tunnel for sinuatum production.

the rapid development of protected horticulture. As of 1995 the total area of the multi-span greenhouse was only about 45 ha. In 1999, it was 588 ha, a 12-fold increase over 1995, of which 180 ha were imported (Table 4.2) and 408 ha were locally made. Modern greenhouse coverings include glass, poly-carbonate (PC), and polyethylene (PE). Glasshouse structures include gate-type steel frame and Venlo-type. The structure of the PC house is similar to the glasshouse, but the glazing material is PC sheet or a combination of PC sheet and PE film. Plastic house structures include arch roof, saw-tooth type, double-pitched roof, Table 4.1.

Area of protected horticultural production in China. Greenhouse area (ha)

Year

High tunnel

Low tunnel

Heated

Solar lean-to

Energy-saving solar lean-to

Total (ha)

1981 1985 1990 1995 1997 1999

1,253 11,766 30,273 186,620 190,580 459,773

4,940 46,473 98,213 333,893 424,160 568,586

300 2,296 3,800 4,793 6,806 14,660

706 6,760 18,380 69,413 78,200 152,293

— 420 8,286 104,413 141,340 200,000

9,180 69,700 160,942 701,127 843,083 1,397,311

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Area (ha) 60.7 33.9 28.5 25.0 10.0 6.2 3.2 2.8 180.3

and double-deck structure (Zhou and Cheng 1998; Zhou and Wang 2001). Modern multi-span greenhouses (Fig. 4.5) have been increasingly researched by Chinese horticulturists, due to the high technology, capi-

Figure 4.5 Multi-span greenhouse for tomato production in eco-organic type soil-less culture system.

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tal, and energy inputs required. Generally, the height of the greenhouse is 4.3–6.0 m and the span is 8–11 m. It has roof and side ventilation, automatically controlled temperature and irrigation systems, and it is covered with glass, PC sheet, plastic film, or double-layer plastic film. Usually, the greenhouse area is 3,000 to 10,000 m2. The cost of constructing this type of greenhouse is US$50–$120/m2, depending on the covering material used and how the greenhouse is equipped. For production of high-quality horticultural crops, the greenhouse requires systems for heating, shading, fertigation, ventilation, and light supplementation. In recent years, due to the expanding greenhouse market in China, many greenhouse enterprises have been established, including those owned by foreign companies [FatDragon (USA), Richel (France), Ach-Olive (Spain)] as well as domestic companies (Jing-peng and Shanghai Long-march). Although the area of the modern greenhouse in China has been increasing sharply, the outputs are unsatisfactory due to poor equipment in the greenhouses, lack of essential knowledge by growers, and lack of adaptation of foreign greenhouses to local conditions. As a consequence, the market proportion of domestic greenhouse companies has been rising continuously in the past three years. Nets for shading and insect control had been used for raising seedlings derived from tissue culture before 1987. In 1988, shading nets were used for commercial production of vegetables, and have expanded rapidly since the 1990s. In 1999, the area of shading net was 16,000 ha, and use of insect net was 73,000 ha. The development of protected horticulture has increased vegetable production in China, especially in winter. The annual consumption of protected vegetables increased from 0.2 kg per capita in 1981, to 24 kg in 1995 (Zhang and Li 1999), and 52 kg in 2000. At present, only 7% of the protected horticulture area (100,000 ha in 1999) is planted to tree and vine fruits (peach, nectarine, grape, cherry, strawberry, and melon), and to flowers. These crops are more profitable than vegetables, so an increase can be expected in the future. II. THE ENERGY-SAVING GREENHOUSE A. General Information Since the mid-1980s, the energy-saving greenhouse (also referred to as an “energy-saving, solar, lean-to greenhouse”) has developed very rapidly in North China (33°N to 47°N). The total area of this type of greenhouse reached 200,000 ha in 1999 (Zhang and Li 1999). The energy-saving greenhouse (Fig. 4.6) was developed from the Chinese

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Figure 4.6

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Basic structure of a typical energy-saving greenhouse.

traditional lean-to greenhouse in Anshan, Liaoning province of North China in the mid-1980s (Chen 1991, 1994, 2001). It is composed of a north (or back) wall, and east and west gable walls for insulation against the cold outside wind. The walls are constructed with bricks and thermal-preservation materials. The front roof has a transparent plastic film for receiving sunlight. During the night, the plastic film is covered by a mat made of insulating materials. In the morning, once the air temperature inside the greenhouse rises, the mat is rolled up. In the afternoon, when the air temperature inside greenhouse goes below 17°–18°C, the mat is rolled down over the front roof to prevent heat loss. A “coldproof” ditch (0.5–1.0 m deep, filled with insulating materials, such as straw and manure) reduces heat exchange through the soil between the inside and outside of the greenhouse. The ridge of the greenhouse is usually 3 to 4 m high, the span is 6 to 8 m wide, and the length is 40 to 100 m long. The back wall is 0.5 to 1.2 m thick. The unit area is about 300–800 m2. The energy-saving greenhouse is a special type of structure. The heat energy resource comes from the solar radiation and depends on structural and heat-conservation technology (Sun 1993; Yang and Chen 1994). Even in the severe cold winter season of North China, air temperature inside the greenhouse, even without supplemental heating, is sufficient for cool-season leafy vegetables such as celery and Chinese chive and also warm-season vegetables such as tomato, cucumber, sweet pepper, eggplant, and even watermelon (Fig. 4.7). In general, capital costs and

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Figure 4.7

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Energy-saving greenhouse for vegetable production in winter.

operational expenses are much lower than that of a modern multi-span greenhouse. In the winter on a clear day, the greenhouse can receive sunlight for 6 hr with light intensity averaging 20–40 klx. The maximum temperature inside the greenhouse can be higher than 25°C, sometimes even up to 30°C, and can last 3–5 hr. Temperatures at night are not lower than 10°C, and on cloudy days, not lower than 6°C. Night temperature differences between the inside and outside of the greenhouse can reach 30°C. In this microclimate condition, certain cultural practices improve plant growth. These include adoption of low temperature resistant cultivars, grafting to cold resistant rootstocks, multi-layer PE film covering, irrigation, and temporary supplementary heating for warm-season crops such as tomato and cucumber. Leafy vegetables perform well in the greenhouse, even in unexpected cold and cloudy days. Why can the energy-saving greenhouse without a heating system grow vegetables when outside winter temperatures drop to –20° to –10°C, even –25°C, in the north of China? The answer is that the continental, monsoon climate of China receives high solar radiation in winter despite the very low temperatures in northern zones. While winter sunlight intensity is only 50%–60% of summer radiation, the solar radiation

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provides enough heat so that it can be stored by heat-conservation strategies (Chen 2001). B. Structure In the earlier developing stage of the energy-saving greenhouse, the greenhouse was built based on farmers’ experiences only, using cheap and simple materials. In the Beijing district, the internal growing space of the greenhouse was small, with a span of 5.0–6.0 m at a ridge height of 2.6–3.0 m. The wall was built of dry earth, brick, and concrete; the front roof frames were made of bamboo or wood, and the outside covering mat made of straw or cattail. Since the late 1980s, considerable research work has been conducted to improve heat preservation and progress has been rapid. As a result, horticultural crop production in the energy-saving solar greenhouse is rapidly increasing. 1. Dimensions. Based on 20 years of research, the span of the greenhouse has been gradually enlarged, based on local climatic conditions. In Northeast and Northwest China, the span is 6.0–7.0 m where the lowest winter temperature is below –17°C. In North China the span is 6.5–7.5 m where the lowest winter temperature is between –17° and –12°C. However, if the lowest temperature does not reach –12°C, the span can be 7.5–8.0 m. Greenhouse length is site dependent. The back (north) wall is about 2.0–2.4 m high, and the ridge is 3.2–3.5 m high; they depend on the span and local climate. At latitude 40°N, the span can be 7.0, 7.5, or 8.0 m, and the ridge 2.9, 3.2, or 3.5 m, respectively. In warmer locations, the span and ridge are wider and higher. 2. Front Support and Wall Body. The front support is made of bamboo or steel pipe covered with 0.1-mm thick PE film. The east, west, and north walls of the greenhouse are 0.5 to 1.2 m thick and made of bricks. During temperature warm-up during the day inside the greenhouse, the wall is an endothermic body, and during temperature cool-down at night, the wall body is exothermic. Therefore, the reasonable structure of the wall is a double layer. Between the two brick layers is a thermalprotective insulation material such as perlite, coal cinder, sawdust, or polystyrene in order to prevent heat loss. 3. The Back Roof. The back roof of the greenhouse is a multi-layered structure composed of wood, straw, coal cinder, polystyrene, and

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cement board. The roof consists of water-resistant, load-bearing, heatpreserving and water-resistant layers from the bottom to top. The elevation angle of the back roof is 35° to 40°, and is more than the local solar elevation angle at noon on the winter solstice to ensure that sunshine can reach the back wall throughout the winter. 4. Covering Materials. During the day, sunlight is transmitted into the greenhouse through PE film in the front (south) roof of the greenhouse. At night the PE film is covered with a 5 cm thick mat in order to keep the greenhouse warm in cold seasons. When the sun rises in the morning, the mat is rolled up and kept on the back roof. Before the mid-1990s, the mats were made of straw or cattails but these were very heavy and difficult to roll up manually. At present, new kinds of mats made from chemical fibers that are waterproof, heat-conserving, and easily carried are widely used as covering materials. Mats made of synthetic fibers can be easily handled by machine.

C. Advantages and Disadvantages The advantages of this type of greenhouse are twofold: (1) it has good thermal-preservation properties, and makes the cost of energy for growing horticultural crops quite low during the cold season; and (2) the cost of greenhouse construction is only US$6 to $18/m2, much less than that of a modern multi-span greenhouse, making it affordable for most Chinese farmers. However, the disadvantages of this type of greenhouse cannot be ignored. The first is the difficulty of controlling environmental conditions in the greenhouse. The second is that the land-utilization ratio is rather low, because this type of greenhouse usually needs 0.5 to 1.0 m thick walls for thermal preservation, and there must be a space between the two greenhouses (Fig. 4.8). The width of the space is at least twice the height of the greenhouse ridge in order to ensure that the front greenhouse will not block sunlight entering the one behind it. Thus, the land between the two greenhouses cannot have good crops due to the shortage of sunlight. The third disadvantage is that the non-standardized structure of the energy-saving greenhouse makes it difficult to install modernized facilities for controlling conditions within the structure. Starting in the early 1990s, many vegetable growers began to switch to flower production because greater profits could be achieved. By 1998, there were over 1230 ha of energy-saving greenhouses used for growing flower crops in China.

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Figure 4.8 The layout of energy-saving greenhouses, showing the space required between greenhouses to avoid shadow interference from adjacent structures.

III. VEGETABLE CROPS China has a long history of growing vegetables, especially those crops originating in China. About 209 taxonomic species of vegetables, belonging to 31 botanical families, are grown in China. The most important 15 vegetables in terms of total production and growing area are Chinese cabbage, radish, potato, chili pepper, cabbage, tomato, cucumber, pok choi, eggplant, green Chinese onion, celery, garlic, Chinese chive, mustards, and spinach. At the present time, vegetables take first place among China’s protected crops. A. Mechanization of Vegetable-Seedling Production Until 1987 there was little commercial vegetable-seedling production in China, and farmers raised their own vegetable seedlings from seed. Most farmers had only one or two energy-saving greenhouses of 500–700 m2, which made it difficult to grow good seedlings. In 1999, the protected area in China was 1.4 million ha, requiring tremendous amounts of seedlings for commercial production. As a consequence, the establish-

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ment of mechanized vegetable-seedling production nurseries receives high priority. In 1987, China established the first mechanized vegetable-seedling production farm in Beijing, a plug-seedling production system imported from the United States. The majority of trays had 72 and 128 cavities mainly used for tomato, pepper, cabbage, and cauliflower. The medium was 70% peat and 30% vermiculite mixed with NPK fertilizers. Good results were obtained in the first 10 years, and many large cities began building their own mechanized vegetable-seedling production farms with facilities imported from the United States, France, Holland, and Israel. At the same time, China developed and produced some small facilities to produce plug trays and planters for vegetable-seedling production, but not enough to meet the demands of the market. At present the scale of mechanized vegetable-seedling production in China is small, and the efficiency is low as compared with Western Europe and North America, but it has raised efficiency tenfold compared with older vegetable-seedling production systems, and costs have been reduced one third. Mechanized seedling production is expected to develop rapidly. B. Soil-less Systems Though soil is still the predominant growing medium in China, continuous cropping in greenhouses results in soil-borne diseases. This problem is difficult to solve using conventional rotations because the greenhouse is a high-investment facility and should not be used to grow low-value crops such as onion, carrot, and cabbage. Tomato, cucumber, pepper, eggplant, and melon can achieve good returns, but these crops require plant rotation. As a result, protected cultivation for vegetable production in greenhouses is gradually changing from soil to soil-less systems (Zheng and Wang et al. 1990; Jensen and Malter et al. 1994; Jiang et al. 1996, 1998b). The commercial soil-less culture in China began in 1941. A farm for soil-less vegetable production was built in Shanghai but the operation failed because of the high cost of production and commercial soil-less vegetable production was discontinued for over 30 years. In 1976, Shandong Agricultural University began to produce hydroponic vegetables in a small area, but there was only 0.1 ha of soil-less culture in 1981. Since then, soil-less culture has developed steadily. In 1993, China had 43 ha of different types of soil-less culture systems, mostly for vegetables. By 2000, there were 365 ha of soil-less culture area in China (Table 4.3) (Jiang et al. 2000, 2001a).

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W. JIANG, D. QU, D. MU, AND L. WANG Table 4.3. Distribution of soil-less culture in mainland China (2000). Location Shanxi Liaoning Shanghai Xingjiang Hebei Beijing Shenzhen Guangzhou Nanjing Hangzhou Tianjin Wushi Zhuhai Daging Shenli Hainan Changzhou Others Tota1

Area (ha) 130 50 30 25 15 15 10 7 6 6 4 4 3 3 3 2 2 50 365

Soil-less culture systems such as nutrient film technique, deep-flow hydroponics, rockwool culture, and bag culture were all learned from western countries. Recently, China has developed new soil-less systems, including eco-organic and floating capillary hydroponics, which are low cost and more suitable for local conditions. These systems have now been widely extended to different parts of China (Jiang et al. 2001a). 1. Nutrient Film Technique (NFT). NFT is mainly used in Nanjing. In the past 10 years, this system was used to grow lettuce and tomato. Normally, NFT systems (Fig. 4.9) use plastic, iron, or concrete troughs, with gravity flow nutrient solution (Jensen and Collins 1985; Jensen and Malter 1994). The depth of nutrient solution in the trough is only 0.5–1.0 cm. Problems of the NFT system are that it cannot withstand unexpected power loss, temperature fluctuations of the nutrient solution are not easily controlled in summer, and the technique results in high nitrates in plant tissues, and often low oxygen in the nutrient solution. We do not expect this system to be expanded rapidly in China (Jiang et al. 2001a).

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Figure 4.9

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The basic feature of a nutrient film technique (NFT) system (Cooper 1979).

2. Deep-Flow Hydroponics (DFH). The system is a trough system, but the depth of nutrient solution is 5–8 cm. The system can keep temperature and oxygen more stable and is resistant to an unexpected power failure (Fig. 4.10). It has now expanded to tropical and subtropical areas in China, such as Guangdong province. 3. Bag Culture. The common bag size is 70 × 35 cm, which contains 18 L of substrate and normally is used for tomato or cucumber production with 2 plants/bag (Fig. 4.11). This method was popularly used in commercial soil-less vegetable production until 1995, but has gradually decreased. 4. Rockwool Culture. Rockwool culture is the same as bag culture except that the substrate is rockwool, an excellent substrate for vegetables and flowers. Because the cost is high, it is not popular in China. Since 1996, China has imported 30 ha of greenhouses from the Netherlands, which mostly utilize rockwool for vegetable production. 5. Shandong-Soilless Culture (Lu-SC). This system was developed by Shandong Agricultural University (Fig. 4.12). The trough is V-shaped, made of iron, cement, or earth with a 0.5% slope covered by PE film with

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Figure 4.10 A deep-flow hydroponics system for lettuce cultivation, A: top view, B: side view (1=valve, 2=pump, 3=flow pipe, 4=filter, 5=solution level adjustment, 6=catchment pipe, 7=catchment tank, 8=plastic film, 9=transplanting pot, 10=nutrient solution, 11=transplanting plate, 12=culture bed).

Figure 4.11 Bag-culture system for fruit and/or vegetable cultivation (1=nutrientsolution tank, 2=filter, 3=inlet tube, 4=dripper, 5-6-7=flow pipe).

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Figure 4.12 Lu-SC type soil-less culture system (1=trough, 2=flow pipe, 3=catchment pipe, 4=timer, 5=pump, 6=tank, 7=trough structure).

each side 20-cm in width. Water enters one end of the trough and is drained at the opposite end with a siphon pipe. An iron screen covered by palm fiber is set 5 cm above the bottom of the trough and filled with 10 cm vermiculite substrate. Irrigation is carried out 3–4 times each day. The system is mainly used in Shandong province. 6. Floating Capillary Hydroponics (FCH). FCH was first developed by the Zhejiang Academy of Agricultural Sciences and Nanjing Agricultural University. The growing beds are connected with preformed units and laid out in parallel on the leveled greenhouse floor (Fig. 4.13). The growing bed, planting plate, and floating board are made of polystyrene board. The size of each unit is 40 cm wide, 10 cm high, and 100 cm long. The planting board containing holes for plants is 39 cm wide, 100 cm long, and 2.5 cm thick and covers the growing bed. A lining of polythene film (about 80 cm wide) makes the bed leak-proof. The floating board is 12 cm wide, 100 cm long, and 1.25 cm thick. The floating board is covered with a piece of capillary mat (non-woven fiber, 25 cm in width) and floats on the nutrient solution in the culture bed. Through capillary action, the floating plate and non-woven fiber can be kept wet, and the root system grows up and down around the floating plate and takes up both oxygen and nutrients to meet crop demand. The depth of solution in culture beds is 3–6 cm and can be adjusted at the outlet (Zhang and Xu 1993; Xu and Zhang 1994).

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Figure 4.13

W. JIANG, D. QU, D. MU, AND L. WANG

Floating capillary hydroponics system.

7. Eco-organic, Soil-less Culture Development. The traditional soil-less culture systems using nutrient solution to irrigate the plant have high initial capital and production costs and are difficult to operate for Chinese growers. To solve this problem, an eco-organic-type soil-less culture system using solid organic fertilizer instead of nutrient solution was developed in the early 1990s by the Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences and has been adopted rapidly in recent years, reaching over 232 ha at the end of 2000. It accounts for over 60% of total area of soil-less culture in China. This sustainable system combines organic agriculture with soil-less culture (Jiang et al. 1996, 1998b, 2000). Structure. Eco-organic soil-less culture is a trough system using locally available substrates (coal cinder, peat moss, vermiculite, coir, sawdust, perlite, sand, rice husks, sunflower stems, maize stems, and mushroom waste) to reduce the initial investment. These materials have buffering

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Figure 4.14

133

Eco-organic type soil-less culture system.

ability and can be used successfully with good results. A mixture of two or three kinds of substrates improves the physical and chemical properties. The system consists of a trough, PE film, irrigation pipe and tape, and substrate (Fig. 4.14). The trough is made of three layers of brick (5 × 12 × 24 cm), 15 cm high and 48 cm wide with varying length of trough depending on the greenhouse. In the traditional Chinese solar, lean-to greenhouse, the trough length is 5–7 m, but in modern, multi-span greenhouses the trough length is around 30 m. The bottom of the trough is covered with 0.1 mm PE film to prevent soil-borne pests and diseases. Only solid manure rather than nutrient solution is used. The bed is irrigated only with fresh water. Development of the eco-organic system decreased initial investment up to 60–80%, and fertilizer cost 60% as compared with nutrient-solution hydroponics. Operations are simplified, vegetable quality is improved, and yields exceed those from soil culture (Table 4.4). Furthermore, crop nitrate levels in eco-organic systems were reduced from 30 to 67%, depending on the crop, as compared to soil-less culture systems with nutrient solutions (Table 4.5). Vitamin C and titrable acidity were also increased (Jiang et al. 2000). Fertilization. Fertilization in eco-organic soil-less culture is quite different from nutrient-film technique, deep-flow hydroponics, or rockwool

134

W. JIANG, D. QU, D. MU, AND L. WANG Table 4.4. The average yield of tomato and cucumber production. Average Annual Yield (kg/m2)

Year

Soil culture

Eco-organic soil-less culture

8 10 19

9 19 30

1989–1990 1994–1995 1999–2000

Table 4.5.

NO–3 content of vegetables in different soil-less culture systems. NO–3 Content of Vegetables (ppm)

Vegetables

Eco-organic system

Liquid hydroponics

NO–3 reduction using eco-organic (%)

Melon Bean Cucumber Pok choi Lettuce

29.8 41.8 17.8 2437.0 1339.0

89.7 90.8 35.4 3855.0 2028.0

–66.7 –54.0 –49.7 –36.8 –34.0

systems (Fig. 4.15). The eco-organic soil-less culture system with combined macro- and micro-elements uses solid organic fertilizers, mostly chicken manure, instead of nutrient solution. Growers need only to consider whether the NPK are sufficient and need not be concerned with micro-element deficiency. In any organic fertilizer, micro-elements are sufficient for plant nutrition and are not harmful to plants because of the buffering effect of the substrate. The amount of base organic fertilizer applied to tomato or cucumber, one-year one-crop (long-term crop), or one-year two-crops, is 15 kg/m3 substrate before transplanting (Fig. 4.16). It is unnecessary to add additional organic fertilizer for the first month. Afterward, a top-dressing of 3 kg/m3 of organic fertilizer is applied every two weeks. For melons or lettuce and other leaf vegetables, 25 kg/m3 of organic fertilizer are added as base fertilizer and further fertilization is unnecessary thereafter. Irrigation. Fresh water is used for irrigating horticultural crops instead of nutrient solution. The frequency and amount of irrigation depends on the phase of plant growth and development, and on season and climate. In general, irrigation is carried out in the morning of clear days and is

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Figure 4.15 Eco-organic soil-less culture for sweet pepper production in multi-span greenhouse.

unnecessary on cloudy or rainy days. In the summer, plants are irrigated two times per day, once in the morning and once in the afternoon. When plants are mature and heavily fruited, the amount of daily irrigation is 1.2 L/plant for tomato, 2 L/plant for cucumber, and 0.9 L/plant for melon. Crop Quality. The producers of organic food are not permitted to use any chemical fertilizers and pesticides, only organic fertilizers and biological control for pests and diseases. About 80% of nitrate in the human body comes from eating vegetables. Excess nitrates can induce stomach cancer. Applying different types of fertilizers lead to different nitrate levels. For example, even if the same amount of NPK were applied in the

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Figure 4.16 Eco-organic soil-less culture for muskmelon production in energy-saving greenhouse.

soil-less culture systems, the contents of nitrate in pok choi and lettuce fed by nutrient solutions were much higher than those using organic manure (Table 4.5). At the same time organic manure can reduce titratable acidity and increase vitamin C content (Jiang et al. 2000). Organic Fertilizer Production. The fundamental raw materials for production of organic fertilizers are oil cakes and animal manure. Soybean, peanut, rapeseed cakes are rich in macro- and micro-elements (Table 4.6). In the suburbs of larger cities in China, there is extensive animal agriculture providing manure for eco-organic soil-less systems. However, as in oil cakes and manure, K content is less than N content, and K supTable 4.6.

Nutrient element content of oil cakes. Macro-element (%)

Crops Soybean Peanut Rapeseed

Trace Elements (mg/kg)

N

P

K

Fe

Zn

B

6.68 6.92 5.25

0.44 0.54 0.79

1.19 0.96 1.04

400 392 621

84.9 64.3 86.7

28.0 25.4 14.6

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plementation is required (Table 4.7). The contents of trace elements are sufficient to meet crop needs. Organic fertilizer production requires composting, drying to 15% moisture, testing, and packaging (Jiang et al. 1996). Composting. Composting is the fermentation of organic wastes under controlled conditions in the presence of oxygen to degrade carbohydrates and to eliminate diseases and weed seeds. Temperature first rises rapidly to 40–45°C due to the respiration of aerobic mesophilic microorganisms fermenting sugars and starch. Temperatures then rise to 60–70°C, leading to the replacement of mesophilic microorganisms by thermophilic and thermo-tolerant ones. Microorganism respiration exhausts the oxygen of the composting mass and makes the environment anaerobic. The development of anaerobic organisms responsible for the emission of volatile compounds leads to a fall in temperature as their metabolism is less thermogenic. High temperatures destroy pathogens, parasites, and weed seeds, and foul-smelling odors are prevented. Fermentation is complete when the temperature stops rising after aeration. The progression from the initial materials to humus depends on numerous external factors such as the dimension of the particles, the kinds and structures of the nutrient present, humidity level, aeration, and pH. Aeration is an essential factor in the composting process. Air should occupy at least 50% of the heap volume. An aerobiosis begins when the oxygen level inside the heap is lower than 10% (air = 21% O2). High levels of water further decrease the quantity of air available in the compost. The heat released by fermentation causes the evaporation of a great quantity of water. Thus, the fermenting mass should be watered to maintain humidity at 50–70% of the fresh mass. The compost pile should be protected from heavy rains and from excessive evaporation by the sun. The materials to compost generally present a pH ranging between 5 and 7. The pH decreases during the first day, then rises and becomes neutral or slightly alkaline. Table 4.7.

Nutrient element content in animal manure. Macro-elements (%)

Trace Element (mg/kg)

Manure

N

P

K

Fe

Zn

B

Cow Horse Poultry Sheep

1.66 1.47 2.33 2.01

0.42 0.46 0.92 0.49

0.90 1.30 1.60 1.32

405 498 812 541

100 163 159 105

13 10 13 22

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The carbon form greatly influences the speed of decomposition of the compost. Simple glucose, starch, hemicelluloses, pectin, and amino acids are easily degraded, but cellulose, a more voluminous polymer, is more resistant. Lignin and other aromatic polymers, extremely strong, will be degraded later, slower, and incompletely (leading to the formation of humus). Too low a C/N ratio (i.e., lower than 15) leads to leakage of nitrogen; too high a C/N ratio slows decomposition. The quantity of nitrogen to be added is difficult to assess, as the degree of carbon fermentation must be taken into account. The speed and efficiency of composting is linked to the presence of an adequate microbial population. Adding effective microorganisms into the compost accelerates fermentation. EM are now widely used for organic fertilizer production in China. A good compost is a product in which organic constituents have stabilized through biological conversion. At the end of fermentation, this compost can be used as organic fertilizer or as a growth medium. A simple way to follow the development of the composting process is to use thermometric probes that go deep into the fermenting materials that are used to evaluate the stage of fermentation. Instruments cannot measure maturity level of the compost, so growers must use their own experience to determine that. C. Nutrient Solution and Substrate 1. Nutrient Solution. The hydroponic systems irrigate with nutrient solutions. The nutrient formulas in Table 4.8 are popularly used for tomato and lettuce production. The nutrient solutions for other

Table 4.8.

Nutrient formulae for tomato and lettuce. Concentration (g/1000 L)

Chemical formulae

Tomato

Lettuce

Ca(NO3)2 KNO3 KH2PO4 MgSO4⋅7H2O Fe EDTA MnSO4⋅4H2O H3BO3 CuSO4⋅5H2O ZnSO4⋅7H2O (NH4)6Mo7O24⋅4H2O

680 525 200 250 15 1.8 2.4 0.1 0.28 0.13

1200 799 20.7 1366 30 5 4.1 0.9 1.1 0.9

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crops differ mainly in nitrogen and potassium; microelements are quite similar. In China, fertilizers for making nutrient solution are quite expensive. Furthermore, Chinese growers, who were not well educated, found it difficult to operate and adjust the nutrient solution. Thus the use of hydroponic systems increased very slowly in China. 2. Substrates. Soil-less substrates had a number of advantages over soil: (1) a better control of water content and fertility; (2) reduced losses by leakage of nutritive elements; (3) control of air porosity; (4) more intensive utilization of cultivation area; (5) easier supervision of pests and disinfection; (6) absence of weeds; (7) high success rate in transplantation; (8) easier transport of young plants; and (9) higher buffering than liquid hydroponics. The physical behavior of the substrate is of fundamental importance and is difficult to correct during cultivation. Ideal substrate properties include: (1) high porosity; (2) sufficient particles size to ensure good drainage; (3) high stability; and (4) substrates that do not shrink when drying and are easy to rewet (Zheng and Wang 1990; Jiang et al. 1996). Using local resources for soil-less substrates can decrease costs. Peat, a highly fibrous material, is a good substrate for horticultural crops with high total porosity and high water holding capacity, but it is an unregenerated natural resource and often difficult to wet. Because the price of peat has increased each year, farmers have gradually decreased the use of peat and changed to other substrates. In North China, popular substrates include coal cinder, sawdust, ground maize and sunflower stalks, and perlite. Two or three substrates are often mixed to improve physical and chemical properties. Sawdust is widely used for soil-less culture in China and is always mixed with sand, coal cinder, and other materials to maintain good physical properties. Sawdust from western red cedar (Thuja plicata) is toxic to plant roots, particularly when fresh, and cannot be used in soilless systems. In Hainan island, South China, there is an abundance of coir, which if used properly can last up to ten years, even though organic. Coir is now considered one of the best substrates worldwide and is regenerable. The advantages of coir include good porosity, high available water, good drainage, good absorbtion ability when reused, low volume weight for easy transport, slow degradation, and good chemical properties (Table 4.9). Plant stalks, such as maize and sunflower stems, if well composted can replace peat as a substrate (Table 4.10) (Jiang et al. 1998a, 2000, 2001a). Mushroom waste is a good substrate for soil-less culture of vegetables and flowers and can be mixed with sand, vermiculite, and other

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W. JIANG, D. QU, D. MU, AND L. WANG Table 4.9.

Element N-NO3 N-NH4 Cu Na Fe P K Mg Mn

Chemical properties of coir. Content (mg/kg dw) <0.10 13 8.5 90 0.4 10 230 2 0.3

pH = 5.7–6.0 EC = 0.70–1.20 mS/cm Organic matter = 95%

substrates to improve physical and chemical properties. Sand is always mixed with sawdust, coir, mushroom waste, and another medium to improve drainage. Pure sand is also used as an inert substrate in hydroponics systems. Rockwool is made by melting certain rocks at 1600°C; various shapes can be formed. Rockwool is a good substrate for soil-less culture but its price is high. In China, most rockwools are used in imported Dutch greenhouses. Perlite is obtained by transforming a siliceous sand of volcanic origin containing crystallization water. This water, when eliminated by high temperature heating (1200°C), transforms the material into porous grains. Perlite substrate has high water and air-holding capacities, and can be mixed with peat and other media. Vermiculite is a phyllosilicate of almina (mica), dried, laminated, and heated at a temperature of 850 to 1000°C. This treatment violently blows out the water situated between sheets of the mineral. The obtained product is particularly light, and can absorb a quantity of water equal to many Table 4.10.

Elemental content of crop stalks. Macro-element (%)

Crop Maize Rice Sugarcane Sunflower Wheat

Micro-element (mg/kg)

N

P

K

Fe

Zn

B

0.92 0.91 1.10 0.80 0.65

0.15 0.13 0.14 0.11 0.08

1.18 1.89 1.10 1.77 1.05

4.93 1134.00 271.00 259.00 355.00

32.2 55.6 21.0 21.6 18.0

6.4 6.1 5.5 19.5 3.4

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times its own weight, while remaining aerated. Vermiculite is widely used for soil-less culture in China (Zheng and Wang 1990; Jiang et al. 1996). E. Disease and Insect Control 1. Root Diseases. Soil-borne diseases are serious diseases in greenhouse production even in soil-less culture systems. The only way to avoid soilborne diseases is to sterilize the substrate after cropping. Because the cost of steam sterilization is high, some chemicals have been used effectively for soil and substrate sterilization, such as methyl bromide, but residue can be taken up by crops and ground water, and human health is threatened. Solar sterilization (solarization) is increasing in popularity in sterilization of substrates. Procedures for solarization are as follows: remove plant residues from the greenhouse, water remaining substrate to 65% moisture, cover substrate with clear PE film, and close ventilation windows and greenhouse door. On sunny days in summertime, the substrate temperature can reach 60°C and substrate can be well sterilized after 3–4 weeks of solarization. This method does not completely kill pathogens, but decreases them and renders them harmless in the short term. After 3–4 years of solarization, enough pathogens accumulate in the substrate to make renewal necessary. The old substrate can be used as fertilizer and soil ameliorator for open-field agriculture (Jiang et al. 2001a,b). 2. Integrated Pest Management. Integrated pest management (IPM), including biological controls and cultural practices, is widely adopted in China for greenhouse crops production. The concept is that pests can be controlled largely by encouraging natural predators and parasites, using resistant cultivars, proper plant spacing, and other cultural practices. Pesticides are used only as a last resort. IPM practices include use of insect nets and yellow sticky traps for controlling aphids and other insects, the use of Encasia formosa for controlling white fly, Phytoseiulus persimilis for two-spotted spider mites, and an electronic sulfur evaporator for preventing downy mildew and powdery mildew. IV. FLORICULTURE A. Present Situation From the mid-1980s through the 1990s, the flower industry had expanded rapidly all over China, mainly because the economic level and social living standards had risen dramatically after 1980. In 1999, the

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total area of flower production in China amounted to more than 122,000 ha (Ministry of Agriculture of China, 2000) as compared to 8,000 ha in 1984. By 2000, the area of protected flower production had increased to 14,469 ha (Ministry of Agriculture of China, 2001). However, 90% of the total area was in energy-saving greenhouses, plastic tunnels, and shade structures. Modern greenhouses accounted for only 10% of protected cultivation. Most flower growers who use modern greenhouses are short of the technical know-how required for efficient operations, and yet the energy-saving greenhouse is too simple and crude to effectively control environmental conditions within the greenhouse for high-quality flower production. Therefore, the rapid expansion of the Chinese flower industry has not brought high returns to growers. Flower yield per unit area is quite low, and the quality of their products is poor. Although Chinese flower growers could gain more profits from their products than from growing grain crops or vegetables, the benefits from the same area are much less compared to those in developed countries, such as Holland, Israel, and the United States. In recent years, many more large floriculture enterprises, especially joint ventures such as Sino-Dutch, Sino-Israeli, and Sino-American, have been established in provinces where the flower industry is more developed. These enterprises possess first-class, high-quality facilities, cultivars, new technology, and skilled management. Thus, product quality is much higher than that of small-farmer enterprises. Some of their products are directly sold abroad. This has raised the level of the flower industry in China and we expect that the flower industry in China is poised for development. B. Facilities and Equipment 1. Irrigation and Fertilization Systems. There are many different irrigation methods in modern greenhouses and other protective facilities. Drip and sprinkler systems are used in modern greenhouses in China. In energy-saving greenhouses and plastic tunnels, flooding is the only method of irrigation, because many flower farmers cannot get sufficient financial support to upgrade their irrigation systems. With flooding, in comparison to drip and sprinkler systems, most water is wasted, soil structure is degraded, and salinity increases, resulting in ever-decreasing product quality. When drip irrigation is used for flower production, most of the nutrients are dissolved in the irrigation water and enter growing media with the water (fertigation). Different fertigation systems are used in China. The most popular is the gravity drip system, in which fertilizer is mixed

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in a raised tank, with no pump required. This system is becoming increasingly popular for many Chinese flower growers because of its simple structure and energy-saving qualities. 2. Temperature. Maintaining optimum temperature is one of the most important tasks of greenhouse management in floriculture. The heating system should be started when temperatures inside the greenhouse drop below the optimum range; when temperatures are above the optimum range, temperatures must be lowered. For most regions in China, it is much easier to heat the greenhouse in winter than to cool it in summer. Traditionally in China, coal-fired boilers were used for heating greenhouses, because coal is much cheaper than petroleum products. However, coal creates more pollutants than fuel oil. From 1999 on, Chinese policy forbids using coal-fired boilers in suburban areas around large cities such as Beijing, Shanghai, and Tianjin. It is difficult to lower the temperature within a greenhouse in summer. Generally, there are two choices of cooling systems in modern greenhouses: fan-pad and spray cooling. In some cases, both methods are used in the same greenhouse. It is much more difficult to lower the temperature in an energy-saving greenhouse during summer than it is in a modern greenhouse. Up to now, no method for lowering the temperature in an energy-saving greenhouse has been as efficient as those used in modern greenhouses. 3. Light. There are three different ways of controlling light intensity and photoperiod in greenhouse. Shading is used to lower light intensity and it also can reduce temperatures in greenhouses. Different types of shading nets are available. The best is made of a thin layer of aluminum foil attached to a layer of black plastic strip, fixed with nylon fibers. This type of shading will not only reduce sunlight, but can also reflect the sun’s energy. This is the most expensive system. In China, flower growers prefer to use shading net composed of black plastic strips fixed with nylon fibers because it is less expensive. In some seasons, sunlight is insufficient and supplemental lighting is required. High-pressure sodium lamps are the most effective type of supplementary light, but the costs of investment are high. Many Chinese farmers prefer to use incandescent lamps as supplementary lighting because they cost less. In addition to increasing light intensity during winter and cloudy days, lamps are used to provide the increased daylength required for some flower crops, such as chrysanthemum and gypsophila. In certain seasons, some flower crops require a short-day treatment for blooming

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and black-cloth shading is used. For example, when cut chrysanthemums are needed during the summer, growers cover the crop with black film at least 15 hr/day (Mu 1997, 1999). 4. Plant Protection. Facilities for plant protection are critical in greenhouses, and many failures are due to a shortage of effective methods of plant protection. Sulfur evaporators are a very effective method of disease control, that are widely used in both modern greenhouses, energysaving greenhouses, and plastic tunnels in China. From the 1980s to the mid-1990s, sulfur evaporators were imported from abroad. Because imported evaporators were too expensive for Chinese flower growers, there are now local factories producing sulfur evaporators. C. Commercial Flower Production 1. Cut Flowers. China’s cut-flower industry was initiated in 1984 and is now an important part of China’s agricultural economy (Fig. 4.17). According to the official statistics, the yield of fresh cut flowers in China was 2.7 billion stems in 1999, and the area of cut-flower production

Figure 4.17 Cut chrysanthemum production with hand-spray irrigation in simple multispan greenhouse.

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under protected conditions was 2488 ha (Ministry of Agriculture of China, 2000). Although China’s cut-flower industry has expanded rapidly, the production level is not high. For instance, in 1999 (Ministry of Agriculture of China, 2000) only 235 ha out of the total area of protected conditions were modern greenhouses with heating systems and accounted for only 3.4% of the total area. The remainder was in energysaving greenhouses, plastic tunnels, and open fields. The major cutflower crops grown under protected conditions are rose, carnation, gerbera, lilies, calla, limonium, and anthurium (Fig. 4.18). About 50% of cut chrysanthemum, gladiolous, and gypsophila are grown in open fields. More than 90% of cut flower crops are produced with soil culture, even in modern greenhouses; less than 10% are produced with soil-less culture. Rose is the number one cut flower crop, with an area of about 2450 ha in 2000 and almost 100% grown under protected conditions. The second crop is cut chrysanthemum, 2016 ha

Figure 4.18 Cut gerbera production in energy-saving greenhouse with yellow sticky traps for insect control.

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5000 4000

Area (ha)

4000 3000 2000

2092

2488

1000 0 1998 Figure 4.19 2000.

1999

2000

Area of cut-flower production under protected conditions in China, 1998 to

in 2000. The third and fourth crops are carnation and gladiolus, respectively. Most of these crop cultivars are from abroad except for gladiolus, many of which are bred in China. In the last five years, the demand for cut lilies has been increasing rapidly in the domestic market, which has stimulated enthusiasm for this crop. China imported more than 50 million lily bulbs in 2000 (Ministry of Agriculture of China, 2001), mainly from Holland. More than 50 species are cultivated commercially in China and the area of cut-flower production under protected conditions has been expanding dramatically in the past few years (Fig. 4.19). 2. Pot Plants. Pot-plant production, including pot flowers and foliage plants, developed earlier than cut flowers in China but did not expand dramatically until the late 1990s. Fig. 4.20 shows the situation of potplant production from 1998 to 2000. As the demand for high-quality pot plants increased in the domestic market, the area of pot-plant production in greenhouses rose sharply during the past several years (Fig. 4.21). Pot-plant production increased 166% from 1998 to 1999, and increased 191% in 2000. Even so, China imported millions of pot flowers from abroad during the Spring Festival of 2000. The major pot flowers that are popular in China, especially during every New Year’s day and Chinese Spring Festival, are azalea, anthurium, guzmania, moth orchid, autumn cattleya, noble dendrobium, poinsettia, cyclamen, tulip, hyacinthus, hippeastrum, New Guinea impatience, and begonia. The facilities requirements for growing pot plants are more complicated than for cut flowers. Thus, modern greenhouses are of utmost importance for quality pot-plant production. China had 1767 ha of greenhouses for pot-plant production in the year 2000 (Fig. 4.21), more than

4. PROTECTED CULTIVATION OF HORTICULTURAL CROPS IN CHINA

8000

147

7394 6792

7000

Area (ha)

6000 5000

4331

4000 3000 2000 1000 0 1998

Figure 4.20 2000.

1999

2000

Area of pot-plant production under protected conditions in China, 1998 to

90% of which were energy-saving greenhouses, where there are few facilities with environmental control (Ministry of Agriculture of China, 2001). The pots are typically placed on the ground in the greenhouse. Lack of raised beds increases insect and disease damage. Drip or sprinkler systems are not used in most energy-saving greenhouses; many growers just add water to the pots when irrigation is required. Thus, the quality of domestically produced pot flowers is not as good as the quality of those from abroad, such as those from Holland, Belgium, and Germany. Most pot flower growers in China are aware of the problems and have begun to construct modern greenhouses to grow quality plants.

Area (ha)

2000

1767 1539

1500 1000

925

500 0 1998

Figure 4.21

1999

2000

Area of pot-plant production in greenhouses in China, 1998 to 2000.

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3. Planting Materials. For many flower species, planting stock is one of the vital conditions for producing quality flowers. In China, the young plant industry was not well developed until the 1990s. There are now four methods for producing young plants: seeding, cutting, grafting, and tissue culture. Theoretically, all species of plants can be propagated by tissue culture. However, carnation, chrysanthemum, azalea, impatience, and some minor crops are propagated by cuttings. Most rose and many ornamental tree cultivars are propagated by grafting. Most annual and biennial flower crops are propagated by seeding. Most foliage plants and some flower crops, such as gerbera, anthurium, orchids, and eustoma, are propagated by tissue culture. Greenhouses used for producing young plants should be highly equipped. Since the early 1990s, many large nurseries possessing modernized greenhouses have been constructed in some major provinces of flower production. Yunnan province of Southwest China is the largest producer of young plants for flower crops in China. There are many large nurseries, each of them producing millions of young plants, including carnation, rose, gypsophila, gerbera, limonium, and many species of pot flowers. For example, a nursery belonging to the Institute of Horticulture, Yunnan Academy of Agricultural Sciences, produces more than 10 million carnation cuttings per year. Yingmao, established as a SinoIsraeli joint venture, also produces more than 10 million carnation cuttings per year. Part of its production is exported to Europe. Xidu produces about 11 million geranium plants per year; most of its production is exported to Germany. Kunming Speedling Ltd. Co. produces 3 million young plants of pot flowers per year. More than 10 large nurseries and many smaller ones in Yunnan province of Southwest China possess very highly equipped greenhouses and produce about 200 million young plants per year, of which more than 20 million are produced by tissue culture and 160 million by cuttings. Shanghai is another region for young plant production; major crops are rose, carnation, chrysanthemum, anthurium, and many minor crops. The greenhouses and other facilities for young plant production in Shanghai are more advanced than in Yunnan province. For instance, Shanghai Kangnan Horticulture Co. Ltd., a Sino-Dutch joint venture, produces millions of quality young plants of anthurium, has 3 ha of modern greenhouses equipped with heating systems, shading nets, drip irrigation, fan-pad, sprinkler cooling, and movable benches. Jinmei, another nursery famous in Shanghai, produces millions of young rose plants. Honghua produces millions of chrysanthemum cuttings per year, mainly for export to Japan. Although their greenhouses are not modernized, they produce chrysanthemum cuttings of very good quality. Other regions, such as Beijing, Sichuan province and Liaoning province, also produce young plants.

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V. FRUIT TREES A. Present Situation Protected fruit-tree culture includes three aspects: (1) advance maturation, widely used by fruit growers in northern China, especially for short-storage-life species such as strawberry and peach (Wang 1998); (2) delayed maturation for fruits such as late-ripening peach first used in Liaoning province in 1998; and (3) rain protection for grape and peach in Southern China (Chen and Sun 1999). Disadvantages of protected fruit culture include high investment and energy input compared with conventional open-field fruit culture and lower sugar content of fruits from protected culture. Protected fruit culture developed later than protected vegetable and flower production in China due to the larger canopy volume required. Since the 1990s, protected fruit culture has developed rapidly in China due to the economic benefits (Shi 1998; Wang et al. 1999a; Wang et al. 1998; Wang et al. 1999b; Zhu et al. 2000d). Fruits in protected culture can be harvested 20 to 90 days earlier (late March to May) in Northern China and the price is several times higher than that of the normal. For example, the price of nectarine fruits was US$4/kg in the middle of March, $1.20 to $2.00 in the middle of April, and $0.90 to $1.20 in May 2001. The earlier the harvest, the higher the price. Now, fruit growers not only use earlier-ripening cultivars in the greenhouse, but also later cultivars for earlier-ripening in plastic tunnels to improve fruit quality, because later-ripening cultivars have higher quality than early-ripening ones. For example, ‘Fengbai’ peach, which ripens 130 days after flowering (DAF), can ripen 40 days earlier in protected culture than in the open field with larger fruits and higher sugar content than early-maturing cultivar natural-ripening seasonal fruits. Generally in high-density commercial production systems, fruits can be harvested in the second year after planting. ‘Shuguang’ nectarine yields reach 3.2 kg/m2 and ‘Katy’ apricot 1.3 kg/m2 in the second year after planting, producing a rapid return on investments (Wang et al. 1999a, 1999d; Peng and Gao 2000). Strawberry takes first place in protected fruit cultivation; other principal fruit species include peach, nectarine, cherry, apricot, plum, and grape in order to advance the maturation of short-storage-life fruit to meet consumer demand for year-round fruit. Strawberry, the most widely planted fruit in protected culture in China, is timed to ripen for the Chinese lunar new year (late January to early February). In some areas, strawberry is harvested year round (Wang et al. 1999b; Wang and Zhang 1999; Yu and Feng 1998; Qian et al. 1999; Liu 1999). In 1991, protected peach culture for commercial purposes was successful in Liao Zhong county in Liaoning province of Northeast China

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(Li 1999), where peach fruits ripen at the end of June in the open field. Starting in 1991, researchers systematically examined cultivars and production, including chilling requirement and physiological response. Protected peach and nectarine culture began to become common in Northern China, and it is estimated that the area of peach and nectarine is just behind strawberry. Although prices have declined in the past two years, growers still have better economic benefits than from open fields, so protected peach and nectarine are increasing gradually. In the 1950s, protected grapes were successful in Qiqihar Horticultural Institute in Heilongjiang province of Northeast China, but there was little commercial exploitation (Li 1999). The area of greenhouse grape production began to expand significantly in high latitude regions of China in the 1990s. Total area of protected grape culture follows that of strawberry and peach. In 1998, protected plum and apricot culture were successful in Tai’an city in Shandong province of East China. ‘Katy’ and ‘Goldensun’ cultivars make this culture a great success (Peng and Gao 2000; Lu and Zhang 2000). Because growers can earn a high income, the government supports this kind of high-value industry. Total area for protected fruit culture was 46,700 ha in 1999, including strawberry, peach, nectarine, plum, apricot, sweet cherry, grape, fig, Chinese date, and even pear (Li 1999). In the past 3–5 years, protected fruits have been grown in every northern province in China; large-scale culture has developed in Liaoning province (Northeast China), Shandong province (East China) (Wang et al. 1999b; Yu and Feng 1998), and Hebei province (North China) because of their suitable climate, large markets, and good grower skills. In Northwest China, the duration and intensity of the solar radiation is more sustainable than in the regions mentioned above, but poorer markets and poorer grower skills limit the development of protected fruit cultivation. Shandong province has the largest area of protected fruit culture in China (Wang et al. 1999b) (Table 4.11). Temperature is often below –20°C in Northern China in winter and below the freezing point during the bloom period of stone fruit. Protected culture can solve the cold injury problem and ensure more consistent production. Thus, protected fruit culture is developing rapidly in Liaoning (Yu and Feng 1998) (Table 4.12) and Xinjiang in the northern part of China, an area unsuitable for open-field peach production, while apricot can seldom be harvested due to spring frost injury. Protected apricot culture not only advances the harvest season, but also results in a good crop return each year. After chilling requirements are satisfied in greenhouses in North China, winter temperatures are too low to satisfy heat requirements unless heaters are used, and fruits cannot ripen as early as expected.

4. PROTECTED CULTIVATION OF HORTICULTURAL CROPS IN CHINA

151

Table 4.11. Greenhouse area, yield, and income for fruits in Shandong province (Wang et al. 1999b).

Fruits

Area (ha)

Yield (t/ha)

Income (US$1000/ha)

Strawberry Grape Nectarine Sweet cherry Plum and apricot Total

4467 353 680 413 187 6100

22.5–30.0 22.5–37.5 15.0–22.5 7.5–11.25 11.25–15.00 —

11–36 36–72 27–54 54–108 36–72 —

Table 4.12. Area of greenhouse and tunnel for fruits in Liaoning province (Yu and Feng 1998).

Fruits Strawberry Grape Peach and nectarine Berries Apricot

Greenhouse area (ha)

Tunnel area (ha)

Total area (ha)

804 492 165

2099 86 6

2903 578 171 1.6 0.13

There are three kinds of structures used for protected fruit culture in China: (1) the energy-saving greenhouse; (2) plastic tunnel; and (3) low plastic tunnel, which is only used for strawberry. Greenhouses are used widely in Northern China, while plastic tunnels are used in Central and South China. The different kinds of structures produce different yields and income (Chen and Sun 1999) (Table 4.13).

Table 4.13. The comparison of yield and income (US$) among different structures for strawberry per hectare (Chen and Sun 1999).

Structure

Yield (kg)

Price ($/kg)

Output value ($)

Cost ($)

Income ($)

Greenhouse Low tunnel Plastic mulch Open field

23,850 27,450 28,350 28,590

3.0 0.7 0.5 0.3

71550 19215 14175 8577

9280 6435 5070 4871

62270 12780 9105 3706

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W. JIANG, D. QU, D. MU, AND L. WANG

B. Cultivars Chilling requirement and fruit development period (FDP) are particularly important to protected fruit culture in order to get earlier harvest (Wang et al. 1995, 1996a,b). Self-pollinating cultivars can increase yield and save labor costs (Zhu 1999). Thus, cultivars with a low chilling requirement, short FDP, and self-pollinated are recommended for protected fruit culture (Wang et al. 1995, 1996a,b). Adapted cultivars should have good quality and also resistance to weak light and lower temperature (Wang et al. 1999a). 1. Peach and Nectarine. Nectarine in protected culture is more popular than peach, because of its attractive appearance and easy-to-eat quality (Wang et al. 1999c,d; Zhu 1999). ‘Shuguang’ and ‘Early Red 2’ are planted widely. White-fleshed nectarines, such as ‘Huaguang’ and ‘Zaohongzhu’, are favorites of the Chinese consumer, but their flesh is soft and fruits are small. American cultivars have a more attractive appearance, larger size, and are firmer for long-distance shipment, but they are too acid for Chinese consumers. ‘Early Red 2’, a low-chilling cultivar, has a round shape, dark-red color, high firmness, freestone, and very high productivity, but is high in acid and has a longer FDP. ‘Early Red 2’ was the only adapted nectarine cultivar before 1995, but it is no longer because of the release of ‘Shuguang’ and ‘Huaguang’ (Wang et al. 2001; Zong et al. 1999). In the last 2–3 years, the flat peach (peento) has had a higher price than nectarine due to its excellent flavor and unique shape. ‘Zaolupantao’, the main flat cultivar, has early maturity, good taste, and high yield, but the flesh is soft. Large high-quality juicy peach, such as ‘Sunagowase’, has a good market, but its planting area is still minor (Table 4.14). 2. Grape. Protected grape cultivated area, following that of strawberry and peach, is about 6290 ha, mainly located in Liaoning, Hebei, and Shandong provinces. Predominant cultivars are ‘Cardinal’, ‘Kohyo’, ‘Hongshuangwei’, ‘Jingxiu’, and ‘Zhengzhou Zaoyu’. Now the tendency is to plant seedless cultivars. Details on grape are summarized in Table 4.15. 3. Apricot and Plum. ‘Katy’ and ‘Goldensun’ apricot have excellent performance in greenhouse (Lu and Zhang 2000), but ‘Dashizaosheng’ plum crops poorly and ‘Misili’ plum only performs well in the later-ripening season (Table 4.16). 4. Cherry. ‘Redlamp’, released from Dalian Agricultural Institute of Liaoning Province in 1973, is one of the main cultivars; FDP is 45 days, and average fruit weight is 9 g with very good flavor. ‘Longguan’ bred

Table 4.14.

Main peach and nectarine cultivars used in protected culture in China.

Cultivar (Type)z

Chilling req.

Season (FDP)y

Weight (g)

Blush (%)

Firmness

Shape

Flesh color

Pit

Ground color

Flavor

Sunagowase (P) Chunlei (P) Shuguang (N) Yanguang (N) Huaguang (N) Zaohongzhu (N) Zaolupantao (F) Danmo (N) Mayfire (N) EarlyRed 2 (N)

850 800 700 700 700 700 700 600 550 500

80 56 65 70 62 65 65 65 62 92

200 85 100 110 90 90 90 90 80 150

30 40 90 60 50 70 60 100 90 100

excel poor good marginal poor poor poor good good excel

round oblong round oblong round oblong flat round oblong round

white white yellow white white white white yellow yellow yellow

cling cling cling cling cling cling cling cling cling free

good marginal good marginal marginal marginal marginal good good good

good marginal good good excellent excellent excellent excellent marginal marginal

z

N = nectarine, P = peach, F = flat peach Fruit development period in days.

y

153

154 Table 4.15.

W. JIANG, D. QU, D. MU, AND L. WANG Grape cultivars used in greenhouses (H.Q. Li, pers. commun.).

Cultivar Cardinal Hongshuangwei Jingxiu Zhengzhouzaoyu z

Season (FDP)z

Cluster wt. (kg)

Avg. fruit wt. (g)

Color

Seeds

Soluble solids (%)

60 60 60 50

535 600 800 436

8.3 6.5 8.5 6.0

purple-black purple-black rose to purple greenish yellow

large

13.4

Fruit development period in days.

Table 4.16.

Apricot and plum cultivars used in Chinese greenhouses.

Species Cultivar

Season (FDP)z

Weight (g)

Apricot Katy Goldensun

70 60

105.5 70.0

Plum Dashizaosheng Misili

65 80

60.0 50.0

z

15.5 16.0

Color

Firmness

Shape

Flavor

yellow yellow

good good

round round

marginal good

red flush dark red

good good

round round

excellent excellent

Fruit development period in days.

by Zhengzhou Fruit Institute of Henan Province has high selfpollination, but has small fruit size and high acidity, so it is used only as a pollinizer. ‘Van’, ‘Rainier’, ‘Bigarreau’, ‘Moreau’, and ‘Lapins’ also are cultivated in greenhouses. C. Cultural Techniques 1. Rootstocks. Fruit trees have a larger canopy than vegetables, so it is very important to control tree volume to get high yield and good quality. At the same time, moisture in soil and air inside the greenhouse is usually higher than that in the open field. High moisture levels increase susceptibility to diseases. Rootstocks recommended for use in greenhouse culture have been similar to those used in open fields. Wild Prunus has been popularly used as a stone fruit rootstock in China. There are three kinds of rootstocks widely used in peach, plum, and sometimes apricot in China. Prunus persica shows the best compatibility and tolerance to waterlogging, and is best for peach, nectarine, and plum in greenhouse use. Although the early output on P. davianada

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155

rootstock is higher than that on P. persica, it is susceptible to crown gall (Agrobacterium tumefaciens) and waterlogging. On P. tomentosa rootstock, trees show dwarf canopy and early bearing that are very good for protected culture, but leaves turn yellow to a certain degree in the second or third year. Fruits are smaller and more bitter than on P. persica rootstocks (Zhu et al. 2000a). ‘Colt’ cherry rootstock, used in Shandong province of East China, induces some dwarfing, but is susceptible to crown gall. ‘Dayechaoyingtao’ (Cerasus pseudocerasus), which was released from Shandong, is more dwarf than ‘Mahaleb’ and has good graft compatibility with most cherry cultivars, but gummosis occurs on the graft union. ‘ZY1’, which was introduced from Italy, ‘Gisela 5’, ‘Gisela 6’, ‘Gisela 7’, and ‘Gisela 12’ are recommended for protected cherry culture (Zhao 2000a). 2. Management of Young Trees. Cultivation of fruit trees in protected environments with high density is necessary in order to obtain maximum early yield. The key practice with young trees is to expand the tree frame before June, and then to stimulate flower bud formation to ensure maximum crop yield. Cultural densities are 0.9 m × 1.2 m for peach, 1.0 m × 1.5 m for nectarine, 1.2 m × 2.0 m for apricot, and 1.5 m × 2.5 m for plum. Rows are in a north-south direction if trees are planted in tunnels, or in an eastwest direction in greenhouses (Wang et al. 1999d). Generally, young trees are planted in Zhengzhou, Central China, at the end of February before new roots begin to grow in an open field. The trees can be planted in mid-January in plastic tunnels in order to prolong the growing season, and to get a larger tree canopy as soon as possible. When young trees reach 60 to 70 cm, they are headed-back to form the “Y” or “cylinder” shape; they are headed-back at 30 to 50 cm for the open-center style. Currently, “Y”, “cylinder”, or “central-leader” shapes are used widely in protected peach and nectarine culture. Studies show that peach trees trained to the cylinder shape had larger leaf area and canopy volume, and better light penetration in the canopies than those trained to traditional open centers. Fruits from cylinder-shaped trees have a more attractive color and higher quality than those from opencenter-trained trees (Zhu 1999; Wang et al. 1999d). Winter pruning should be as light as possible to attain the desired shape and yield. With proper pruning and training, every tree can produce 15 to 20 fruits, which is a profitable level of production in the second year (Zhu 1999). After the second year, paclobutrazol (PP333) should be applied in the soil to advance flowering, increase the number of flower buds, and enhance fruit weight.

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3. Breaking Dormancy. Daytime temperatures higher than 18°C result in a negative chilling effect (Wang et al. 1997a). In order to decrease the temperature to meet the chilling requirement as soon as possible, straw mats are usually used to cover the plastic roof during the daytime of the dormancy period. The Zhengzhou Fruit Research Institute has monitored chilling accumulation and developed a simple method to estimate the end of dormancy for growers based on a 10-year study (Table 4.17), enabling growers to regulate temperature according to the chilling requirement of cultivars (Wang and Hu 1992; Wang et al. 1995, 1997a,b). In cold areas such as Liaoning province, fruits can ripen in mid-March in greenhouses; 40 to 90 days earlier than those in the open field if the heat requirement is satisfied. However, in warm winter areas, fruit maturation may start in late April and normally in early May. Because of the necessity for accumulating the required chilling prior to covering the orchard, only a small advancement in fruit ripening occurs. Cold areas in winter can attain a faster advancement in fruit ripening than warmer areas, so protected fruit culture develops rapidly in cold areas (Table 4.18). 4. Temperature Adjustment. Temperature is the most critical factor in obtaining high yield and improving fruit quality. A common error is to maintain high temperatures to take “advantage” of the advancement in fruit ripening. A temperature of 30°C or higher may be easily reached on a clear day in a closed greenhouse in mid-February. High temperatures during blooming and fruit set are detrimental, leading to no fruit set or to severe fruitlet drop (Erez et al. 1998). From experience, it was found that temperature at bloom time should not be above 22°C during bud break because high temperature negatively affects fruit set and development. Thus, greenhouse temperature should be 28°C at maximum during the breaking of dormancy and 22°C during blooming. When tem-

Table 4.17. Date chilling requirements are met in Zhengzhou (Wang et al. 1997a). Cultivar chilling requirement

Date

200 300 400 500 600 700 800

early December middle December late December 5 to 10 of January 10 to 20 of January 20 to 25 of January 25 to 30 of January

4. PROTECTED CULTIVATION OF HORTICULTURAL CROPS IN CHINA Table 4.18.

City

157

Ripening dates of ‘Shuguang-nec’ peach in different latitudes (Zhu 1999).

Latitude

Annual average temp. (°C)

Jan. average temp. (°C)

Dec.– April (light hr)

Field

Greenhouse

Advance (days)

34° 43′ 36° 04′ 38° 04′ 36° 03′ 41° 46′ 43° 54′

14.3 14.3 12.9 8.9 7.8 7.3

–0.2 –1.4 –2.7 –7.3 –12.7 –15.2

911 1069 1108 1081 1022 945

6/05 6/12 6/10 6/25 6/30 6/30

5/01 4/20 4/20 4/01 4/15 4/15

35 52 50 85 75 75

Zhengzhou Jinan Shijiazhuang Lanzhou Shengyang Urumqi

Ripening Date

peratures are below 0°C , flowers could freeze or fruit could be poorly set. Thus, in very cold areas, such as Shengyang of Northeast China and Urumqi of Northwest China, the installation of a greenhouse heating system is necessary. Table 4.19 (Wang et al. 1997a,b). lists temperature and relative humidity during growth of plant and fruit for peach, nectarine, apricot, and cherry.

Table 4.19. Temperature, humidity, and key practice for peach in greenhouses (Wang et al. 1997b). Temperature (°C) Development stage

Highest

Lowest

Relative humidity (%)

Dormancy Budbreak

28.0

0.0

80

Flower emergence

28.0

5.0

50.0–60.0

Full bloom

22.0

5.0

50.0–60.0

Petalfall After bloom New shoot growth

25.0 25.0 25.0

5.0 5.0–10.0 10.0

50.0–60.0 < 60.0 < 60.0

Double line Fruit expansion Fruits color

25.0 28.0 28.0

10.0 10.0 10.0

< 60.0 < 60.0 < 60.0

Harvest Postharvest

30.0 30.0

18.0 18.0

< 60.0

Key practice Cover plastic sheet and straw mat Cover the field with plastic film Avoid from high temp. moisture; hand pollination required Cut buds First thinning Second thinning; summer pruning Irrigation Selecting fruit Use reflecting plastic film Summer pruning

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5. Irrigation System. Furrow and flooding irrigation systems are still very commonly used in China, while drip irrigation is steadily increasing. In greenhouses, irrigation is reduced to 2 or 3 times for stone fruits and 3 or 4 times for grape. A drip-irrigation system with field-mulch film is recommended in greenhouses because this system saves water resources, reduces humidity, and increases the fruit yield and quality.

VI. FUTURE DEVELOPMENT OF PROTECTED HORTICULTURE Protected horticulture has undergone great progress during the last decade in China, but the level of protected horticultural crop production in China is still lower than that in developed countries. Many problems still need to be solved. The requirements for research and development of protected horticulture in China in the near future are summarized below. 1. Almost all local cultivars used in protected culture are those that were bred for the purpose of open-field production in China. This results in low yield, poor quality, and low profit in protected cultivation. Breeding of special cultivars for the purpose of protected cultivation is an urgent research priority. 2. Much attention should be paid to developing a cultivation protocol for protected conditions for each crop, to standardize cultivation methods. This includes cultivar selection, irrigation, fertilization, and IPM. The productivity level of protected horticulture in China could be greatly enhanced in the coming decade. 3. More effort on techniques for water-saving irrigation should be made for protected horticulture, because of the deficiency of water resources in China, especially in North and Northwest China. Water availability is one of the main limiting factors for agricultural development and protected horticulture requires more water than other cropping methods. 4. The market of greenhouse and accessory equipment for horticulture production will be greatly expanded. The area of modern multi-span greenhouses in China is expected to increase dramatically, a great opportunity for both Chinese and foreign greenhouse manufacturers. Industries related to protected horticulture have many opportunities in China. 5. The number of large floriculture enterprises will increase, while small units of flower production will decline. The form of flower

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markets in China will change and auctions, wholesaling, and supermarket sales will increase gradually. 6. The nursery industry is relatively weak in China. This is one of the main reasons that the quality of flower products in China is not high. Demand for quality planting materials will greatly increase in the coming 5 to 10 years, and large-scale nurseries producing planting materials for horticulture crops will increase. 7. Protected horticulture is a labor-intensive industry, which provides a great opportunity for Chinese horticulture products in overseas markets, especially after China’s entry into the World Trade Organization (WTO). There is no doubt that protected horticulture in China will become increasingly important in the near future.

LITERATURE CITED Chen, D. S. 1991. Technology of the energy-saving sunlight greenhouse in China (in Chinese). Proc. Int. Symp. Applied Technology of Greenhouse (ISTG), Beijing: Knowledge Publ. House, p. 41–49. Chen, D. S. 1994. Advance of the research on the architecture and environment of the Chinese energy-saving sunlight greenhouse (in Chinese). Trans. Chinese Soc. Agr. Eng. (Trans. CSAE) 10(1):123–129. Chen, D. S. 2001. Theory and practice of energy saving solar greenhouse in China (in Chinese). Trans. CSAE 17(1):22–26. Chen, Y. Y., and G. M. Sun. 1999. Protected strawberry culture (in Chinese). China Fruit 3:42–43. Cheng, J. S. 2000. The genetics and breeding of garden plants (in Chinese). Chinese Forestry Press, Beijing. China Greenfood Development Center. 1997. Trainee reference for green-food management (in Chinese). Chung, C. 1999. Use of plastic shelter for improving peach production. Int. Sem. Protective Structures for Improved Crop Production. Suwon, Korea. Cooper, A. 1979. The ABC of NFT. Grower Books, London. Encyclopedia of Chinese ornamental horticulture (in Chinese). Chinese Agr. Press, 1996. Erez, A., Z. Yablowitz, and R. Korcinski. 1998. Greenhouse peach growing. Acta Hort. 465:593–600. Huang, Y. S. 1997. MOA Natural farming in Japan (in Chinese). Nangshen Publ. Ltd., Taibei. Jensen, M. H., and W. L. Collins. 1985. Hydroponics vegetable production. Hort. Rev. 7:484–558. Jensen, M. H., and A. J. Malter. 1994. Protected agriculture. World Bank Techn. Paper 253. World Bank, Washington, DC, USA Jiang, W. J., W. Liu, and H. J. Yu. 1998. Evaluation and application of various low cost and environmentally friendly materials as substrates for soilless cultivation of greenhouse crops. J. Japan. Soc. Hort. Sci. 67(1):167. Jiang, W. J., W. Liu, and H. J. Yu. 1998a. Application of agricultural waste as peat substitute for soilless culture (in Chinese). Trans. Chinese Soc. Agr. Eng. 14 (suppl):177–180.

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5 Greenhouse Tomato Fruit Cuticle Cracking Martine Dorais Agriculture and Agri-Food Canada Centre de Recherche en Horticulture Université Laval Ste-Foy, QC, G1K 7P4, Canada Dominique-André Demers and Athanasios P. Papadopoulos Agriculture and Agri-Food Canada Greenhouse and Processing Crops Research Centre Harrow, ON, N0R 1G0, Canada Wim Van Ieperen Horticultural Production Chains Group Wageningen University Marijkeweg 22, 6709 PG, Wageningen, The Netherlands

I. INTRODUCTION II. FRUIT CHARACTERISTICS RELATED TO THE DEVELOPMENT OF CUTICLE CRACKING A. Fruit Anatomy B. Fruit Growth Rate C. Fruit Size and Shape D. Fruit Water Status E. Assimilate Supply to Fruit III. GENETIC ASPECTS OF FRUIT RESISTANCE TO CUTICLE CRACKING IV. CLIMATIC FACTORS RELATED TO THE DEVELOPMENT OF CUTICLE CRACKING A. Light B. Temperature C. Relative Humidity D. CO2 Enrichment Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 163

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V. CULTURAL FACTORS RELATED TO THE DEVELOPMENT OF CUTICLE CRACKING A. Plant Balance B. Irrigation C. Mineral Nutrition D. Electrical Conductivity VI. CONCLUSION LITERATURE CITED

I. INTRODUCTION Research has been directed toward improving the internal and external quality of tomato fruit produced in greenhouses (Dorais et al. 2001a). One of the major problems encountered by greenhouse tomato growers is fruit cuticle cracking (CC), also called russeting, hair cracking, swell cracking, shrink cracking, rain check, crazing, and cuticle blotch. In contrast to concentric and radial fruit cracking where large (one or more cm long by a few mm wide) and deep (a few mm) cracks occur in circles around the stem scar (Fig. 5.1) or radiating from the stem scar (Fig. 5.2), CC are very fine hair-like cracks (0.1 to 2 mm in length) limited to the cuticle and first layers of cells of the epidermis that develop in concentric circles around the stem scar (Fig. 5.3A) or are oriented in all directions on the sides and bottom of the tomato, giving a net-like appearance to the surface of the fruit (Fig. 5.3B). Cuticle cracking downgrades the quality of tomato because it causes poor appearance (roughened skin and

Fig. 5.1.

Circular cracking of greenhouse tomato fruit.

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Fig. 5.2.

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Radial cracking of greenhouse tomato fruit.

cork tissue) and reduces shelf life (Hayman 1987), while concentric and radial fruit cracking immediately renders the fruit unmarketable for fresh consumption. Since the information on CC of greenhouse tomato fruit is limited, we occasionally refer to literature on concentric and radial cracking in field-grown tomato (fruit cracking), and CC in greenhouse sweet pepper. The appearance of tomato CC occurs in the last phase of fruit growth, 42–49 days after anthesis (DAA) (Bakker 1988; Ehret et al. 1993). In fieldgrown tomato, initiation of CC was noted on 2% of the affected fruit at

Fig. 5.3. Concentric cuticle cracking (CC) on the shoulder (A), and multidirectional CC (net-like appearance) on the side (B) of a greenhouse tomato fruit.

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the immature-green, 61% on mature-green, 27% on breaker, and 10% on red stages (Emmons and Scott 1997). Severity of CC is generally correlated to the length of time between crack initiation and fruit harvest (Bakker 1988; Ehret et al. 1993; Demers et al. 2001a). In fruit with severe CC (over 40% of fruit surface affected), cuticular cracks were initiated 6 to 7 days earlier than in fruit with light CC. Fruit most severely affected by CC (over 80% of fruit surface affected) had a longer total growth period and took more time to reach the harvest stage (pink stage) (Bakker 1988). Fruit left on the plant after the turning stage is more susceptible to CC (Peet 1992). CC is common in greenhouse tomato production, where the percentage of harvested fruit affected can vary from 10% to 95% of total fruit (Bakker 1988; Demers et al. 2001a). Over the course of the year, incidence and severity of CC is highest during the summer months and usually low in spring and fall (Demers et al. 2000; Khosla et al. 2000). CC is a problem in many crops, including sweet pepper (Aloni et al. 1998; Aloni et al. 1999; Moreshet et al. 1999), apple (Faust and Shear 1972), pear (Borys and Bustamante-Oranegui 1990), grape (Considine 1982), and sweet cherry (Andersen and Richardson 1982; Belmans and Keulemans 1996). The relationships between cultivars, greenhouse environment, cultural practices and CC are complex in tomato, and recent research has been focused on solving this problem (Chrétien et al. 2000; Demers et al. 2000; Demers et al. 2001a,b; Dorais et al. 2000, 2001c,e; Estergaard et al. 2001; Jobin-Lawler et al. 2002; Simard 2002). This paper presents fruit characteristics related to the development of CC, genetic aspects of fruit resistance to CC, and greenhouse climatic and cultural factors involved in its development. We conclude this review by identifying several prospects for future research.

II. FRUIT CHARACTERISTICS RELATED TO THE DEVELOPMENT OF CUTICLE CRACKING Between species and cultivars, differences in susceptibility to fruit cracking and CC have been associated with fruit cuticle, epidermis and pericarp, fruit shape and size, fruit growth rate, fruit water status, and sugar content (Hankinson and Rao 1979; Koske et al. 1980; Bakker 1988; Den Outer and van Veenendaal 1987; Ehret et al. 1993; Wacquant 1995; Emmons and Scott 1997, 1998a; Demers et al. 2001a; Guichard et al. 2001).

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A. Fruit Anatomy Tomato fruit are composed of flesh (pericarp walls and skin) and pulp (placenta and locular tissue including seeds) (Ho and Hewitt 1986). The skin (epicarp or exocarp) is formed by the cuticle, which is highly integrated to the cell wall of the epidermis (Ho and Hewitt 1986; Emmons and Scott 1998a). CC in tomato fruit is initiated over the cell junctions, where the cuticle is formed of nonreticulate (amorphous) material. Above the epidermal cell wall, where the cuticle is formed of reticulate material deposited in layers, few cracks are initiated (Emmons and Scott 1998a). The cell junction region, because of its amorphous and noncontaining cellulose cuticle, might be less resistant to pressure as the fruit expands. Genotypic differences in composition, skin anatomy, and cell morphology are related to tomato fruit cracking. Indeed, the proportion of trihydroxy C18 cutin monomers decreases during fruit development, which results in a slight reduction in the hydroxylation and intraesterification of the cutin matrix (Holloway and Baker 1970; Baker et al. 1982). The hydroxyl and ester links in the cutin matrix are important for the structural integrity of the cuticle. Other changes in the cuticle composition (increased triterpenols and flavonoids, decreased long chain hydrocarbons) occur during fruit development (Baker et al. 1982), and may also affect cuticle structural integrity, and consequently the CC susceptibility of tomato fruit. Sensitive cultivars had a deeper cutin penetration (3rd layer of epidermal cells) than less-resistant cultivars where cutin only penetrated to 2nd layer (Hankinson and Rao 1979), and had flatter epidermal cells or larger hypodermal cells (Cotner et al. 1969; Hankinson and Rao 1979). The crack resistance of the sticky peel (pe) mutant is associated with highly elastic skin (Ho and Hewitt 1986). Both high tensile strength and extensibility of the skin (elasticity), which vary during fruit development (they are very high during the immature stages of the tomato fruit and then decrease rapidly between maturegreen to early pink stages), are important characteristics of tomato resistance to fruit cracking (Voisey et al. 1970; Kamimura et al. 1972; Hankinson and Rao 1979). Cuticle cracking-resistant genotypes such as ‘Fla. 7497’, ‘Freshmarket 9’, and ‘Campbell 28’ had combined thicker epidermal and cuticle layers (10.38–11.37 µm) than susceptible genotypes such as ‘Fla. 7181’ and ‘Suncoast’ (6.45–7.76 µm) (Emmons and Scott 1998a). Thicker cell walls, however, reduce the extensibility of the epidermis and increase fruit cracking and CC as reported by several authors (Den Outer and van Veenendaal 1987; Wacquant 1995; Guichard

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et al. 2001), and could explain why CC are initiated over the cell junctions. However, correlation between CC resistance and skin elasticity is not often made, although this physiological disorder occurs at the beginning of the last phase of fruit growth, which corresponds to the decrease of skin elasticity, increase of cell wall degrading enzyme activity (pectinases), and changes in the composition of the cuticle. B. Fruit Growth Rate Growth of tomato fruit, from the fertilized ovary to a red ripe, takes from 49 to 70 days according to cultivar, fruit position on the cluster, climatic conditions, and cultural practices. Fruit growth can be divided into three phases. The first phase is characterized by a slow fruit growth (10% of the final weight) for 14–21 days, and very active cellular division. The second phase (for 21–35 days) is one of rapid growth due to cell enlargement, and most of the fruit weight is accumulated by the end of this mature-green stage. By 20–25 days after anthesis (DAA), the rate of growth per day increases to a maximum (0.35 g dw d–1), and then declines. The third phase is characterized by slow growth and intense metabolic changes due to maturation. The cessation of assimilate import occurs about 10 days after the first change of color (Ho and Hewitt 1986). During the day, fruit growth rate increased from morning until midday, then decreased until the end of the day, and remained low through the night (Pearce et al. 1993a,b; Guichard et al. 2001). Cuticular cracking initiation occurs after the time (20–25 DAA) when fruit absolute growth rates reach maximum values, and could not be related to an excessive stretching of the cuticle resulting from a high fruit growth rate. Indeed, the relative growth rates of tomato fruit with and without CC were similar at the time when cuticular cracks are initiated, supporting that fruit growth rate, at the moment cracks occur, is unrelated to the incidence of CC (Bakker 1988; Ehret et al. 1993). Moreover, no correlation between the severity of CC and the fruit relative growth rate at the time cracking was initiated (44 DAA) or at earlier dates (14 and 28 DAA) was found (Ehret et al. 1993). Variations of tomato fruit growth rate during the day (Pearce et al. 1993a,b; Guichard et al. 2001) resulting from changes in the plant water status (Section II.D) and air temperature (Section IV.B) may contribute significantly to CC. C. Fruit Size and Shape According to the theoretical model of Considine and Brown (1981) on the distribution of forces on the fruit surface, stress on the containing

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membrane increases as the radius of the spheroid increases. Hence, the skin of large fruit should be subjected to a greater stress than the skin of small fruit, and therefore should be more likely to crack. Indeed, the incidence and severity of tomato fruit CC were positively correlated to fruit size (Koske et al. 1980; Emmons and Scott 1998a); larger fruit was more frequently affected by CC than smaller fruit (Demers et al. 2001a). However, Ehret et al. (1993) found that decreasing the fruit load on the plant through fruit pruning increased both the size and amount of CC of the fruit, but suggested that the two factors changed independently. That is, increased size did not necessarily cause the increased CC (Ehret et al. 1993; Emmons and Scott 1998a; Demers et al. 2001a). In a spheroid object, stress on the containing membrane also increases as the shape of the spheroid deviates from a perfect sphere toward an oblate or prolate spheroid (Considine and Brown 1981). Greenhouse tomato fruit generally have an oblate shape: 70–80% of fruit have a height (fruit diameter from the calyx to stylar end) to width (horizontal diameter) ratio between 0.75–0.85, resulting in a larger stress at the polar regions. The calyx itself also increases the stress force on the skin (Considine and Brown 1981). The presence of CC around the stem scar and on the side and bottom of spherical tomato fruit cultivars (Section I) supports this model. However, conflicting results are reported in the literature (few cultivars tested) and no clear relationship between tomato fruit shape and CC has been shown (Emmons and Scott 1998a). We also found no direct correlation between fruit shape and tomato CC (data not published). D. Fruit Water Status In plants, water movement is controlled by a water potential gradient, that is, water moves from regions of high to low water potential. Fruit growth is closely linked to water movement to the fruit, which is positively correlated with changes in the stem water potential (Johnson et al. 1992; Pearce et al. 1993a,b; Leonardi et al. 2000; Guichard et al. 2001). In tomato fruit, 85% to 90% of water is imported via the phloem (Ho et al. 1987), together with assimilates (Bertin et al. 2000). Fruit shrinkage, which is associated with water flux out of the fruit, can occur after the night to day transition and is related to a temporary water stress associated with increased water demand as plant transpiration increases rapidly after illumination (Pearce et al. 1993a,b). Fruit shrinkage is also observed at midday under conditions that caused high plant transpiration—high solar radiation and low relative humidity (Leonardi et al. 2000), and could have a major impact on CC of tomato as variations

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in tension forces on the fruit skin is associated with changes in fruit turgor pressure (Ehret et al. 1993; Guichard et al. 2001). Consequently, early morning and the end of afternoon are the most likely moments of the day for initiation of CC (Wacquant 1995; Guichard et al. 2001). In sweet pepper, a daily cycle of fruit shrinkage and expansion resulted in severe CC (Aloni et al. 1999; Moreshet et al. 1999). Water flux through the pedicel could also be involved in tomato fruit CC. The abscission zone in jointed pedicels prevented organic compounds (e.g., sugars) and water from entering the fruit (McCollum and Skok 1960). In fruit with a jointless pedicel (no abscission zone), water movement in and out of the fruit would not be restricted, thus possibly producing larger variations in the fruit water status, which could result in increased incidence of CC in the jointless pedicel fruit. Indeed, Emmons and Scott (1998a) observed for one segregating population that fruit with a jointless pedicel had a higher incidence of CC than fruit with jointed pedicel. E. Assimilate Supply to Fruit Several studies suggest that an increase in assimilate supply to tomato fruit is related to the development of CC. For instance, low fruit load on the plant resulted in an increase in tomato CC (Bakker 1988; Demers et al. 2001a) and percentage of fruit dry weight (Ehret et al. 1993). Under low fruit load or high light levels more assimilates are available for each individual fruit (Ehret et al. 1993; Demers et al. 2000; Khosla et al. 2000; Demers et al. 2001a). Increased assimilate supply to fruit may influence CC through its impact on water flux to the fruit (Guichard et al. 2001). Since water moves from regions of low to high concentration, higher sugar content in the fruit increases the movement of water from the stem and leaves into the fruit. The increased water intake by the fruit would result in a higher fruit turgor pressure, and thus increase the stress applied on the skin and increase the risk of CC. Indeed, when assimilate import to the fruit is eliminated but not the water movement through the xylem (girdled fruit), fruit cracking was eliminated (Peet and Willits 1995).

III. GENETIC ASPECTS OF FRUIT RESISTANCE TO CUTICLE CRACKING Differences in susceptibility to CC or fruit cracking among various tomato cultivars have clearly been established in the past (Cotner et al. 1969; Voisey et al. 1970; Hankinson and Rao 1979; Davies and Hobson

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1981; Cortés et al. 1983; Abbott et al. 1986; Ho and Hewitt 1986; Den Outer and van Veenendaal 1987; Wacquant 1995; Emmons and Scott 1998a). Many genes may be involved in the process of fruit cracking, and each type of cracking may be controlled by specific genes (Cuartero et al. 1981), making it difficult in selecting for resistant cultivars (Peet 1992). As a consequence, very few cultivars resistant to radial cracking (Peet and Willits 1995) and CC are currently available for greenhouse production. Less-susceptible cultivars currently available are of Dutch origin and were developed for growing conditions characterized by low light intensities such as those prevailing in northern Europe. Under conditions conducive to more rapid growth, these cultivars are very susceptible to CC and fruit cracking. Generally, ‘Rapsodie’, ‘Trust’, ‘Quest’, ‘Clarion’, ‘Baronie’, and ‘Romance’, which are frequently used by commercial growers, are susceptible to CC, while ‘Rz 74/56’ is slightly less sensitive to CC and ‘Tradiro’ is moderately resistant. In studies on CC-resistant and sensitive genotypes of tomato, Emmons and Scott (1998a,b) observed that epicarp thickness was an important fruit characteristic that significantly affected genotype resistance to CC, while fruit shape and pedicel type (jointed vs. jointless) were of minor importance. Development of greenhouse tomato cultivars resistant to CC should also be done in accordance with other criteria such as resistance to diseases, yield, plant vigor, fruit type, fruit flavor, and fruit shelf life (Dorais et al. 2001a).

IV. CLIMATIC FACTORS RELATED TO THE DEVELOPMENT OF CUTICLE CRACKING The incidence of tomato fruit CC varies through the growing season, suggesting the involvement of climatic factors (Ehret et al. 1993; Demers et al. 2000; Khosla et al. 2000; Demers et al. 2001a). Light, temperature, relative humidity, and CO2 may affect CC development by their influence on fruit anatomy, growth, and turgor pressure. A. Light Cuticle cracking of greenhouse tomato fruit progressively increases as the natural light level increases in spring and summer (Demers et al. 2000; Khosla et al. 2000), and decreases with the decline in light level during the fall season (Ehret et al. 1993). However, no direct relationship between light level and CC of greenhouse tomato has been shown (Estergaard et al. 2001; Ehret et al. 2002; Simard 2002). In field tomato, a positive relationship between light level and CC was reported (Frazier and

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Bowers 1947), but no direct relationship has been shown. Although decreased fruit cracking was measured when field tomato plants or fruits were shaded with muslin (Brown and Price 1934; Frazier and Bowers 1947), a decrease in the assimilate supply to the fruit could have explained this reduction. In contrast to sweet pepper (Moreshet et al. 1999) and apple (Faust and Shear 1972), the direct effect of light on tomato skin structure and CC has not been studied. B. Temperature Increasing CC with light level could be related to an increase in air and fruit temperature, as exposure of tomato fruit to direct sunlight increased fruit temperature (Cockshull et al. 1992). Corey and Tan (1990) suggested that with increasing fruit temperature, increasing gas pressure inside the fruit could cause the fruit to expand in volume, thus stretching the skin of the fruit. However, gas pressures inside the fruit are very low (Almeida and Huber 2001) and possible variations are unlikely to cause volume changes that can be related to fruit cracking and CC. Temperature is the most important climatic factor influencing sink strength and consequently photoassimilate partitioning between plant organs. Thus, an increase in fruit temperature could indirectly increase CC by an increase of assimilate supply to the fruit (Walker and Ho 1977) and an increase of the fruit growth rate (Pearce et al. 1993a,b). Recently, Simard (2002) observed under Quebec (Canada, 46–47° N, 71° W) conditions that CC was positively and linearly correlated with the averages of the day (optimal for minimizing CC at 20–21°C), night (optimal for minimizing CC at 18°C), and daily (24-hr) temperatures (optimal for minimizing CC at 19°C), as well as with the average of the day/night temperature differential (optimal for minimizing CC at <6°C). Similarly, it was shown that a daily temperature average between 19.25 to 20.25°C is optimal for minimizing CC of greenhouse tomato under British Columbia (Canada, 45°28 N, 73°45 W) conditions (Estergaard et al. 2001; Ehret et al. 2002). For lower daily temperature (average of 17°C), no difference in CC was noted when plants were grown under low day/high night, high day/low night or constant temperature regimes (Schilstra-van Veelen and Bakker 1985). Contrary to tomato, low night temperature resulted in increased CC in greenhouse sweet pepper due to a lower leaf transpiration rate and increased water flow to the fruit (Aloni et al. 1998; Moreshet et al. 1999). C. Relative Humidity Relative humidity (RH) indirectly affects the development of CC through its influence on plant transpiration, and consequently fruit water status.

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High RH decreases leaf transpiration, which might result in increased fruit water supply and turgor pressure. Under such conditions, a greater stress would be applied to the fruit skin, which would increase the likelihood of the development of CC. This effect of high RH on CC would be more pronounced if the high RH occurred at night when leaf transpiration is already reduced. In a recent study of tomato CC in relation to many climatic and cultural conditions, Estergaard et al. (2001) found that CC was negatively correlated with vapor pressure deficit (VPD) during the night and positively correlated with VPD during the day, while Simard (2002) observed that tomato CC was negatively correlated with 24-hr average VPD. Similarly, tomato CC and fruit cracking were observed more frequently at low VPD (Bertin et al. 2000). For close RH intervals (low RH of 70%; high RH of 85%), however, occurrence and severity of tomato fruit CC was similar under high day/low night and low day/high night RH regimes (Demers et al. 2001a). Similarly, Schilstra-van Veelen and Bakker (1985) noted no significant difference in tomato fruit CC when plants were grown under either low day/high night (24-hr RH average of 81%), high day/low night (24-hr RH average of 82%), continuous low (78%) and continuous high (87%) RH regimes. Since the effect of RH on tomato CC is likely through its influence on the plant water status, it is possible that factors such as temperature, light and irrigation, which can also influence the plant water status, may affect the plant response to RH treatments and partly explained different results reported in the literature. On the other hand, clear interaction between RH and plant fruit load on fruit cracking has been observed by Bertin et al. (2000). The use of misting for increasing RH during the summer increases the incidence of CC and fruit cracking (Bertin et al. 2000; Leonardi et al. 2000). This is due to a better plant water status, a lower plant transpiration, and an increase in the water and carbon fluxes entering the fruit (Guichard 1999). D. CO2 Enrichment Enrichment of the atmosphere with CO2 is common practice in greenhouse tomato production to increase photosynthesis, plant growth, fruit set, fruit size, and the number of fruit produced (Frydrych 1984; Yelle et al. 1987; Yelle et al. 1990). The lower leaf to fruit ratio resulting from higher number of fruit under high CO2 concentration could explain the lower CC generally observed (Section V.A). Estergaard et al. (2001) suggested that, in British Columbia (Canada), the CO2 level of the greenhouse atmosphere should be maintained between 785 and 950 µmol L–1 for minimizing CC of tomato. A similar finding was previously reported under 600–1500 µmol L–1 (Kretchman and Bauerle 1971).

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V. CULTURAL FACTORS RELATED TO THE DEVELOPMENT OF CUTICLE CRACKING A. Plant Balance To insure long-term productivity, commercial greenhouse tomato growers adjust the balance between vegetative and reproductive growth by routinely pruning leaves and fruits to maintain plant vigor. While removal of older leaves had no significant effect on tomato CC (Ehret et al. 1993), a positive relationship between the number of leaves on the plant and tomato fruit CC has been found (Estergaard et al. 2001). For beefsteak tomato ‘Rhapsodie’, low leaf number (13–15 leaves, 42–46 cm long) should be kept on the plant to minimize CC (Estergaard et al. 2001). Increasing the leaf:fruit ratio by fruit pruning (Bakker 1988; Ehret et al. 1993; Bertin et al. 2000; Demers et al. 2001a) favors CC and tomato fruit cracking (Guichard et al. 2001), while decreasing the leaf :fruit ratio by deleafing decreases CC (Demers et al. 2001a). Fruit pruning had a much stronger effect on CC than leaf pruning (Demers et al. 2001a), and could be disastrous in terms of external appearance (CC) when used to promote individual fruit size under high VPD in summer (Bertin et al. 2000). Similarly, Ehret et al. (1993) observed increased CC in fruits from plants subjected to severe fruit pruning compared to deleafed and normally pruned plants. These results could be explained by changes in the source/sink balance of the plant leading to an increase in the supply of assimilates and water toward the fruit (Guichard et al. 2001). When comparing fruit of the same size but from the different leaf :fruit ratio treatments, both Ehret et al. (1993) and Demers et al. (2001a) noted that CC occurred more frequently and was more severe in treatments with high leaf :fruit ratio. Estergaard et al. (2001) found that higher average weekly yield (2.0–2.7 kg m–2 per week) related to lower levels of greenhouse tomato CC, and observed no significant differences in CC severities between truss positions. In order to minimize CC in beefsteak tomatoes in Canada, more fruits per truss are advised to be kept in summer than in spring and fall (Demers et al. 2001a). For example, under South Eastern Canadian growing conditions (42°02 N, 82°54 W), clusters of beefsteak tomato ‘Trust’ and ‘Rapsodie’ should be pruned to 4 fruit during spring (March until May) and fall (September until December), and to 5 fruit during the summer (June until August) to minimize CC (Demers et al. 2001a). B. Irrigation In modern greenhouse vegetable production, plants are grown in soil-less media. Fertilization is generally accomplished by adding soluble fertilizers in the irrigation water, and the resulting nutrient solution is dis-

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tributed to plants using a drip irrigation system. The one exception is the nutrient film technique (NFT), in which roots grow in a continuously circulating shallow stream (film) of nutrient solution. The daily amount of nutrient solution and frequency of irrigation strongly influence CC and fruit cracking (Abbott et al. 1985; Abbott et al. 1986; Peet 1992; McAvoy 1995; Peet and Willits 1995; Chrétien et al. 2000). A larger supply of water (at constant number of irrigations) increases the average water potential in the root environment, which probably increased fruit turgor pressure and consequently caused CC and fruit cracking (Peet and Willits, 1995). Abbott et al. (1986) observed a reduction in the incidence of greenhouse tomato fruit cracking when the daily irrigation frequency was changed from 1 to 4 waterings per day, while total daily irrigation quantity remained the same. It has been shown that a sudden increase in media water content reduces the elasticity of the tomato cuticle (Kamimura et al. 1972). Infrequent irrigation probably results in alternation of episodes of low growth rate or even water efflux from the fruit and turgor loss (around midday) during periods of drought, and episodes of sudden high water flux entering the fruit immediately after irrigations. This may cause excessive turgor pressures resulting in CC as well as changes in epidermis and cuticle elasticity, causing changes in sensitivity for CC (Kamimura et al. 1972; Guichard et al. 2001). To reduce fruit cracking, Peet and Willits (1995) suggest that the amount of water provided to plants should be based on the amount of water the plants are using at the time. Results from a radiation-based water management study showed that the percentage of cracked fruit (CC and fruit cracking) did not increase when irrigation frequency (100 ml plant–1 per irrigation) was increased from 612 to 468 KJ. m–2 of solar radiation received (Chrétien et al. 2000). Drastic effects of inadequate watering (frequency and volume) on fruit cracking have been reported for field tomato (Brown and Price 1934; Frazier 1934; Frazier and Bowers 1947; Emmons and Scott 1997). C. Mineral Nutrition Since the development of tomato CC is related to variations in tension forces on the fruit surface caused by various climatic and cultural factors during the period when the epidermis loses its elasticity, mineral nutrients associated with the stability, elasticity, and flexibility of the cell wall are important in the prevention of tomato CC and fruit cracking (Wilson 1957; Gill and Nandpuri 1970; Simon 1978; Jobin-Lawler et al. 2002). Inside the cell, calcium linked to pectic acids of the middle lamellae is responsible for maintaining cell wall and tissue rigidity (Marschner 1995). Calcium pectate is also involved in cell wall plasticity and elongation (Yamauchi et al. 1986). In periods of rapid plant

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growth (for example, under high irradiance), an accelerated cellular enlargement and fruit development require an additional supply of nutrients such as calcium. Due to the immobility of Ca in the phloem, Ca in the leaves will not be remobilized to the fruit and Ca supply to the fruit is restricted to the xylem water that accounts for less than 15% of total water import by a fruit (Ho et al. 1987). Therefore, Ca distribution to fruit is less than 2% of total calcium content (Ehret and Ho 1986b; Ho 1999). In addition, Yamauchi et al. (1986) showed that boron plays an important role in calcium metabolism of the cell wall. A boron deficiency in tomato plants can decrease the calcium concentration associated with pectic compounds. Consequently, boron has a stabilizing effect on calcium complexes of the middle lamella and is thus essential to the maintenance of the structure of the cell wall (Clarkson and Hanson 1980). Early works showed that boron and calcium sprayed individually or in combination had a highly significant effect in reducing tomato fruit cracking (Wilson 1957; Gill and Nandpuri 1970). Recently, it has been shown that weekly or bi-monthly cluster calcium and boron spraying (6.6 g L–1 CaCl2 + 3g L–1 borax) on 40- to 60-day-old fruit reduced significantly the proportion (11%–15%) and the severity (47%–66%) of fruits with CC and increased the proportion of fruits of Class 1 (Dorais et al. 2000; Dorais et al. 2001c,e; Jobin-Lawler et al. 2002). Boron concentration in those fruits was two times higher than control fruits (water spraying), which is beneficial for human health (Hunt and Stoecker 1996). They also observed that the commercial spray ramp spraying at low concentration (0.38 g L–1 Borax + 6.66 g L–1 CaCl2 on fruit and leaves) reduced the occurrence and severity of CC by 25% and 50%, respectively, compared to the water control treatment, without visual boron phytotoxicity or yield and fruit size reduction. Under warmer growing conditions (higher radiation, temperature, and RH), however, Demers et al. (2001b) observed that similar calcium and boron concentration treatments produced slight necrosis spots (phytotoxicity) on the apex of the sepals. Increasing the calcium level in the nutrient solution by 1.25- to 1.50fold (238 to 371 ppm Ca) of the normal calcium concentration (144 to 238 ppm Ca) resulted in a decrease (5%, P <0.10) of the incidence of CC of greenhouse tomato fruit (Demers et al. 2001b), while Schilstra-van Veelen and Bakker (1985) observed no significant decrease in tomato fruit CC when the calcium concentration of the nutrient solution fed to the plants was increased by 1.6-fold. Increasing the calcium level in the nutrient solution is a practice that should be used carefully, since its effect on CC is little and may compete with other nutrients, such as potassium, and decrease other quality fruit attributes (Dorais et al.

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2001a). Peet and Willits (1995) observed in their irrigation experiments that the number of fruits with blossom-end rot (BER), also caused by local Ca deficiency in the fruits, was inversely proportional to the number of cracked fruits. They attributed this to over-stimulation of water and concomitant Ca transport toward fruits, which reduces the incidence of BER, but increases the incidence of fruit cracking by an increase in turgor. High N, P, and Cl levels in the nutrient solution can interact negatively (N) or positively (P and Cl) (De Kreij et al. 1992; De Kreij 1996) with Ca uptake in tomato (Van der Boon 1973; Bar-Tal and Pressman 1996) or have an effect on cell growth (Eggert and Mitchell 1967; Faust and Shear 1972). However, recently it was observed that N (100 to 309 ppm), P (minimum 20 to 72 ppm), and Cl (30 to 200 ppm) levels in the nutrient solution had no influence on the incidence and severity of tomato CC (Demers et al. 2001b). D. Electrical Conductivity Adjusting the electrical conductivity (EC) of the nutrient solution allows greenhouse growers to modify water availability to the plant (lower water potential), which will reduce the water flow into the fruit and therefore the rate of fruit expansion (Johnson et al. 1992). Under high ECs, tomato fruit generally have a smaller size (Ehret and Ho 1986a,b; Adams 1991; Pearce et al. 1993b; Hao et al. 1998; Dorais et al. 2001b), thicker and more resistant cuticle, a lower turgor pressure (Verkerke and Schols 1992), and a lower susceptibility to CC and fruit cracking (Sonneveld and Van der Burg 1991; Chrétien et al. 2000; Hao et al. 2000). However, fruit strength (sink activity) and the quantity of photoassimilates imported by the fruit are not affected by a moderate-high EC normally found in greenhouse hydroponic culture, and by a reduction in water absorption (Ehret and Ho 1986a; Ho 1996a,b). Increasing the EC by 1.3-fold of the control EC (2.6–4.6 compared to 2.0–3.5 mS cm–1) for a greenhouse tomato spring crop reduced the incidence of fruit with CC and fruit cracking by 68% (Chrétien et al. 2000). Similarly, Hao et al. (2000) found that an EC of 3.82 mS cm–1 compared to 2.54 mS cm–1 decreased the incidence of tomato CC. For similar ECs (3.5 vs. 2.5 mS cm–1), Schilstra-van Veelen and Bakker (1985) observed no significant effect, which could be explained by different growing conditions and cultivars (Cortés et al. 1983; Abbott et al. 1985, 1986). For greenhouse tomato plant grown in a split root system and irrigated with different EC values (0.75 to 5.0 mS cm–1), high EC tended to decrease the CC index from 0.44 to 0.28 (0, unaffected, to 3, heavily affected fruit) (Sonneveld

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and Voogt 1990). Using a neural network model, Estergaard et al. (2001) found a significant effect of EC on CC of beefsteak-type tomato and recommend a range value of 3.90 and 4.35 mS cm–1 for minimizing greenhouse tomato fruit CC under their growing conditions. The relationship between EC levels and tomato CC could also be influenced by climatic factors such as CO2 concentration. For example, a high supply of photoassimilate to the fruit under CO2 enrichment associated with a high uptake of water under low EC increased the fruit susceptibility to fruit cracking. Sudden dramatic changes to root zone EC during the day due to climatic variations can have a negative effect on plant water status and consequently on tomato fruit quality such as CC (Dorais et al. 2001b). However, studies on the influence of a diurnal-EC-variation strategy supplying a low EC feed solution during the active plant transpiration period and a high EC solution for the remaining part of the day on the occurrence of CC have not been conclusive (Adams and Ho 1989; Niedziela et al. 1993; Hao et al. 2000; Dorais et al. 2001d). Indeed, no difference in tomato fruit CC of plants fed with a nutrient solution with a varying EC (1.5 to 2.7 mS cm–1 during midday, 3.0 to 4.0 mS cm–1 for the remaining of the day) and plants fed with a solution with a constant daily EC (1.8 to 3.5 mS cm–1 according to the solar radiation) was found (Dorais et al. 2001d). For a similar daily EC average of 3.82 mS cm–1, no difference was also observed in the incidence of fruit CC between tomato plants receiving a nutrient solution with a low EC in morning and noon and high EC in afternoon and night, and in plants fed with a constant EC nutrient solution (Hao et al. 2000). In comparable experiments with fluctuating EC levels, Van Ieperen (1996) observed a larger average fruit size and reduced incidence of blossom-end rot in fruits from plants grown at low EC during the day and high EC during the night compared to the constant average EC or opposite fluctuating EC treatment. He did not report effects on fruit cracking or CC.

VI. CONCLUSION Synergistic and antagonistic effects of genetic, climatic, and cultural factors occur and influence greenhouse tomato CC. We conclude that a high fruit load should be kept on the plant according to an adequate plant vigor to minimize CC and insure long-term yield. Cuticle cracking may be considerably decreased by spraying a boron/calcium mix on the fruit or the crop, but this practice requires more labor. High temperatures, large day/night temperature differential, and high relative humidity are

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conditions propitious to the development of CC, and should therefore be avoided. Direct exposure of the fruit to solar radiation may also promote CC. Large variations in fruit water status should be avoided by coordinating the supply of water (frequency and volume, EC), nutrient, and photoassimilates with the stage of shoot and root development and fruit load. Newly developed cultivars, satisfying the criteria of consumers and producers, should also be CC resistant. Future research should investigate the effects of relative humidity, temperature, mineral nutrition, and irrigation practices on the tomato fruit characteristics and fruit water status in relation with the development of CC. This knowledge is essential to the development of predictive models for tomato fruit CC. In addition, reducing CC can be achieved by developing appropriate and reliable irrigation management systems for different substrates based on the monitoring of moisture (TDR) and EC directly in the media and plant water and nutrient uptake (Dorais et al. 2001b). Better automated monitoring of greenhouse crops (Ehret et al. 2001) and water and nutrient supplies (Heinen 2001; Kläring 2001) would increase fruit quality by reducing fruit CC.

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Ho, L. C., R. I. Grange, and A. J. Picken. 1987. An analysis of the accumulation of water dry matter in tomato fruit. Plant Cell Environ. 10:157–162. Ho, L. C., and J. D. Hewitt. 1986. Fruit development. p. 201–239. In: J. G. Atherton and J. Rudich (eds.), The Tomato Crop: a Scientific Basis for Improvement. Chapman & Hall, New York. Holloway, P. J., and E. A. Baker. 1970. The cuticles of some Angiosperm leaves and fruits. Ann. Appl. Biol. 66:145–154. Hunt, C. D., and B. J. Stoecker. 1996. Deliberations and evaluations of the approaches, endpoints and paradigms for boron, chromium and fluoride dietary recommendations. J. Nutr. 126:2441S–2451S. Jobin-Lawler, F., K. Simard, A. Gosselin, A. P. Papadopoulos, and M. Dorais. 2002. The influence of solar radiation and boron-calcium fruit application on cuticle cracking of a winter tomato grown under supplemental lighting. Acta Hort. 580:235–239. Johnson, R. W., M. A. Dixon, and D. R. Lee. 1992. Water relations of the tomato during fruit growth. Plant Cell Env. 15:947–953. Kamimura, S., S. Yoshikawa, H. Ito, and K. Ito. 1972. Studies on fruit cracking in tomato. Bul. Hort. Res. Stat. Ministry Agr. For. Ser. C (Morioka) 7. Khosla, S., A. P. Papadopoulos, C. Breault, D.-A. Demers, and M. Dorais. 2000. The influence of multi-stemming and liquid CO2 supplementation on greenhouse fruit quality, including cuticle cracking. Greenhouse Vegetable Research Team Annu. Rep., Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre, Harrow, ON, Canada. p. 98–102. Kläring, H.-P. 2001. Strategies to control water and nutrient supplies to greenhouse crops: A review. Agronomie 21:311–321. Koske, T. J., J. E. Pallas, and J. B. Jones. 1980. Influence of ground bed heating and cultivar on tomato fruit cracking. HortScience 15:760–762. Kretchman, D. W., and W. L. Bauerle. 1971. CO2 enrichment effects on yield and fruit quality of the new tmv-resistant cultivars of tomatoes. Res. Sum. Ohio Agr. Res. Dev. Cent. Wooster, Ohio. 50:15–18. Leonardi, C., S. Guichard, and N. Bertin. 2000. High vapour pressure deficit influences growth, transpiration and quality of tomato fruit. Scientia Hort. 84:285–296. Marshner, H. 1995. Mineral Nutrition of Higher Plants. 2nd ed. Academic Press, London. McAvoy, R. 1995. Don’t let your tomatoes crack up—Here’s how to prevent those unsightly and profit-robbing cracks on fruit. Am. Veget. Grower, August, p. 46–47. McCollum, J. P., and J. Skok. 1960. Radio-carbon studies on the translocation of organic constituents into ripening tomato fruits. Proc. Am. Soc. Hort. Sci. 75:611–616. Moreshet, S., C. Yao, B. Aloni, L. Karni, M. Fuchs, and C. Stanghellini. 1999. Environment factors affecting the cracking of greenhouse-grown bell pepper fruit. J. Hort. Sci. Biotechnol. 74:6–12. Niedziela, C. E. J., P. V. Nelson, D. H. Willits, and M. M. Peet. 1993. Short-term salt-shock effects on tomato fruit quality, yield, and vegetative prediction of subsequent fruit quality. J. Am. Soc. Hort. Sci. 118:12–16. Pearce, B. D., R. I. Grange, and K. Hardwick. 1993a. The growth of young tomato fruit. I. Effects of temperature and irradiance on fruit grown in controlled environment. J. Hort. Sci. 68:1–11. Pearce, B. D., R. I. Grange, and K. Hardwick. 1993b. The growth of young tomato fruit. II. Environmental influences on glasshouse crops grown in rockwool or nutrient film. J. Hort. Sci. 68:13–23.

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Peet, M. M. 1992. Fruit cracking in tomato. HortTechnology 2:216–223. Peet, M. M., and D. H. Willits. 1995. Role of excess water in tomato fruit cracking. HortScience 30:65–68. Schilstra-van Veelen, I. M., and J. C. Bakker. 1985. Cracking of tomato fruits. Ann. Rep. Glasshouse Crops Research Experimental Station, Naaldwijk, Netherlands. p. 39–40. Simard, K. 2002. L’influence de la conduite des cultures sur l’incidence et la sévérité du micro-fendillement de la cuticule de la tomate de serre produite au Québec. Mémoire de maîtrise, Faculté des Études Superieures, Université Laval, Ste-Foy, Québec, Canada. Simon, E. W. 1978. The symptoms of calcium deficiency in plants. New Phytol. 80:1–15. Sonneveld, C., and A. M. M. Van der Burg. 1991. Sodium chloride salinity in fruit vegetable crops in soil-less culture. Netherlands J. Agr. Sci. 39:115–122. Sonneveld, C., and W. Voogt. 1990. Response of tomatoes (Lycopersicon esculentum) to an unequal distribution of nutrients in the root environment. Plant and Soil 124:251–256. Van der Boon, J. 1973. Influence of K/Ca ratio and drought on physiological disorders in tomato. Neth. J. Agr. Sci. 21:56–67. Van Ieperen, W. 1996. Consequences of diurnal variation in salinity on water relations and yield of tomato. University of Wageningen. Ph.D. Thesis. Verkerke, W., and M. Schols. 1992. The influence of EC level and specific nutrients on the firmness, taste and yield of tomato. Glasshouse Crops Res. Stat., Naaldwijk. p. 37. Voisey, P. W., L. H. Lyall, and M. Kloek. 1970. Tomato skin strength—its measurements and relation to cracking. J. Am. Soc. Hort. Sci. 95:485–488. Wacquant, C. 1995. Microfissures ou rugosité des fruits de la tomate. Ctifl, Centre de Balandran, France. Walker, A. J., and L. C. Ho. 1977. Carbon translocation in tomato fruit: Carbon import and fruit growth. Ann. Bot. 41:813–823. Wilson, I. S. 1957. Growth cracks in tomato. Queensland Agr. J. 83:371–374. Yamauchi, T., T. Hara, and Y. Sonoda. 1986. Distribution of calcium and boron in the pectin fraction of tomato leaf cell wall. Plant Cell Physiol. 27:729–732. Yelle, S., R. C. Beeson, M. J. Trudel, and A. Gosselin. 1990. Duration of CO2 enrichment influences growth, yield, and gas exchange of two tomato species. J. Am. Soc. Hort. Sci. 115:52–57. Yelle, S., A. Gosselin, and M. J. Trudel. 1987. Effect of atmospheric CO2 concentration and root-zone temperature on growth, mineral nutrition, and nitrate reductase activity of greenhouse tomato. J. Am. Soc. Hort. Sci. 112:1036–1040.

6 Fresh-Cut Vegetables and Fruits* Jeffrey K. Brecht Horticultural Sciences Department University of Florida Gainesville, Florida 32611-0690 Mikal E. Saltveit Department of Vegetable Crops University of California Davis, California 95616-8631 Stephen T. Talcott, Keith R. Schneider, and Kelly Felkey Food Science and Human Nutrition Department University of Florida Gainesville, Florida 32611-0370 Jerry A. Bartz Plant Pathology Department University of Florida Gainesville, Florida 32611-0680

I. INTRODUCTION II. PHYSIOLOGY A. Physiological Consequences of Wounding 1. Ethylene Production 2. Lipid Degradation 3. Respiration 4. Discoloration *This review was adapted and updated from the USDA, CSREES Multistate Research Project S-294 Project Proposal. 1998. “Postharvest Quality and Safety in Fresh-cut Vegetables and Fruits.” http://research.ifas.ufl.edu/s294/index.html. Florida Agricultural Experiment Station Journal Series No. R-09235. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 185

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J. BRECHT, M. SALTVEIT, S. TALCOTT, K. SCHNEIDER, K. FELKEY, AND J. BARTZ B. Wound Healing C. Water Loss D. Disorders 1. Chilling Injury 2. Atmosphere Injury SENSORY QUALITY A. Appearance B. Texture C. Taste and Aroma 1. Soluble Sugars and Organic Acids 2. Aroma Volatiles PHYTONUTRIENTS A. Fresh-cut Effects on Phytonutrients 1. Carotenoids 2. Ascorbic Acid 3. Polyphenolics 4. Secondary Metabolites B. Prevention of Nutrient Loss 1. Physicochemical Treatments 2. Modified Atmospheres 3. Edible Coatings and Dips MICROBIOLOGY A. Decay B. Food Safety TREATMENTS TO MAINTAIN QUALITY A. Physical 1. Modified Atmospheres 2. Heat Treatments 3. Irradiation B. Chemical 1. Antimicrobials 2. Browning Inhibition 3. Firmness Retention 4. Edible Coatings CONCLUSIONS LITERATURE CITED

I. INTRODUCTION “Fresh-cut” refers to raw vegetables and fruits that have been cut, shredded, peeled, abraded, or otherwise prepared to produce convenient ready-to-eat or ready-to-cook portions. Early terminology referred to “minimal processing,” which was described as “handling, preparation, packaging and distribution of agricultural commodities in a fresh-like state” (Shewfelt 1987). The term “minimally processed” evolved into “lightly processed” (Huxsoll et al. 1989; Abe and Watada 1991), how-

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ever, “fresh-cut” is currently the most widely accepted term (Watada et al. 1996; Watada and Qi 1999; Gorny 2001; Saltveit 2002). Key criteria for a vegetable or fruit product to be considered a “fresh-cut” product include that it consist of 100% usable material (IFPA 2000) and that the tissue is in a living, respiring physiological state (USFDA 2000). The term “minimally processed” now is used primarily in reference to products (including non-plant foods) that are retained in a “fresh-like” state following mild processing techniques such as blanching, ultra-highpressure treatment, or osmotic dehydration (Tapia deDaza et al. 1996; Butz and Tauscher 2000; Moreno et al. 2000; Pardio et al. 2000; Vijayanand et al. 2001; Hill et al. 2002). Fresh-cut vegetables and fruits are a relatively new and rapidly developing part of the U.S. fresh produce industry. Farm income in 2000 from vegetables and fruits was about $46 billion and consumer expenditures for fresh produce totaled about $108 billion (U.S. Dept. of Comm. 2001). Industry estimates in the U.S. indicate that sales of fresh-cuts average about 10% of total produce sales ($10–12 billion) per year, including $1.6 billion for packaged salads (IFPA 2000). No estimates for postharvest losses of fresh-cut produce are available, but an earlier estimate (Pierson et al. 1982) of from 9% to over 16% losses of all fresh produce is likely to be conservative given the added perishability of fresh-cut compared to intact produce. Using these percentages, the retail value of fresh-cut produce losses may approach $2 billion annually. Growing evidence suggests that increasing dietary consumption of vegetables and fruits has long-term health benefits, and may prevent or reduce the risk of some chronic diseases. For example, certain naturally occurring polyphenols (or flavonoids) seem to function via one or more biochemical mechanisms to interfere with, or prevent, carcinogenesis. The antioxidants vitamin C, vitamin E, and β-carotene are known to prevent the oxidation caused by free radicals that lead to damage to cells and DNA and many degenerative diseases. In addition, several other carotenoids such as lycopene, lutein, and zeaxanthin are known to exhibit antioxidant properties. Since vegetables and fruits in our diet are the major sources of these important antioxidants, maximum utilization through proper fresh-cut processing of vegetables and fruits is highly desirable. The attractiveness and convenience of fresh-cut vegetables and fruits are helping to bring about increased consumption of fresh produce, but these benefits are offset by the rapid deterioration/short shelf life of the products in the marketplace and the potential health hazards associated with spoilage. Understanding the physiology of fresh-cut vegetables and fruits is essential for ensuring their wholesomeness and

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nutritional value, and for developing the most effective handling procedures and innovative, new technologies for maintaining their quality to meet increasing consumer demand. To date, the fresh-cut industry has relied on established technologies derived mainly from studies and experience with whole, intact produce to provide some control of product deterioration. These technologies have proven to be barely adequate to supply high-quality product to domestic markets as evidenced by the trend of the major U.S. freshcut processors to establish regional processing facilities in place of earlier attempts to ship their product cross-country from facilities located in the production region (mainly California). The current practices are thus obviously insufficient to consistently supply more distant export markets. Increasing the storage life of fresh-cut produce by developing new techniques for slowing the rate of deterioration would greatly expand the opportunities for the industry to supply high-quality freshcut vegetables and fruits to local and export markets. However, such techniques should not suppress growth of microorganisms causing spoilage while at the same time create a niche for the growth of human pathogens that might be present on vegetables and fruits. In any approach to studying quality or safety of fresh-cut produce, the two concepts must be integrated. Increased convenience and consumer desires for fresh rather than traditionally processed items have driven sales of fresh-cut vegetables while potentially compromising the safety of the products. Likewise, any technique focused solely on improving safety that results in products unacceptable to the consumer is doomed to failure. Fresh-cut vegetable and fruit products differ from traditional, intact vegetables and fruits in terms of their physiology and their handling requirements. Fresh-cut produce is essentially purposely wounded plant tissue that must subsequently be maintained in a viable, fresh state for extended periods of time. Fresh-cut vegetables deteriorate faster than intact produce. This is a direct result of the wounding associated with processing, which leads to a number of physical and physiological changes affecting the viability and quality of the produce (Brecht 1995; Saltveit 1997). The visual symptoms of deterioration of fresh-cut produce include flaccidity from loss of water, changes in color (especially increased oxidative browning at the cut surfaces), and microbial contamination (King and Bolin 1989; Varoquaux and Wiley 1994; Brecht 1995). Nutrient losses may also be accelerated when plant tissues are wounded (Klein 1987; Matthews and McCarthy 1994), however, compared to physiological and microbial changes that occur with time, little information is available concerning the retention of many vitamins,

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minerals, nutritive components, and antioxidant constituents in freshcut produce during handling, storage, and senescence. The knowledge that has developed to date concerning the postharvest physiology and handling requirements of fresh-cut produce indicates that fresh-cut produce behaves differently and thus must be handled differently than the corresponding intact vegetables and fruits. This means that the knowledge accumulated over many decades regarding the physiology and handling of commercial vegetable and fruit crops has had to be reexamined and new understanding and information developed for each fresh-cut produce item. The increased perishability of fresh-cut produce items compared to the corresponding intact crops also requires that questions be addressed regarding maintenance of nutritional and other aspects of postharvest quality that have not previously been addressed at all for certain crops. The study of fresh-cut produce handling has been confined to little more than the last two decades. The earliest studies already showed the beneficial effects of temperature control, minimizing the microbial load, ensuring knife sharpness, application of antibrowning and firming chemicals, removal of adhering surface liquid, and modification of the package atmosphere on the stability of various salad vegetables and fruits (Ponting et al. 1972; Priepke et al. 1976; Bolin et al. 1977). Early research and commercial success focused on fresh-cut salad vegetables (Garg et al. 1990; Bolin and Huxsoll 1991; Howard et al. 1994) with a primary emphasis on modified atmosphere packaging (MAP) to slow respiration and decay (Cameron et al. 1995). More recent research and commercial emphasis is focusing on fresh-cut fruits and melons (Kim et al. 1993; O’Connor-Shaw et al. 1994, 1996; Cartaxo et al. 1997; Gorny et al. 1998; Portela and Cantwell 1998). Fruits for fresh-cut products need to be harvested as close to fully ripe as possible. Some challenges associated with development of fresh-cut fruit products include within-fruit tissue variability and dramatic ripeningrelated textural changes. In addition to the above, the delicate and evanescent flavors of fresh fruits suggest that the commercialization of fresh-cut fruits will be more difficult than that of fresh-cut vegetables (Gorny et al. 1998). The first reviews on fresh-cut vegetables and fruits appeared in a 1987 issue of the Journal of Food Quality devoted entirely to various aspects of the topic (Barmore 1987; Brackett 1987; Klein 1987; Rolle and Chism 1987; Shewfelt 1987). The authors were forced by lack of availability of specific information on fresh-cut products to extrapolate and speculate based on knowledge from whole produce. The proceedings of a colloquium sponsored by the American Society for Horticultural Science in 1993 documented the expansion of interest in fresh-cuts (Baldwin et al.

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1995a; Brecht 1995; Burns 1995; Cameron et al. 1995; Hurst 1995; Romig 1995; Schlimme 1995). Individual, general reviews of fresh-cut physiology and handling include Huxsoll et al. (1989), King and Bolin (1989), Watada, et al. (1990), Brecht (1995), Ahvenainen (1996), and Saltveit (1997). Topics related to fresh-cut vegetables and fruits that have been the subject of individual reviews include quality (Watada et al. 1996; Watada and Qi 1999), coatings (Baldwin et al. 1995a,b), enzymatic browning (Sapers 1993; Artes et al. 1998; Laurila et al. 1998), packaging (Myers 1989; Cameron et al. 1995), sanitation (Hurst 1995), microbiology (Garg et al. 1993; Francis et al. 1999; Nguyen-the and Carlin 1994), and the interaction of microbiology and MAP (Church and Parsons 1995; Zagory 1999). There have also been several books devoted to fresh-cut vegetables and fruits (Wiley 1994a; Alzamora et al. 2000; Lamikanra 2002). A recent book chapter describes handling systems for fresh-cut fruits and vegetables (Cantwell and Suslow 2002). The most recent handling recommendations for fresh-cut vegetables and fruits are found in the newly revised USDA Handbook 66 (Barth et al. 2002; Beaulieu and Gorny 2002). This review will cover the general responses of vegetables and fruits to fresh-cut processing in terms of their physiology, sensory quality, nutritional value, and microbiology, as well as the treatments used to maintain fresh-cut vegetable and fruit quality.

II. PHYSIOLOGY “The physiology of (fresh-cut) vegetables and fruits is essentially the physiology of wounded tissue” (Brecht 1995). There are immediate physical effects of fresh-cut processing, including mechanical shocks to the tissue, removal of the protective epidermal layer, accumulation of surface moisture, and exposure of the interior tissues to contaminants (Table 6.1). Later, as the surface water evaporates and the tissue starts to respond physiologically, there are further alterations in gas diffusion and surface appearance. Wounding induces signals that elicit physiological and biochemical responses in both adjacent and distant tissues (Ke and Saltveit 1989; Saltveit 1997). Many of these induced responses are detrimental to the quality of fresh-cut produce. A few of these changes happen very quickly after wounding, while others can take many days to complete. Some of the physiological effects of wounding are listed in Table 6.2. The earliest physiological responses to wounding include a transient increase in ethylene production and an enhanced rate of respiration, which may be interlinked with induction of phenolic metabolism and the wound healing response of the tissue (Fig. 6.1).

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Physical effects caused by the preparation of fresh-cut vegetables and fruits.

Initial effects Mechanical shock to tissue Bruises, cracks, fractures, tears Hydraulic shocks dispersed or focused by reflective and refractive properties of nonhomogenous tissues within the commodity Removal of protective epidermal layer Alters gas diffusion Water vapor, O2, CO2, C2H4 Provides entry for contaminants Chemicals, microorganisms Liquid on cut surface Reduces gas diffusion Elevated CO2, C2H4 Reduced O2 Accelerates water loss Provides substrate for microbes Liquid in tissue Translucent tissue caused by water in intracellular spaces Density changes in the commodity Subsequent effects Elimination of natural barriers Enhances gas diffusion Reduced internal CO2, C2H4 Elevated internal O2 Loss of aroma volatiles Accelerates water loss Changes in appearance White blush formation because of surface debris desiccation Uneven surface resulting from uneven water loss by tissues Splitting or fracturing resulting from differential changes in turgor Intrusion of water into intracellular spaces causes translucent tissue Juice leakage

Ethylene can in turn stimulate other physiological processes, resulting in accelerated membrane deterioration, loss of vitamin C and chlorophyll, abscission, toughening, and undesirable flavor changes in a range of horticultural crops (Kader 1985; Saltveit 1999). Wounding can also directly compromise flavor and aroma volatile production (Moretti et al. 2002). Wounding plant tissues makes them more susceptible to attack by plant pathogenic microorganisms and possibly more conducive to survival and growth of food poisoning microorganisms (Wells and Butterfield 1997, 1999). In order to develop treatments and handling practices for fresh-cut produce that minimize these negative consequences of wounding, it is necessary to understand the basic biological processes

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Table 6.2.

Physiological effects caused by the preparation of fresh-cut vegetables.

Immediate effects Wound signal (nature, speed) Plant growth regulators (e.g., ABA, ethylene, jasmonic acid, salicylic acid, systemin, traumatin, etc.) Wall fragments Hydraulic Bioelectrical wave Membrane depolarization Increased permeability Mixing of cellular compounds Calcium & signal transduction Vacuole contents released Membrane disorganization Lipid oxidation Free fatty acids production Loss of protoplasmic streaming Subsequent effects Elevated C2H4 production ACC pathway Wound pathway? (ethane) Elevated respiration CO2 production O2 consumption Heat production Fermentative metabolism Oxidative reactions Non-respiratory O2 consumption Browning Induction of enzymes ACC synthase and ACC oxidase PAL, PIIF, etc. Altered phenolic metabolism Phytoalexins Browning substrates Induction of wound healing Lignin and suberin synthesis Cell division Altered protein synthesis Compositional changes Ascorbic acid Organic acids Carbohydrates Sugar to acid balance Toughening Softening Loss of flavor

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underlying the plant responses. In this way, more effective approaches that are more widely applicable to different fresh-cut products may be more quickly developed. Many factors may affect the intensity of the wound response in freshcut vegetables and fruits. Among these are species and variety, stage of physiological maturity, extent of wounding, temperature, O2 and CO2 concentrations, water vapor pressure, and various inhibitors. However, by far the most significant factor affecting the wound response, as in all other postharvest situations, is temperature. Different commodities and tissues may have different capacities and modes of responding to injury. For example, the pith of a celery stalk has lower rates of metabolism compared with cells associated with the phloem in the vascular tissue (Saltveit and Mangrich 1996). A few hours after wounding, tissue at the blossom end of a mature-green tomato fruit produces wound-induced C2H4 at over twice the rate of tissue excised from the equator or stem end (Brecht 1995). When incubated at 20°C, the maximum rates of C2H4 production eventually attained by tomato fruit blossom-end, equatorial, and stem-end tissues were similar, but C2H4 production by tissue from the blossom end peaked about 2 days before tissue from the equator, and tissue from the stem end peaked about 2 days later. Inclusion of such differently responding tissues in the same consumer package may result in produce of uneven quality. A. Physiological Consequences of Wounding Upon preparation of fresh-cut products, various proportions of the tissue are cut, bruised, and bent. The proportion of damaged tissue and the wounding severity varies greatly among different products and for different preparation procedures. Cutting of produce removes the natural protection of the epidermis and destroys the internal compartmentation that separates enzymes from substrates in those cells directly affected. While the number of cells actually cut is relatively small, damaged plant tissue rapidly produces a wound signal that is thought to be responsible for the induction of many physiological responses throughout the tissues, including increased respiration, increased C2H4 production, induction of phenolic synthesis, and the initiation of wound healing (Fig. 6.1). Evidence for propagation of a wound signal includes the temporal and spatial progression of induction of the important phenolic metabolism enzyme phenylalanine ammonia-lyase (PAL) away from a wound site (Ke and Saltveit 1989). The response of plant tissues to wounding usually increases as the severity of the injury increases; however, the level of response appears to be quickly saturated by additional

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WOUND Signal Respiration Ethylene

Phenolic metabolism

Wound healing

Heat Ripening

PAL PPO

Reduced Carbohydrates Organic acids Ascorbic acid

Oxygen

Periderm Phenolic compounds

Softening Poor flavor

Suberin

Cell division Lignin

Browning

Toughening

Fig. 6.1. The interrelationship among the many effects of wounding on physiological processes in fresh-cut vegetables and fruits (Saltveit 1997).

injuries (Ke and Saltveit 1989). A discussion of wound signal hypotheses can be found in Saltveit (1997). 1. Ethylene Production. Wounding of plant tissues induces elevated ethylene production rates (Abeles et al. 1992), which may accelerate deterioration and senescence in vegetative and nonclimacteric tissues and promote ripening or senescence of climacteric tissues. The level of ethylene has been shown in several vegetables and fruits to increase in proportion to the amount of wounding. Wounding climacteric fruits may cause increased ethylene production, which can speed up the onset of the climacteric, resulting in different physiological ages between intact and sliced tissue (Brecht 1995; Watada et al. 1990). Slicing breaker stage tomato fruit increased ethylene production 3- to 4-fold and increased ripening compared to whole fruit (Mencarelli et al. 1989). The peel tissue of climacteric fruits generally produces ethylene at a much higher rate than the fruit flesh; however, the wounding associated with removal of the peel still results in a several-fold increase in ethylene production by fresh-cut slices compared with the whole fruit (Agar et al. 1999; Gorny et al. 2000). Wounding effects differ between climac-

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teric and nonclimacteric fruits (Rosen and Kader 1989) and wound ethylene production is usually greater in preclimacteric and climacteric than postclimacteric tissues (Abeles et al. 1992). Whereas wound ethylene has no effect on ripening of nonclimacteric fruits, it may advance the ripening of climacteric fruits. For example, C2H4 induced by the physical action of cutting was sufficient to accelerate softening of banana and kiwifruit (Abe and Watada 1991). Ethylene production in climacteric fruits is promoted by the endogenous concentration of C2H4 through positive feedback and increases dramatically during ripening. However, the feedback of C2H4 on C2H4 production in nonclimacteric vegetative and fruit tissues is negative (Saltveit 1999). Apart from some transient increases in C2H4 production associated with the traumas of harvest, endogenous C2H4 levels are maintained at low levels by this negative feedback, and endogenously produced C2H4 may have a minimal effect on the postharvest quality of some nonclimacteric vegetables and fruits. Ethylene induced by cutting was sufficient to accelerate chlorophyll loss in spinach but not broccoli (Abe and Watada 1991). As an example of the contrast between climacteric and nonclimacteric tissues, C2H4 production from fresh-cut lettuce (Ke and Saltveit 1989) is much smaller than that from mature-green tomato fruit pericarp discs (Brecht 1995). The maximum rate of C2H4 production from wounded lettuce and tomato was 0.6 and 8.0 ηL g–1 h–1, respectively, and elevated C2H4 production lasted for less than a day for lettuce while it was still elevated after 2 weeks for the tomato discs, which underwent a climacteric and ripened. Furthermore, the induction of PAL activity in lettuce tissue is more rapid in wounded tissue than in C2H4-treated tissue. If wounding acted through the induction of C2H4, then the level of PAL in lettuce tissue exposed to C2H4 should have been higher than in wounded tissue, since the putative step in which wounding induced C2H4 production was bypassed (Ke and Saltveit 1989). In the case of lettuce, elimination of wound-induced C2H4 production would therefore have no effect on the induction of PAL. 2. Lipid Degradation. Wounding of plant tissues in the course of preparation of fresh-cut products may cause membrane lipid degradation (Rolle and Chism 1987; Deschene et al. 1991; Picchioni et al. 1994; Zhuang et al. 1997). Extensive enzymatic degradation occurs in damaged membrane systems, causing loss of lipid components and loss of compartmentation of enzymes and substrates (Marangoni et al. 1996). The ethylene produced upon wounding may play a role in this process by increasing the permeability of membranes and reducing phospholipid biosynthesis (Watada et al. 1990). The enzymatic reactions catalyzed by

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lipid acyl hydrolases and phospholipase D produce free fatty acids from the membrane lipids (Picchioni et al. 1994). These free fatty acids are toxic to many cellular processes and are capable of causing organelle lysis, and binding to and inactivating proteins. Lipoxygenase (LOX) catalyzes the peroxidation of di- and tri-enolic fatty acids to form conjugated hydroperoxides, resulting in the generation of free radicals, which can attack intact membranes, causing further membrane disruption (Thompson et al. 1987; Shewfelt and del Rosario 2000). Lipoxygenase activity is also involved in the production of desirable and undesirable aroma volatiles (Mazliak 1983). Calcium is thought to stabilize membrane systems and maintain cell wall structure in vegetables and fruits (Poovaiah 1986). Calcium has been shown to reduce ethane production, a marker of lipid peroxidation, in potato tuber disks (Evensen 1984). Calcium appeared to both delay senescence-related membrane lipid changes and augment membrane-restructuring processes in fresh-cut carrots (Picchioni et al. 1996). Calcium and a combination treatment of calcium and ascorbic acid were effective in preventing discoloration of fresh-cut apples (Ponting et al. 1972; Drake and Spayd 1983) and pears (Rosen and Kader 1989). 3. Respiration. The increase in respiration seen in wounded plant tissues is thought to be a consequence of elevated ethylene, which stimulates respiration. Breakdown of starch is enhanced, and both the tricarboxylic acid cycle and electron transport chain are activated (Laties 1978). The respiratory climacteric may also be affected by wounding. The respiration rates of fresh-cut vegetables and fruits are generally from a few to over 100% higher than the intact produce (Rosen and Kader 1989; Watada et al. 1990, 1996; Varoquaux and Wiley 1994). However, more extensively damaged tissue (e.g., shredded carrots) can have even greater respiration rates (Varoquaux and Wiley 1994). Respiration of the peel of kiwifruit (Agar et al. 1999) and pear (Gorny et al. 2000) was much higher than that of the fruit flesh, probably stimulated by the much higher ethylene production by peel tissue (see above). However, the respiration rates of peeled slices were still higher than those of intact fruit. Wound respiration in some plant tissues may be related to α-oxidation of fatty acids (Shine and Stumpf 1974), which oxidizes fatty acids to CO2 and has been shown to be responsible for the CO2 released following slicing of potato tubers (Rolle and Chism 1987). Carbon dioxide production increases in tissue undergoing wound healing (see below) as respiration is stimulated to furnish not only energy, but also to synthesize the molecules needed for repair. Other respiratory reactions accelerate softening of some tissues and the toughen-

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ing of others. The breakdown of cell wall components produces soft tissues (e.g., tomato), while the synthesis of lignin strengthens the cell wall of fibers, making the tissue tough and stringy (e.g., asparagus). 4. Discoloration. Browning from oxidation of phenolic compounds and yellowing from loss of chlorophyll occur in fresh-cut vegetables and fruits as a result of the disruption of compartmentation that occurs when cells are broken, releasing acids and enzymes, that can then come in contact with their substrates (Martinez and Whitaker 1995; Heaton and Marangoni 1996; Laurila et al. 1998). Commodities with constitutive high levels of phenolic compounds, like artichoke and potato, brown easily when wounded tissue is exposed to the O2 in air. Wounding also induces synthesis of a number of enzymes involved in the browning reactions or substrate biosynthesis (Rolle and Chism 1987; TomásBarberán et al. 1997). Commodities like lettuce and celery have low levels of naturally occurring phenolic compounds, but wounding stimulates phenylpropanoid metabolism and the subsequent accumulation of phenolic compounds leads to browning in these commodities. Cultivar differences in fresh-cut browning potential have been demonstrated for several fruit species such as apple (Kim et al. 1993) and carambola (Weller et al. 1995). As shown by Hansche and Boynton for peaches (1986), both the concentrations of the substrates and the relative activities of the oxidases can affect the intensity of browning in different genotypes and tissues. Oxidative browning at the cut surface may be the limiting factor for many fresh-cut vegetables and fruits. The browning potential of many vegetable and fruit tissues is affected by their prior treatment (Lopez-Galvez et al. 1996a,b). Stresses (e.g., temperature, physical injury, and disease) tend to increase the production of many phenolic compounds that brown easily upon injury. Many tissues initially low in the activity of enzymes of phenylpropanoid metabolism and in phenolic content (e.g., celery, lettuce) are predisposed by previous stresses to rapidly mobilize the phenylpropanoid pathway and accumulate significant quantities of oxidizable phenolic compounds (Lopez-Galvez et al. 1996b). Phenylalanine ammonia-lyase catalyzes the rate-limiting step in phenylpropanoid metabolism (Ke and Saltveit 1989). Both ethylene and wounding induce PAL activity in many plant tissues (Abeles et al. 1992; Lopez-Galvez et al. 1996b), but apparently by separate mechanisms. Ethylene-induced PAL activity is a good predictor of fresh-cut lettuce storage life (Couture et al. 1993). Investigations utilizing inhibitors of either ethylene synthesis (AVG) or action (STS or 2,5-norbornadiene) have shown that ethylene alone does not control induction of PAL in wounded winter squash (Hyodo and Fujinami 1989)

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or iceberg lettuce (Ke and Saltveit 1989). Browning occurs when the products of phenylpropanoid metabolism, such as various phenolic and possibly other substrates (e.g., anthocyanins) are oxidized in reactions catalyzed by phenolases such as polyphenol oxidase (PPO) or peroxidases (Hanson and Havir 1979; Martinez and Whitaker 1995). Yellowing of fresh-cut green vegetables is due to chlorophyll degradation revealing preexisting yellow carotenoid pigments. Cabbage processed into coleslaw changes from green to a lighter white color because it lacks yellow pigments (Heaton et al. 1996). Degradation of chlorophyll in fresh-cut products may be initiated by wound ethylene or by free radical products of membrane lipid peroxidation (Heaton and Marangoni 1996; Shewfelt and del Rosario 2000). B. Wound Healing The injury associated with the preparation of fresh-cut vegetables and fruits is most likely perceived no differently than the naturally occurring stresses to which plants have evolved elaborate defense responses. In some postharvest situations, these defense responses are encouraged. For example, the curing of potato tubers promotes healing of harvestrelated injuries through the development of wound periderm and suberization of tissue adjacent to the wound (Burton 1966). But in fresh-cut vegetables and fruits, these responses are usually detrimental to the overall quality of the product. For example, wound-stimulated phenylpropanoid metabolism promotes the synthesis and accumulation of phenolic compounds that promote the browning of fresh-cut lettuce (Saltveit 2000). Temperature management is important for minimizing such undesirable reactions related to wound healing. The rate of the reactions related to wound healing would probably be minimal at temperatures below about 5°C (Lipetz 1970). While the physiological processes discussed thus far all probably have as their biological role the ultimate sealing of the site of injury, the phrase “wound healing” generally is used to refer to the production and deposition of suberin and lignin in the walls of cells at the wound site (Dyer et al. 1989; Dixon and Paiva 1995), possibly followed by cell division beneath the suberized layer to form a wound periderm (Burton 1982). This cell wall crosslinking by phenolic compounds has been proposed to be potentially exploitable for improving texture stability in processed plant foods (Waldron et al. 1997). The first visually observed change at the cut surface of plant tissue is desiccation of the first layer of broken cells and one to a few additional subtending layers of cells.

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Suberization of the next layers of cells occurs in many tissues, including potato and yam tubers, sweetpotato and carrot roots, bean pods, and tomato and cucumber pericarp (Kolattukudy 1984; Walter et al. 1990). The environment surrounding the tissue has been shown to influence both suberization and the formation of a wound periderm. Wigginton (1974) reported that suberization of potato tubers can take 3 to 6 weeks at 5°C, 1 to 2 weeks at 10°C, and 3 to 6 days at 20°C, while initiation of the wound periderm requires 4 weeks, 1 to 2 weeks, and 3 to 5 days, respectively. Wound healing of potato at 10°C was optimal at 98% relative humidity (RH) and decreased at RH below 90%, but at 20°C wound healing was similar at all RH levels above 70%. Levels of O2 below 10% and CO2 levels above 5% inhibit suberization and periderm formation in potato tubers (Wigginton 1974; Lipton 1975). Since all fresh-cut products are handled in vapor barrier packages of some sort, high RH levels favoring wound healing are a given. Exposure to moderate (5 to 10°C) temperatures that allow wound healing to occur may, unfortunately, also be all too common (Verlinden and Nicolaï 2000; Jacxsens et al. 2002; Warton and Wills 2002). On the other hand, the modified O2 and CO2 levels within fresh-cut packages would tend to inhibit wound-healing processes. Plants synthesize an array of secondary compounds in response to wounding (Toivonen 1997), many of which appear to be related to wound healing or defense against attack by microorganisms and insects (Dixon and Paiva 1995). The specific complement of secondary compounds formed depends on the species of plant and the tissue involved. In certain cases, these compounds may affect the aroma, taste, appearance, nutritive value, or safety of fresh-cut products. Some aroma and taste compounds may be relatively evanescent, resulting in poor flavor after a short period of storage compared to freshly prepared items, while some off odors and flavors may be relatively persistent. The classes of compounds produced in wounded vegetables and fruits include phenylpropanoid phenolics, polyketide phenolics, flavonoids, terpenoids, alkaloids, tannins, glucosinolates, and long-chain fatty acids and alcohols (Miller 1992). C. Water Loss Plant tissues are in equilibrium with an atmosphere at the same temperature with an RH of 99–99.5% (Gaffney et al. 1985; Rooke and van den Berg 1985). Any reduction of water vapor pressure in the atmosphere below that in the tissue results in water loss. Accelerated water

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loss is a major physical problem with fresh-cut vegetables and fruits. In whole organs, the water in the intercellular spaces is not directly exposed to the outside atmosphere. However, cutting or peeling the fruit or vegetable exposes the hydrated interior tissues and drastically increases the rate of evaporation of water. The difference in rate of water loss between intact and wounded plant surfaces varies from about 5- to 10-fold for organs with lightly suberized surfaces (e.g., carrot and parsnip), 10- to 100-fold for organs with cuticularized surfaces (e.g., spinach leaf, bean pod, and cucumber fruit), to as much as 500-fold for heavily suberized potato tubers (Burton 1982). Maintaining a high RH around the fresh-cut product will reduce the vapor-pressure deficit and minimize water loss. This is most easily accomplished by packaging in barrier films. However, some water loss is unavoidable since removal of the heat of respiration by external cooling creates a gradient of water potential that drives water from the product to the cooling surface. In a package, the cooling surface is the inner surface of the bag. Condensation of water evaporated from the product on the inner surface of the package shows that this concomitant movement of heat and water vapor is ubiquitous. Solutes in the water on the surface of the commodity lower its vapor pressure, but the result is slight in the dilute solutions associated with fresh leafy vegetables and has only marginal effects on evaporation. Fruits, including melons and mature squashes, and some underground storage organs like potato tubers and sweetpotato roots would lose water somewhat less readily. Avoiding desiccation at the cut surface of some fresh-cut products is critical for maintaining acceptable visual appearance. For example, the development of “white blush” on the surface of abraded “baby” carrots, caused by desiccation of cellular remnants on the carrot surface (Tatsumi et al. 1991), is the limiting factor in marketing the product despite the use of polymeric film packages. Surface coatings to minimize water loss are effective, but thick, impermeable coatings may interfere with the diffusion of other gases and produce unwanted anaerobic conditions within the commodity. This is especially true immediately after processing when wounding temporarily stimulates respiration. It is also difficult to formulate coatings that will adhere to the wet, unstable surface of cut vegetables or fruits yet act as a barrier to water loss (Avena-Bustillos et al. 1994, 1997). However, for most fresh-cut items, centrifugation or other procedures are recommended for complete water removal or even slight desiccation of the surface (Cantwell and Suslow 2002). This is done primarily to reduce microbial growth. Desiccation can also induce stress ethylene production in detached vegetables and fruits (Yang 1985).

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D. Disorders 1. Chilling Injury. The visible symptoms of chilling injury (CI) in whole vegetables and fruits vary widely, but typically include surface pitting, watersoaked and discolored flesh, failure to ripen normally, and increased susceptibility to decay (Saltveit and Morris 1990). Chilling sensitive vegetables and fruits that have been processed into fresh-cut products are usually stored at low temperatures that would be expected to cause CI in the whole, intact vegetable or fruit. This is considered necessary to minimize microbial activity and tissue deterioration. In most, but not all (Kim and Klieber 1997), cases the commonly recognized symptoms of CI in whole vegetables and fruits are not observed in freshcut products. It is debatable whether fresh-cut products are actually more chilling tolerant than their intact counterparts or if the visible symptoms of CI are just less likely to be observed. For example, peel pitting that occurs in whole fruit is of no consequence if the fresh-cut product is peeled during processing. One possible explanation for the apparently greater chilling tolerance of fresh-cut products is that their increased perishability leads to the end of shelf life due to microbial activity or tissue senescence prior to the appearance of CI symptoms. In comparing fresh-cut zucchini squash stored at 0, 5, or 10°C, chillinginduced lesions were severe at 0°C and senescence-related browning was moderate to severe at 10°C, thus 5°C was the best storage temperature even though it caused slight to moderate CI (Izumi and Watada 1995). O’Connor-Shaw et al. (1994) similarly recommended a chilling storage temperature of 4°C for fresh-cut honeydew melons because senescencerelated deterioration was much more severe at higher temperatures. Fresh-cut vegetables and fruits are ideally held continuously at low temperature. Since CI symptoms are usually not clearly expressed unless the tissue is transferred to a warm, non-chilling environment (Saltveit and Morris 1990), this may also partly explain the apparently greater tolerance of CI in most fresh-cut products. Furthermore, fresh-cut vegetables and fruits are almost universally handled in MAP. There are many cases for which modified or controlled atmospheres have been shown to alleviate CI in whole products (Forney and Lipton 1990), and this has also been reported for fresh-cut zucchini squash (Izumi et al. 1996) and tomato slices (Hong and Gross 2001). There are also some indications that fresh-cut products are, in fact, subject to CI despite little visual manifestation of injury. For example, the elevated respiration of fresh-cut products compared with the corresponding whole vegetable or fruit may, in some cases and to some

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extent, be an indicator of CI (Kang and Lee 1997). Chilling injury causes membrane damage and solute leakage (Jackman et al. 1989; Todd et al. 1992; Marangoni et al. 1996), and juice leakage or tissue translucency is an important problem during storage of fresh-cut citrus (Baker and Hagenmaier 1997), tomatoes (Artes et al. 1999; Hong and Gross 2000), and melons (Portela and Cantwell 1998, 2001; Bai et al. 2001), all of which are susceptible to CI as intact fruit. Juice leakage can be the limiting factor in storage of fresh-cut watermelons (Durigan et al. 1996). Juice leakage from fresh-cut watermelon cubes was minimal at 3°C, greater at 1°C (presumably due to CI), and increased rapidly at ≥5°C due to accelerated senescence. The increased susceptibility of fresh-cut products to microbial proliferation is usually ascribed to exposure of the inner tissues, which removes the cuticle as a barrier to microbial entry and makes the nutrients present in the tissue available to support microbial growth. However, CI is well known to increase plant tissue susceptibility to microbial infection (Barkai-Golan 2001) and may play an unknown role in the relative microbial stability of whole versus freshcut chilling-sensitive crops. An extremely important (and insidious) consequence of CI is flavor loss due to inhibition of aroma volatile production, which has been shown most clearly for tomato fruit (Kader et al. 1978; Buttery et al. 1987; Maul et al. 2000; Boukobza and Taylor 2002). This is often the first symptom of CI and, in cases of mild chilling exposure, it may be the only symptom. Poor flavor retention by fresh-cut products, especially fruits (Beaulieu and Gorny 2002) is a widely recognized problem. If the choice is between temperatures that may cause some slight CI and temperatures that allow accelerated senescence and microbial growth, then the former is currently preferable (Watada and Qi 1999). However, there may be sufficient expectation that the flavor of fresh-cut products prepared from chilling-sensitive vegetables and fruits could be improved by being handled at non-chilling temperatures to justify efforts to develop supplementary treatments and procedures that allow those products to be handled at higher temperatures. 2. Atmosphere Injury. Fresh-cut vegetables and fruits are almost universally exposed to modified levels of O2 and CO2 in MAP and as a result of coatings. There is always a danger that the products may be exposed to very low O2 or very high CO2 levels, both of which can induce fermentation (Peppelenbos et al. 1996; Peppelenbos and vant Leven 1996). Extreme O2 and CO2 levels decrease cytoplasmic pH and ATP levels and reduce pyruvate dehydrogenase activity, while pyruvate decarboxylase, alcohol dehydrogenase, and lactate dehydrogenase are induced or acti-

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vated. Activation of these enzymes stimulates fermentative metabolism with the accumulation of acetaldehyde, ethanol, ethyl acetate, and/or lactate (Kader and Saltveit 2002). The tolerance of any tissue to low O2 is less as storage temperature increases since O2 requirements for aerobic respiration of the tissue increase with higher temperatures. Depending on the commodity, damage associated with CO2 may either increase or decrease with an increase in temperature. Production of CO2 increases with temperature but its solubility decreases. Thus, the CO2 concentration in the tissue can increase or decrease with an increase in temperature. Further, the physiological effect of CO2 could be temperature dependent. For example, cut snap beans developed CO2 injury in 14 days when exposed to ≥8% CO2 at 1°C, ≥18% CO2 at 4°C, or ≥20% CO2 at 8°C; but no CO2 injury developed even after 21 days in 6% CO2 at 1°C (Costa et al. 1994). While most research studies concerning the tolerance limits of vegetables and fruits to reduced O2 and elevated CO2 levels have been limited to one or the other gas, a combination of low O2 and high CO2, which is the typical situation in MAP, had an additive effect on acetaldehyde and ethanol accumulation in pear (Ke et al. 1994) and avocado (Ke et al. 1995), as well as nectarine and peach (Gorny et al. 1999). Undesirable reduced O2 plus elevated CO2 atmospheres at 2.5°C caused off-flavor and discoloration (“brown stain”) of fresh-cut iceberg lettuce due to ethanolic fermentation and induced phenolic metabolism, respectively (Mateos et al. 1993a); but the CO2 levels that cause brown stain in fresh-cut lettuce (~20%) are, surprisingly, much higher than the level (2%) that causes the same disorder in intact heads (Mateos et al. 1993b). At the same time, 10 to 20% CO2 inhibits phenolic discoloration at the cut edges of fresh-cut lettuce. Because the time for induction of brown stain in fresh-cut lettuce is relatively long (10 to 20 days) compared to shelf life, and because cut-edge browning is a more serious (i.e., rapidly developing) problem than brown stain, commercial fresh-cut lettuce is typically held in MAP designed to develop an atmosphere of about 0.5 to 3% O2 + 10 to 15% CO2 at 0 to 5°C (Gorny 2001). III. SENSORY QUALITY Important considerations in quality of fresh-cut items include a consistent and fresh appearance, acceptable texture, characteristic flavor, and sufficient shelf life to survive the distribution system (Shewfelt 1987; Schlimme 1995; Watada et al. 1996). A number of factors affecting the quality of fresh-cut products are listed in Table 6.3. Enzymatic browning represents a major challenge in fresh-cut products (Kim et al. 1993;

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Table 6.3. Factors affecting the sensory quality and the microbial stability and safety of fresh-cut vegetables and fruits. Sensory quality Processing operations Minimizing damage during processing reduces stress effects Reduces shock to tissues Reduces respiration and ethylene production Reduces browning Washing and sanitizing operations Removes cellular debris and cell contents from cut surfaces May reduce browning Cold water minimizes deterioration Hot water treatment Induces heat shock & redirects cellular energy from wound reactions Reduces browning Temperature management Low temperature during processing and handling minimizes deterioration Reduces respiration and ethylene production Reduces browning Reduces textural changes (softening, toughening) Reduces losses of sugars and organic acids Reduces water loss Chemical application Inhibition of browning (acidulants, reducing agents, cysteine) Maintenance of firmness (calcium salts) Application of edible coatings for manipulation of gas and water vapor movement and as carriers for other chemicals Irradiation Inhibits ripening May negatively affect texture, flavor, and nutritional content May cause browning Packaging Vapor barrier minimizes desiccation, flaccidity Protects product from further damage MAP reduces rate of deterioration Microbial stability and safety Elimination of natural barriers Exposes interior tissues to microbial infection pH of tissue Fruits are low pH (3.5–4.5)—favor molds and yeasts Vegetables are nearer neutral (6.0–6.5)—favor bacteria Temperature Low temperature during processing and handling minimizes microbial growth Fluctuating temperatures favor condensation and microbial growth Ethylene production May directly promote or inhibit microbial growth Enhances tissue senescence and ripening, which reduces tissue resistance to microbial infection

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Wound healing Secondary metabolites can have antimicrobial effects Washing and sanitizing operations Reduce microbial levels on produce and in the environment Elimination of natural microflora may increase risk of human pathogen growth on produce Hot water treatment Destroys microbes on produce surface Chemical application Acidulants lower pH Antimicrobials inhibit growth Edible coatings help retain acidulants and antimicrobials on cut surface Irradiation Destroys vegetative cells of microbes Packaging Barrier to (re)contamination by microbes Condensation in vapor barrier packaging may favor microbial growth MAP may reduce growth and survival of microbes Biocontrol Competition between different microbes Antagonistic reactions

Weller et al. 1997; Sapers and Miller 1998). Textural and flavor deterioration limit fresh-cut shelf life if browning and microbial proliferation are controlled. Factors affecting quality include preharvest growth and cultural factors (Romig 1995), cultivar and maturity at harvest (Yano and Saijo 1987; Kim et al. 1993; Romig 1995; Weller et al. 1995; Beaulieu and Gorny 2002), physiological status of the raw material (Brecht 1995), postharvest handling and storage (Watada et al. 1996), processing technique (Bolin et al. 1977; Garg et al. 1990; Howard et al. 1994; Wright and Kader 1997b), sanitation (Hurst 1995), packaging (Solomos 1994; Cameron et al. 1995), and storage conditions (Lange and Kader 1997a,b; Wright and Kader 1997a), including prior storage conditions of the intact commodity (Gorny et al. 2000), and marketing decisions (Schlimme 1995). Too often, what is considered as quality of intact and fresh-cut vegetables and fruits emphasizes maintenance of appearance, at times sacrificing flavor and texture quality (Sapers et al. 1997; Kader 2002). A. Appearance Oxidative browning is a severe problem that can limit the shelf life and even the development of fresh-cut vegetable and fruit products. The exclusion of O2 or the application of antioxidants can be used to control browning by inhibiting the oxidase reactions. Alternatively, interfering with the wound signal, the synthesis of enzymes of phenolic metabolism,

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or the synthesis of the phenolic compounds themselves will prevent the accumulation of deleterious levels of phenolic compounds and eliminate browning. Being able to predict the browning potential of tissue before processing would help in marketing decisions and in deciding which treatments, packaging, and storage conditions would be needed to maintain maximal quality and shelf life. Measuring the initial levels of enzymes of phenylpropanoid metabolism (e.g., PAL, PPO) or the level of phenolic compounds in these tissues does not give a good indication of their shelf life (Couture et al. 1993). In contrast, these factors measured a few days after wounding are highly correlated with subsequent shelf life. A rapid test that measured inducibility before processing would certainly be preferred over one that measured the induced products a few days after processing. Fresh-cut onions and sweetcorn kernels develop a brown or black discoloration of unknown cause after cooking. This discoloration, which limits the shelf life of these products, increases with longer storage time of the fresh tissue at higher temperature, and is reduced by lowered O2 and/or elevated CO2 (Langerak 1975; Blanchard et al. 1996; Riad and Brecht 2001). Wounding before storage is apparently a prerequisite for after-cooking browning because it does not occur if sweetcorn kernels cut from stored cobs are cooked. Water loss can also negatively affect the appearance of fresh-cut vegetables and fruits, such as the whitening of peeled carrot segments, which is due to drying of cellular remnants on the surface of the tissue (Tatsumi et al. 1991; Cisneros-Zevallos et al. 1995). This phenomenon can also occur on fresh-cut potato, onion, asparagus, and bean pods (Reyes 1996) and can be a serious quality defect because consumers may associate the white blush with decay. The surface debris left on carrots after peeling is held appressed to the tissue and rendered transparent by a thin film of water (Cisneros-Zevallos et al. 1995). As the water evaporates, portions of the abraded cell walls that are still attached to the tissue are released from the surface tension of the aqueous film and refract light to give a whitish “bloom” on the surface. Cutting with very sharp knives reduces the number of cells damaged, removes more cleanly the cut cells, and reduces the appearance of white blush on fresh-cut carrot (Tatsumi et al. 1991), and likely would have a similar effect on other fresh-cut products. B. Texture Textural changes during storage of fresh-cut vegetables and fruits are either ripening- and senescence-related or caused by loss of liquid. Ripening and senescence are associated with changes in cell wall enzy-

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matic activity (Huber 1983; Fischer and Bennett 1991) and changes in pH and levels of chelating agents (MacDougall et al. 1995) that result in such textural changes as flesh softening, cell separation, and increased juiciness. Senescence-related enzymatic changes also may result in toughening as a result of lignification of tissues (Smith et al. 2002). Loss of liquid may be due to either evaporation of water or leakage of juice from the cells, both of which result in soft, flaccid tissue. Ripening and senescence result in increased membrane permeability and leakage of cell contents in overripe and senescent tissues. Juiciness of ripe fruits is distinct from juice leakage, being a sensory experience related to cell size and cell wall thickness and how easily the cells are broken and release their contents upon eating (Szczesniak and Ilker 1988). Juice leakage of fresh-cut tropical and subtropical vegetables and fruits may also be a manifestation of CI (see Section II.D.1, above). C. Taste and Aroma Flavor quality of fresh-cut vegetables and fruits is critical to their acceptance and appreciation by consumers. Sensory attributes such as sweetness and characteristic aroma may be the most important indicators of shelf life from the consumer’s point of view. Taste and aroma together make up flavor, which contributes to the recognizable nature of a food. Taste refers to detection of nonvolatile compounds on the tongue while aroma is related to volatile compounds detected in the nose. These two aspects of flavor are inextricably linked, as it has been shown that perception of aroma can be influenced by levels of taste components, and vice versa (Beaulieu and Baldwin 2002). The challenge in fresh-cut vegetable and fruit handling is to maintain the taste and aroma attributes of the original whole product. It is presently not practical to test for sensory quality during storage and handling, which makes initial maturity and quality standards that affect taste and aroma extremely important in any attempt to ensure good flavor shelf life (Beaulieu and Gorny 2002). 1. Soluble Sugars and Organic Acids. Depletion of carbohydrate reserves as a result of stimulated (i.e., wound-induced) respiration rate can lower the organoleptic quality of some fresh-cut commodities like melons whose quality is highly dependent on sugar content, or those with naturally low levels of sugars and reserve carbohydrates (e.g., starch). In contrast to apple and banana fruit that convert large amounts of starch to sugars as they ripen, melon and tomato fruit have very limited capacity to replenish soluble sugars lost to accelerated respiration during storage or ripening. Organic acids are another major respiratory substrate

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and increased tissue pH in fresh-cut apples has been ascribed to utilization of organic acids in respiration (Kim et al. 1993). Depletion of acids can have negative organoleptic effects in fruits like apple, peach, and mango for which the balance of sweetness (sugars) and tartness (acids) is an important flavor attribute. 2. Aroma Volatiles. Aroma volatiles may be synthesized during the normal course of vegetable or fruit development, as with the increased aroma intensity that develops during fruit ripening. These include a vast array of alcohols, aldehydes, esters, ketones, lactones, and other compounds (Baldwin 2002). Little is known about what effect different storage temperatures and atmospheres have on normal aroma volatile production in fresh-cut vegetables or fruits other than the inhibition that occurs as a consequence of CI (Buttery et al. 1987; Maul et al. 2000) previously mentioned. Other aroma volatiles are short-lived compounds that are synthesized only upon disruption of tissue. Increased LOX activity is a common feature of plant senescence (Siedow 1991) and its action on membrane lipid degradation products that form upon maceration of tissue results in characteristic, but evanescent, aroma compounds in a number of vegetables and fruits (Gardner 1989). Other aroma compounds are released from glucosides and glucosinolates as well as other bound forms (Baldwin 2002). The persistence (or lack thereof) of these aroma compounds in fresh-cut products should be of concern. It is well known among researchers and processors that fresh-cut fruit taste becomes bland during the course of extended storage. It has recently been suggested that bruising has a similar effect on whole tomato flavor due to wound-induced disruption of biosynthetic pathways for aroma volatiles, leading to premature synthesis (and loss) of these compounds (Moretti et al. 2002). Interestingly, there is potential to design edible coatings (see below) to retain volatile flavor compounds within the tissue (Miller and Krochta 1997; Baldwin et al. 1998), which could address one of the most intractable problems with fresh-cut fruit. Recently, a great deal of interest has developed in the potential use of electronic nose technology, which uses multiple sensor arrays to create volatile “fingerprints,” for quality control in the food industry (Bartlett et al. 1997; Giese 2000). Electronic noses have been used to compare volatile characteristics or evaluate changes in volatiles during storage of several types of juices and fresh vegetables and fruits (Demir 2002). Maul et al. (1998, 2000) used an electronic nose to nondestructively identify and classify ripe tomatoes that had been harvested at different maturity stages and exposed to different postharvest temperatures. Riva et al. (2001) correlated electronic nose response with the degree of fresh-

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ness of fresh-cut chicory and shredded carrots in terms of color and microbial spoilage. They used principal component analysis and found that the first principal component was correlated to microbial population and color index, indicating that the electronic nose could potentially substitute for those measures.

IV. PHYTONUTRIENTS Appreciable epidemiological evidence exists to suggest that regular consumption of vegetables and fruits has long-term health benefits and may reduce the risk of cancer and chronic diseases such as coronary heart disease. A variety of phytochemical compounds such as polyphenolics, vitamin C, vitamin E, β-carotene, and other carotenoids are reported as functional antimutagens, anticarcinogens, and inhibitors of chemically induced cancers; these phytochemicals are referred to as “antioxidant vitamins,” even though β-carotene is actually a provitamin A compound (Elliott 1999). Most of these compounds are known to inhibit cellular and DNA damage caused by reactive oxygen species and free radicals that may lead to degenerative diseases. Vegetables and fruits are the primary source of these antioxidant compounds in our diet and fresh-cut operations serving to retain maximal bioactivity are important considerations affecting processing, packaging, and storage. Current investigations into the fresh-cut industry have demonstrated that concentrations of vitamins, minerals, and other phytochemical compounds are reduced following fresh-cut operations and are affected by conditions of handling, packaging, and storage. Nutrient losses are generally accelerated following tissue wounding (Klein 1987) but stress associated with processing may also initiate biosynthesis of numerous compounds that affect antioxidant content and product quality. The synthesis of wound ethylene after fresh-cut operations can stimulate a diversity of physiological responses, including loss of vitamin C and chlorophyll and induction of polyphenolic metabolism (Kader 1985; Saltveit 1999; Tudela et al. 2002a,b). Current recommendations from The American Cancer Society encourage consumption of five or more daily servings of vegetables and fruits to maintain optimum human health and the convenience of fresh-cut foods is a complement to this program. Growing evidence suggests that increasing dietary consumption of vegetables and fruits has long-term health benefits, and may prevent or reduce the risk of many chronic diseases. Much of the evidence relating to the benefits of fruit and vegetable consumption is based on epidemiological studies that show strong

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correlations between the delay or suppression of degenerative diseases and consumption rates (Ziegler 1991; Gershoff 1993; Block and Langseth 1994; Steinmetz and Potter 1996; van Poppel and van den Berg 1997). Phytochemicals present in a plant-based diet can act as reducing agents, free radical scavengers/terminators, metal chelators, and quenchers of reactive oxygen species (ROS), and can modulate the effects of various antioxidant enzymes in the body (Ho 1992; Okuda 1993). However, a major concern with fresh-cut operations is the potential for significant loss of phytonutrients and other antioxidant compounds from enzymatic and non-enzymatic oxidation reactions that occur at cut surfaces or during storage. Upon cellular disruption, action from various peroxidases, LOX, and PPO can lower nutritional quality, while generation of ROS can destroy phytonutrients under normal storage conditions. A. Fresh-cut Effects on Phytonutrients 1. Carotenoids. Carotenoids are important compounds in vegetables and fruits because of their excellent antioxidant properties and the diversity of color they provide. The distribution and concentration of carotenoids obviously varies among commodities but varietal differences must also be considered (Sood et al. 1993; Mercadante and Rodriguez-Amaya 1998; Abushita et al. 2000; Holley et al. 2000; Leonardi et al. 2000), making it difficult for fresh-cut processors to deliver a consistent product with uniform color and nutrient content. Our daily intake of carotenoids is primarily from vegetables and fruits (Goddard and Matthews 1979) and the six most important compounds imparting oxidative protection include α-carotene, β-carotene, lutein, lycopene, zeaxanthin, and β-cryptoxanthin (VERIS 2000). Carotenoids may be classified as having provitamin A activity (β-carotene, αcarotene, and β-cryptoxanthin) or as oxygenated xanthophylls that have no vitamin A activity (Levy et al. 1995) but are potent antioxidants that may help prevent age-related macular degeneration and cataracts (Seddon et al. 1994; Matsufuji et al. 1998). Epidemiological studies have indicated the role of carotenoids and other antioxidant compounds in the prevention of numerous chronic diseases, including certain types of cancer, cardiovascular disease, stroke, and cataracts (Gaziano and Hennekens 1993; Block and Langseth 1994; Steinmetz and Potter 1996; van Poppel and van den Berg 1997) and they are essential for normal growth, reproduction, and resistance to infection (Tee 1992). Due to their role as antioxidant compounds, as well as the color characteristics they impart to vegetables and fruits, exploration of techniques to retain carotenoids is vital for nutritional and sensory quality characteristics.

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Carotenoids are mostly responsible for the diversity of colors found in vegetables and fruits that range from yellow to orange and red depending on the commodity and their concentration, and carotenoid retention during fresh-cut operations is the subject of numerous investigations. Carotenoids are synthesized via the mevalonic acid pathway in vegetables and fruits with concentrations generally increasing with maturity. Carotenoids have a diverse role in the biological functioning of plants and humans and possess provitamin A and antioxidant activity, modulate detoxifying enzymes, regulate gene expression, aid in cellular communication, and augment immune functions (Clevidence et al. 2000). Carotenoid pigments are relatively stable in their natural environment but become more labile when subjected to postharvest treatments or processing operations (Rigal et al. 2000) due to oxidative damage resulting from their high degree of unsaturation that is also responsible for color and antioxidant properties. Concentrations are typically static in nonclimacteric crops following harvest, leading to investigations focusing on maintaining these levels during handling and storage. Cultivar evaluations and means to prevent loss during fresh-cut operations will influence overall antioxidant levels and provide maximum provitamin A activity upon consumption (Heinonen 1990; Rao et al. 1998). Carotenoids are generally unstable under acidic conditions, with destruction accentuated in the presence of light, enzymes, oxygen, metal catalysts, and low water activity (Dorantes-Alvarez and Chiralt 2000). Disruption of plant tissues by mechanical means or during senescence can also lead to rapid destruction of carotenoids through the action of oxidase enzymes, and may be prevented by the use of reducing agents or modified atmospheres (MA) (Simpson et al. 1976; Biacs and Daood 2000). 2. Ascorbic Acid. Ascorbic acid is a water-soluble antioxidant long associated with inhibition of oxidative reactions and is a key marker compound for determining the extent of oxidation in fresh-cut vegetables and fruits (Barth et al. 1993). With anti-scorbutic properties, ascorbic acid can enhance the absorption of non-heme iron and may protect against oxidative or stress-related diseases and degeneration associated with aging, such as coronary heart disease, cataract formation, and certain cancers (Gershoff 1993; Sauberlich 1994). Levels of L-ascorbic acid do not always relate to actual vitamin C content since dehydroascorbic acid also has vitamin C activity and is utilized by the body in a similar manner (Petersen and Berends 1993; Lee and Kader 2000). Ascorbic acid is easily destroyed during fresh-cut operations and levels are affected by cutting technique (Barry-Ryan and O’Beirne 1999), gas

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composition (Gil et al. 1998b, 1999), package design (Barth and Zhuang 1996), water loss and storage time/temperature (Nunes et al. 1998; Lee and Kader 2000), light intensity, heat, O2, oxidase enzymes, and prooxidant metals (Albrecht et al. 1991; Lee and Kader 2000). 3. Polyphenolics. Polyphenolics are a major category of antioxidant compounds present in vegetables and fruits that encompass thousands of individual compounds in various commodities and concentrations. Polyphenolics are generally classified into distinct groups based on structural or functional characteristics (Rice-Evans et al. 1996) that uniquely distinguish each, and their effectiveness as antioxidants is generally dependent on the number and location of hydroxy groups. Of these, flavonoids are the most diverse class, encompassing anthocyanins, flavonols, flavones, flavonones, flavan-3-ols, and biflavans, and are known for their excellent antioxidant activity. Other major polyphenolics include hydroxycinnamic and hydroxybenzoic acids, both derived primarily from the phenylpropanoid pathway, and tannins, which are polymers of flavonoids or phenolic acids. Epidemiological data has suggested a role of certain polyphenolics in prevention of carcinogenesis by reducing oxidant formation, scavenging free radicals, decreasing reaction intermediates, or inducing oxidative repair systems. Phenolic compounds are known to possess antimicrobial, antioxidant, and oxidase inhibiting properties that vary with structure and solubility of each compound (Sichel et al. 1991; Tereschuk et al. 1997; Kujumgeiv et al. 1999; Palma et al. 1999; Kabuki et al. 2000; Rauha et al. 2000). Most vegetables and fruits contain at least moderate levels of both neutral (flavonoids) and acidic polyphenolics that play a significant role in reducing chronic and degenerative diseases (Hertog et al. 1993; Keli et al. 1996; Knekt et al. 1996, 1997; Garcia-Closas et al. 1998). Specifically, flavonoids have been studied in detail in both biomedical and agricultural applications due to their diverse effect in a variety of systems. Flavonoids are potent antioxidants and inhibitors of ROS (Sorat et al. 1982; Robak and Gryglewski 1988; de Whalley et al. 1990), can inhibit oxidoreductase enzymes (Laughton et al. 1991; Bruyne et al. 1999; Casella et al. 1999; Schubert et al. 1999; Shimizu et al. 2000), and modulate immune and inflammatory cell functions (Decharneux et al. 1992), and are therefore important components to be retained in fresh-cut products. Polyphenolics, along with carotenoids and ascorbic acid, constitute a significant portion of the overall antioxidant capacity of vegetables and fruits; therefore their retention in fresh-cuts is critical for optimal human health. Recent findings have increased the interest in polyphenolic com-

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pounds present in fresh and fresh-cut vegetables and fruits due to their elevated antioxidant capacity. Polyphenolics, especially anthocyanins, were found to be major contributors to antioxidant capacity in various vegetables and fruits (Cao et al. 1996; Wang et al. 1996, 1997; Prior et al. 1998; Kalt et al. 1999; Chang et al. 2000; Ehlenfeldt and Prior 2001). Polyphenolics were shown to be more effective than carotenoids in inhibiting in vitro oxidation (Chang et al. 2000), but often these systems are complex, containing a diversity of compounds contributing to overall antioxidant status (Velioglu et al. 1998), and the role of an individual compound is often difficult to identify. 4. Secondary Metabolites. Many vegetables and fruits have adapted defense mechanisms in the form of phytoalexins to confer additional physical and chemical barriers as a response to stress conditions. These compounds are classified as secondary metabolites and usually consist of low molecular weight proteins and phenolic compounds. Plants can synthesize a diverse array of these compounds pre- or postharvest in response to stresses such as wounding, wound healing, ethylene exposure, or attack by microorganisms and other pests (Babic et al. 1993a,b; Dixon and Paiva 1995; Toivonen 1997). The complement of secondary compounds formed is dependent on the species of plant, the tissue involved, and the extent of the stress factor. The various compounds that can be produced in wounded vegetables and fruits include hydroxycinnamic and hydroxybenzoic acids, polyketides, flavonoids, terpenoids, alkaloids, tannins, glucosinolates, long-chain fatty acids, and various alcohols (Miller 1992), most serving in plant-defense roles against fungal and bacterial decay. In many cases, these compounds significantly affect aroma, taste, appearance, nutritive value, or safety of fresh-cut products. Fortunately, some aroma and taste compounds may persist for relatively short periods of time, but others persist throughout the shelf life of the commodity, resulting in poor sensory characteristics compared to fresh. Minimizing many of these stress factors during fresh-cut operations can improve shelf life stability and help retain greater concentrations of available phytonutrients. Several studies have reported the loss, biosynthesis, and metabolic turnover of polyphenolic compounds following the physiological stress associated with fresh-cut operations. Hydroxycinnamic or hydroxybenzoic acid derivatives were significantly altered in irradiated potatoes (Ramamurthy et al. 1992) and shredded carrots (Babic et al. 1993a,b), with polyphenolic compounds reaching maximum concentration shortly after the initial stress, followed by decreases during storage. Such losses may be the result of further metabolism or from enzymatic

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and non-enzymatic condensation reactions. Increases in cinnamic acid derivatives were also observed in colorless midribs of red lettuce, but a corresponding increase was not observed in the polyphenolic-rich red and green leaf sections, indicating localized phenolic biosynthesis influenced by initial polyphenolic content (Ferreres et al. 1997). Cinnamic acid derivatives are often among the first compounds to be synthesized when vegetables and fruits are stressed. Enzymatically regulated by PAL (Howard et al. 1994; Lopez-Galvez et al. 1996b; Saltveit 2000), rapid accumulation of polyphenolic compounds such as chlorogenic, isochlorogenic, caffeic, and hydroxybenzoic acids can occur. Although these compounds are known as effective antioxidants, their effect on overall nutritional quality is unknown and their increase may be generally undesirable since many are excellent substrates for oxidative enzymes. However, determining the benefits of de novo polyphenolic synthesis as a result of tissue wounding may be an important factor in protecting other phytonutrients from oxidative reaction.

B. Prevention of Nutrient Loss 1. Physicochemical Treatments. It is generally accepted that fresh-cut operations and storage are conducive to the destruction of phytochemical compounds through enzymatic and autooxidative reactions. However, the magnitude of nutritional change is highly dependent on the commodity, severity of wounding, atmospheric composition, and postprocessing storage conditions. Proper temperature control is among the most critical factors influencing nutrient retention in fresh-cut vegetables and fruits, as most enzymatic and oxidative reactions occur more rapidly at elevated storage temperatures. Temperature control serves to reduce microbial populations and slow chemical reactions that affect sensory characteristics and phytochemical concentrations, and should be factored into all techniques designed to retain phytonutrients in fresh-cut vegetables and fruits. In previous reviews, the nutritional content was believed to decrease in fresh-cut as compared with intact vegetables and fruits, especially levels of vitamin C (Klein 1987; McCarthy and Matthews 1994). Following tissue wounding and exposure to light and air, antioxidant phytochemicals may be lost to enzymatic and oxidative action at the site of cellular disruption, in secondary or coupled oxidation reactions with lipids, in reactions with wound ethylene, from exposure to chlorinated sanitizers, or from mild desiccation (Barth et al. 1990; Park and Lee 1995; Wright and Kader 1997a,b; Nunes et al. 1998). Therefore, developing postharvest treatments to alleviate phytonutrient

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loss following fresh-cut operations is vital to insure that maximum levels of phytonutrients reach the consumer. Various physical and chemical treatments have been investigated in fresh-cut vegetables and fruits as means to maintain fresh-like characteristics and nutritional quality. Mild heat treatments or surface acidification have been used as means to inhibit oxidative enzymes and serve to protect some nutrient compounds, as long as a high water-activity is maintained (Dorantes-Alvarez and Chiralt 2000). Maintaining a high RH during storage was shown to be effective in retaining antioxidant compounds (Jiang and Fu 1999). Ascorbic acid is commonly applied to cut surfaces through edible coatings or dips to prevent browning on cut surfaces: Acting both as an acidulant and a reducing agent, ascorbic acid can reduce quinones back to normal phenolic compounds. Combinations of reducing agents and acids were effective in prevention of surface browning and retention of sugars and organic acids in fresh-cut apples (Buta et al. 1999) and their effect may be enhanced when combined with additional preservation techniques such as MAP or proper temperature control. 2. Modified Atmospheres. The use of MAP is an effective means to reduce enzymatic and autooxidative reactions affecting phytonutrients in fresh-cut vegetables and fruits by reducing concentrations of O2 and increasing CO2. Modified atmospheres were used to maintain higher levels of provitamin A and vitamin C in fresh-cut broccoli (Barth et al. 1993; Barth and Zhuang 1996; Paradis et al. 1996) and jalapeno peppers (Howard and Hernandez-Brenes 1998), but had little effect on provitamin A concentrations in peach and persimmon slices (Wright and Kader 1997a) and was ineffective in ascorbic acid retention in sliced strawberry or persimmon (Wright and Kader 1997b). Extreme CO2 concentrations (>20%) may actually cause greater degradation or suppressed synthesis of vitamin C (Wang 1983; Agar et al. 1997; Tudela et al. 2002b) and anthocyanins (Gil et al. 1997; Holcroft et al. 1998; Holcroft and Kader 1999; Tudela et al. 2002a), while certain CO2 levels may induce biosynthesis of provitamin A carotenoids (Weichmann 1986). Modified atmospheres did not affect flavonoid content of Swiss chard and significantly reduced levels of ascorbic acid (Gil et al. 1998b), while flushing packages of fresh-cut lettuce with 100% N2 retained higher ascorbic acid concentrations than passive MAP and air controls (Barry-Ryan and O’Beirne 1999). In fresh-cut spinach, flavonoid content remained constant during storage in air or MAP, but spinach in MAP contained higher dehydroascorbic acid concentrations that resulted in lower antioxidant activity compared with air-stored spinach (Gil et al. 1999). However, decreases in flavonoids were observed in ‘Lollo Rosso’ lettuce stored in

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MAP (Gil et al. 1998a), further indicating a commodity-specific role of gas composition on overall phytonutrient retention. 3. Edible Coatings and Dips. The application of food-grade compounds into wash water or on the surface of fresh-cut vegetables and fruits as coatings has an advantage of producing immediate benefits at the active site of phytonutrient deterioration. The benefits of these edible coatings include decreased respiration rate, browning inhibition, and retention of various quality factors by creating a barrier to O2, which influences enzymatic and nonenzymatic oxidation rates (Li and Barth 1998). And although the effect of edible coatings on intact vegetables and fruits has been well studied, efficacy for phytonutrient retention in fresh-cut products has not been extensively investigated. Vitamin A, vitamin C, and polyphenolic retention in fresh-cut vegetables and fruits during handling and storage are known for only a few products, and limited information is available on changes in overall antioxidant activity. With increasing demand for fresh and fresh-cut vegetables and fruits, a need exists for accurate assessment of biologically active components and their changes following packaging and storage. Edible coatings are a common method used to extend the fresh-like appearance and quality characteristics of many vegetables and fruits (Baldwin et al. 1995a,b, 1996). Fresh-cut carrots with cellulose-based edible coatings retained greater provitamin A levels during storage in one study (Li and Barth 1998) but another coating had no effect (Howard and Dewi 1996). Coatings are generally used as a barrier to O2 movement but can also serve as a carrier for chemicals that improve oxidative stability or inhibit oxidase enzymes. Little or no evidence exists on the efficacy of naturally occurring or isolated phytochemicals incorporated into an edible coating for retention of native antioxidants in any fresh-cut product, but the use of organic acids, ascorbic acid, or related compounds is most common. Important considerations for phytochemical retention include control of oxidoreductase enzymes, pro-oxidant metals, and reactive oxygen species that can be partially controlled using edible coatings. Fresh-cut operations serve to disrupt cellular membranes, decompartmentalizing enzyme/substrate systems (Rolle and Chism 1987) and leading to oxidative deterioration (Kader and Ben-Yehoshua 2000) or accumulation of secondary metabolites (Talcott and Howard 1999), the effects of which may be slowed by the use of edible coatings. Application of edible coatings to fresh-cut vegetables and fruits should be tailored to chemical composition, processing, and packing techniques employed for a particular commodity, and future efforts should concentrate on resultant color, flavor, and antioxidant properties throughout storage.

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V. MICROBIOLOGY Microbial contamination and growth on or in fresh-cut vegetables and fruits is a major concern for the industry (Nguyen-the and Carlin 1994; Hurst 1995; Beuchat 1996; Fain 1996; Zink 1997; Francis et al. 1999). The growth of microorganisms is facilitated by plant cell injury, senescence, or stress. Cells injured during fresh-cut production release fluids containing compounds that microbes can use for nutrition (King and Bolin 1989). The amount of injury during cutting processes is related to the potential for growth of microorganisms in the product (Heard 1999). Stressed or senescent tissues have leaky membranes, which allow diffusion of small molecular weight compounds and water into intercellular spaces and wound surfaces (Salveit 2002). These conditions provide ideal conditions for microbial growth. Certain human pathogens also can grow or survive in fresh-cut vegetables and fruits. These microbes ordinarily have no direct effect on the life of the product, but their presence renders the fresh-cut product unwholesome and, as a result, eliminates further shelf life considerations. Microorganisms are natural inhabitants of plants either as epiphytes living on the surfaces of plants or as endophytes existing inside plant tissues. Epiphytes are not uniformly or randomly distributed over leaf surfaces. They are most commonly found in areas protected from physical stress such as at the base of trichomes, in depressions over the adjacent walls of epidermal cells, and in open or closed flower buds (Leben 1965; Hirano and Upper 1983). Endophytes arise either through penetration of roots and movement up xylem vessels or entrance into intercellular spaces or xylem through wounds or water-congested openings in the plant surface (e.g., hydathodes, stomata, lenticels, etc.). Crops can also become contaminated with microflora from plant debris, soil, contaminated equipment, or harvest crews. Plant debris or soil are likely to harbor decay pathogens, whereas certain human pathogens could be dispersed by contaminated water, harvest crews, certain animals, birds, and equipment (Brackett 1994; Bartz and Wei 2002). Epiphytes are commonly embedded in biofilms, which helps them resist erosion by rainfall (Manceau and Kasempour 2002; Morris et al. 2002). The biofilms can be composed of many different bacteria as well as yeasts and, perhaps, filamentous fungi. Biofilm morphology may include microcolonies, surrounded by “water channels.” The film itself is usually composed of polysaccharides. Biofilms can also develop on wet inert surfaces such as fresh-cut processing line equipment (Frank 2001). Bacteria embedded on plants as microcolonies often disperse as aggregates in wash water. As such, dilution plate analysis of bacterial

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density in wash water would likely underestimate the true number of bacteria present. This phenomenon may explain situations in which higher numbers of bacteria on a fresh-weight basis are detected on freshcut products as compared with the raw material (Heard 1999). Except where the cutting machinery is grossly contaminated by biofilms and microorganisms, it seems more likely that the cutting process disperses at least a portion of the bacterial aggregates found on plant surfaces. Microorganisms located in plant tissues (endophytes) are protected from desiccation, wide swings in temperature, and UV radiation (Manceau and Kasempour 2002). However, to survive, endophytes must not stimulate defense reactions by the plant such as occur when pathogens start colonizing host tissues. For example, treatment with methyl jasmonate extended the shelf life and reduced the microbial load on fresh-cut celery and peppers (Buta and Moline, 1998). Arguably, this observation supports the theory that the general population of microbes associated with fresh-cuts are sensitive to host resistance responses. On the other hand, such microbes apparently do not themselves stimulate plant resistance responses since microbe growth is not affected unless the tissues are amended with an intermediate in the host resistance response. Alternatively, the methyl jasmonate treatment may delay senescence and only indirectly inhibit microbe growth through limiting the diffusion of nutrients to the endophytes. Prior to harvest, plants are covered with a continuous coating of waxy materials, specialized appendages, or cells differentiated into corky layers. This coating protects plant cells from desiccation, exposure to damaging UV radiation, and attack by microbes. The act of cutting plant tissues produces an immediate breach in the protective layer. Additionally, passage of a knife through plant tissues can drag bacteria into damaged cells (Lin and Wei 1997). Cell sap is released from cut cells and floods adjacent intercellular spaces. Bacteria, either as cells or in aqueous suspension, that contact the cell sap become suspended and move in the flooded intercellular spaces to positions that are protected from surface treatments: Within 5 seconds of application to a cut surface, cells of E. c. carotovora became located in sites within tomato fruit tissue that could not be successfully disinfected with 100 ppm chlorine at pH 6.0 (Bartz et al. 2001). Rigorous sanitation of preparation areas reduces the level of microbial contamination, while chemical treatments and low temperatures restrict microbial growth during storage and marketing. Although chlorine and other sanitizers may be quite effective for inactivating microbes in clean solutions and on inorganic surfaces, their ability to remove microbes that

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are on vegetables or fruits is quite limited (Bartz and Tamplin 2002). In addition, if processing equipment is not rigorously and continuously sanitized, biofilms can easily develop (Frank 2001; Momba and Binda 2002; Peng et al. 2002). Biofilm formation is inhibited on hydrophobic surfaces and at low temperatures (Chavant et al. 2002). Electropolished stainless steel has been shown to resist biofilm formation better than stainless steel with other finishing treatments (Arnold et al. 2001). Factors that influence microbial growth on fresh-cut products include temperature, RH, and gas composition of the environment (Omary et al. 1993; Babic and Watada 1996), as well as the pH and composition of the product (Breidt and Fleming 1997). Maintenance of low temperature is the single most important factor both for inhibiting microbial growth (Heard 1999) and delaying tissue senescence. Table 6.3 lists many of the factors affecting microbial stability and safety of fresh-cut products. Since fresh-cut products are (ideally) held at refrigeration temperatures, psychrotropic microorganisms that are able to grow at low temperatures (0 to 10°C) are of the most concern. Fortunately, most human pathogens are mesophiles associated with warm-blooded animals and grow slowly or not at all at such low temperatures. A notable exception to this generalization, however, exists in the case of the human pathogen Listeria monocytogenes, that has been shown to grow on some, but not all, vegetables at temperatures as low as 4 to 5°C, albeit slowly (Heard 1999; Bartz and Wei 2002). Modified atmosphere storage affects both plant physiology and microbial growth. Most postharvest plant pathogens are aerobes and have only limited ability to infect plant tissues when O2 is limited. However, the extreme levels of O2 or CO2 that directly stop microbe growth often also injure plant tissues. As these gases approach injurious levels, host respiration is greatly reduced, which slows ripening and senescence, thereby preserving the natural resistance of juvenile tissues to microbial attack. Still, there has been concern that MAP may create conditions that favor growth of anaerobic or microaerophilic microbes with human health implications, especially under temperature abuse conditions. However, a number of studies have shown that fresh-cut vegetable products are inedible by the time microbial populations have risen to dangerous levels (Zagory 1999). For example, samples of fresh-cut Romaine lettuce and shredded cabbage inoculated with Clostridium botulinum spores were judged to be inedible by the time they became toxin positive (Petran et al. 1995). In contrast, use of an inappropriate film covering allowed not only C. botulinum spores on mushrooms to germinate but also the resulting cells to produce toxin (Brackett 1994).

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A. Decay The growth of certain bacteria or fungi directly limits the life of freshcut vegetables and fruits by causing changes in the appearance and/or texture of the products that make them inedible. Common microbes directly limiting shelf life include pectolytic species or strains of the bacteria Pseudomonas, Erwinia, Bacillus, Cytophaga, and Clostridium spp. (Bartz and Wei 2002); fungi belonging to species of Fusarium, Alternaria, Mucor, Rhizopus, Colletotrichum, Stemphyllium, Botrytis, Sclerotinia, Sclerotium, Geotrichum, Penicillium, Aspergillus, and Phoma; and Oomycota (Kingdom Chromista) belonging to Phytophthora and Pythium (Korsten and Wehner 2002). The lactic acid bacteria, Lactobacillus and Leuconostoc spp., are found on vegetables subject to brine pickling as well as many salad vegetables (Heard 1999). Decays are caused by lactic acid bacteria (Bartz and Wei 2002) or the lactic acid producing fungi, Geotrichum candidum (Korsten and Wehner 2002) or G. citri-aurantii (Farr et al. 1989). The lactic acid bacteria appear more active in microaerophilic environments such as where container surfaces directly contact cut surfaces. Leuconostoc mesenteroides can produce thick slime (King and Bolin 1989). Many of the relatively firm, lactic acid decays have been attributed to Geotrichum spp. because of the failure of investigators to isolate lactic acid producing bacteria (Bartz and Wei 2002). Such bacteria are relatively fastidious and require a special medium for culture. In general, bacteria and certain fungi cause decays in vegetables, including “fruit vegetables,” whereas fungi cause most of the decays in fruits. The major reasons for the separation between classes of microbes and plant host are not only the low pH of true fruits, but also the quantity and nature of the acidulants responsible for the low pH. Certain microbes indirectly reduce the shelf life of fresh-cut vegetables and fruits through production of off flavors, slimes, cloudy plant juices, or discoloration. These bacteria and fungi do not produce pectolytic enzymes or lactic acid. As such, they cannot cause tissue maceration or rapid cell death. Examples of this group include both pigmented bacteria as well as bacteria that produce pigments, Serratia marcesens, Xanthomonas spp., Pseudomonas chloraphis, P. fluorescens, Pantoea herbicola (Bartz and Wei 2002; Robbs et al. 1996). Additionally, certain saprophytic bacteria (Klebsiella spp. and Enterobacter agglomerans) are capable of causing discoloration in salad vegetables such as fresh-cut celery (Robbs et al. 1996). Zagory (1999) recently argued that the physiological deterioration of fresh-cut fruits and vegetables leads to microbial proliferation rather than the “conventional wisdom” of

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general microbial growth being responsible for deterioration. However, there may be a distinction between fresh-cut vegetables and fruits in this regard since low initial microbial (especially yeast and mold) counts do, in fact, correlate well with increased fresh-cut fruit shelf life (O’ConnorShaw et al. 1994; Qi et al. 1999). B. Food Safety Safety must be of primary concern in any food product. A major consideration in terms of fresh-cut safety has been identified as inoculation of the nutrient-rich flesh of vegetables and fruits with human pathogens from the surface tissues, which are less conducive to microbial growth and development than internal tissues. The presence of human pathogens is of particular concern with fresh-cut products because they are almost always consumed raw (i.e., without a heat treatment). In addition, it has been suggested that the elimination of spoilage microbes without elimination of human pathogens may extend shelf life of a fresh-cut product to the point that safety is compromised because the human pathogens may be more likely to proliferate (Hintlian and Hotchkiss 1986; Brackett 1994). There has been a remarkable safety record associated with fresh, intact produce (Beuchat 1996). Nevertheless, it has been established that C. botulinum can grow on Romaine lettuce and shredded cabbage in pouches (Petran et al. 1995), and Escherichia coli O157:H7 on fresh-cut apple tissue (Janisiewicz et al. 1999), while L. monocytogenes has been cultured on apple slices (Conway et al. 2000) and several fresh-cut vegetables (Zhang and Farber 1996; Babic et al. 1997; Farber et al. 1998; Juneja et al. 1998). When vegetables or fruits were co-inoculated with either bacterial (Erwinia carotovora) or fungal (Botrytis cinerea or Rhizopus stolonifer) plant pathogens, and a human pathogen, Salmonella typhimurium, the Salmonella grew significantly faster than when it was the only inoculum, suggesting potential synergism between plant and human pathogens (Wells and Butterfield 1997, 1999). However, there was no apparent synergism between S. typhimurium and the fungal plant pathogens Alternaria alternata or Geotrichum candidum (Wells and Butterfield 1999). Similarly, populations of L. monocytogenes continually increased on apple slices decayed by Glomerella cingulata, in which the tissue pH increased from pH 4.7 to 7.0, but did not survive on tissue decayed by Penicillium expansum, in which the pH of the decayed area declined from pH 4.7 to 3.7 (Conway et al. 2000). Additionally, Babic et al. (1997) reported that L. monocytogenes growth on fresh-cut spinach was restricted by the presence of native microflora.

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In the past ten years, outbreaks due to foodborne pathogens on fresh produce have risen to a level of unacceptable risk for consumers and producers (Altekruse et al. 1997). Between 1973 and 1988, the Centers for Disease Control and Prevention (CDC) found that 2% of outbreaks were attributed to produce. By 1991, this percentage had increased to 5% (Tauxe et al. 1997; Olsen et al. 2000). The increase in foodborne illness in industrialized countries, such as the United States, has been associated with dietary changes and the increased importation of produce (Altekruse et al. 1997). Domestically, both consumers and retail establishments have become accustomed to the ease of using fresh-cut produce in the home and restaurant settings. Any raw material with surface contamination may allow transference to the inner flesh of the fruits and vegetables during cutting and processing (Lin and Wei 1997). Unknowing consumers could be purchasing produce that, in appearance, is free of pathogens. In response to an emerging public health concern, the National Integrated Food Safety Initiative (NIFSI) was established in 1997 (USDA 1999). The NIFSI budget was finalized in 2000. The purpose of the new resources was to improve, coordinate, and target important areas of the food trail from farms to retail. One of the most important aspects of NIFSI was the increased surveillance of foodborne illness and outbreaks (USDA 1999). Nontyphoidal salmonellosis is noted for being the most commonly reported foodborne infection in the United States, with Campylobacter having the highest estimated total number of cases (Altekruse et al. 1997; Bean et al. 1997; Mead et al. 1999). As of 1996, the genus Salmonella had at least 2,400 known serovars, and many more are still to be discovered (Robinson et al. 2000). Birds and animals are common reservoirs of Salmonella; however, there are several serovars in humans capable of causing disease and these have been associated with several outbreaks. Garcia-Villanova Ruiz et al. (1987) analyzed 345 samples of vegetables between 1981 and 1983 from farms, wholesale markets, supermarkets, and small shops in Spain for Salmonella spp. Artichoke, beet leaves, celery, cardoon, cabbage, cauliflower, lettuce, parsley, and spinach had detectable levels of Salmonella. An outbreak of Salmonella saphra in the spring of 1997 was traced to cantaloupes imported from Mexico resulting in 24 cases of illness (Boetani-Mohle et al. 1999). Salmonella has also been implicated in several domestic outbreaks involving fresh fruits and vegetables (Beuchat 1996). Most recently, there have been outbreaks associated with watermelons and cantaloupes (CDC 1979; Blostein 1991; CDC 1991). Salmonella oranienburg and S.

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javiana were implicated in an outbreak resulting from consumption of watermelons. While in June and July of 1991, there were more than 400 laboratory-confirmed infections of S. poona that occurred in 23 states and in Canada. The outbreaks were traced to cantaloupes that were distributed from the Rio Grande region of Texas. Salmonella has also been implicated in several outbreaks involving tomatoes (Wood et al. 1991; Hedberg et al. 1994). Salmonella javiana was responsible for an outbreak in 1990 and S. montevideo in 1993. Contamination of fruits and vegetables with human pathogens can occur during growth in the fields, harvesting, postharvest handling, processing, and transporting (Beuchat 1996). Human pathogens found on produce include bacteria, viruses, and parasites. These pathogens make contact with the produce by cross contamination or by being naturally present in the environment. That environment can include fields, air, animals, and dust within a processing or packing facility. In the field, produce is subjected to irrigation, fertilization, and animal contact. Irrigation water is often not potable water and may contain pathogens (Sadovski et al. 1978). Beuchat and Ryu (1997) pointed out that soil contact can lead to accidental contamination by immature compost or environmentally present pathogens. They also stated that animal removal and control should be monitored frequently and, if possible, all animals should be eliminated from entering the premises of vegetable and fruit production and processing facilities. Animal contact is almost unavoidable. The FDA Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables (USFDA 1998) covers several of the following recommendations and many already discussed. This guide is only suggested and encouraged for use among farmers, producers, and processors. During harvesting, produce may be contaminated by human contact, equipment, or even packing or transport containers. Once it reaches the packing facility, all raw produce needs to be separated from sanitized product. Packinghouses and processing facilities have a need for increased awareness of proper wash sanitizers and worker cleanliness. This need is most critical in fresh-cut facilities because, as mentioned above, fresh-cut processing of vegetables and fruits removes the natural protective barriers to microbial attack, making the moisture and nutrients of the interior tissues readily available as a medium conducive to growth of microorganisms. Vegetable and fruit outbreaks have become more frequent and the result is a demand for regulations involving sanitation of all areas of the food chain (USFDA 1998; Brackett 1999).

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VI. TREATMENTS TO MAINTAIN QUALITY Fresh-cut vegetables and fruits are intended to be “ready-to-eat” products. This implies that they will be at their peak of freshness and quality when consumed, a difficult promise to fulfill given the diversity and vagaries of marketing that may impact the time and environmental conditions encountered between processing and consumption. To maintain the quality of these products at an acceptable level through their anticipated shelf life, a number of different treatments have been developed that address the negative quality changes associated with loss of fresh appearance, texture, flavor, and nutrition. Treatments to reduce browning and texture loss in fresh-cut products have been reviewed recently by Garcia and Barrett (2002). As with all other aspects of fresh-cut vegetable and fruit physiology and handling, temperature management is the first line of protection against negative quality changes.

A. Physical 1. Modified Atmospheres. Packages for fresh-cut vegetables and fruits protect the commodity against water loss and contamination by microorganisms. Fresh-cut packages are also designed to create and maintain a MA around the commodity to reduce unwanted metabolic reactions. Modified atmospheres help maintain fresh-cut quality and extend storage life by inhibiting metabolic activity, decay, browning (Gunes and Lee 1997; Gil et al. 1998c), chilling injury (Hong and Gross 2001; Gil et al. 2002), and especially by inhibiting ethylene biosynthesis and action (Kader 1986a; Kader et al. 1989; Mathooko 1996), which in turn helps to inhibit tissue browning and softening. The most common atmospheres consist of reduced O2 and elevated CO2 levels. Carbon monoxide is also sometimes included for inhibition of browning and microorganism growth. Modified atmosphere packaging is widely used for fresh-cut vegetables and fruits. Semipermeable plastic films are chosen for MAP so that the film permeability and product respiration can combine to produce a desirable steady state atmosphere within the package at an anticipated temperature (Kader et al. 1989). It is necessary to know the gas permeability characteristics of a potential MAP film at the temperatures to which it will be exposed and when the MAP contains a high-moisture product. Films for MAP typically have low water vapor permeability. Thus, the atmosphere within a fresh-cut MAP will usually be saturated with water vapor and condensation can easily occur. Although gas movement through water is slower than through films, the

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changes in package gas permeability when condensation occurs are not easily predicted. Carbon dioxide is more soluble in water than O2 or C2H4 and some film materials may exhibit a swelling of their structure and cross-link matrix and pores, resulting in higher rates of gas diffusion (Kader et al. 1989). Film permeability increases with temperature increase, but not nearly as rapidly as produce respiration. This means that MAP systems must be maintained within narrow temperature ranges to be effective and to avoid atmosphere injury to the product in the package. Plastic films typically have CO2/O2 permeability ratios of from 2 to 7 (Kader et al. 1989), meaning that elevated CO2 cannot easily be established without the O2 reaching a dangerously low level. The permeability ratio of CO2/O2 through a perforation is equal to 0.8, which allows much higher CO2 levels to be safely established for products that benefit from high CO2 (Fonseca et al. 1999), but perforation permeability is even less responsive to temperature than semipermeable plastics. The differential response of gas permeation through plastic films and the rate of respiration by the commodity combine to make temperature management extremely important for MAP products (Exama et al. 1993; Talasila et al. 1995). Elevated temperatures would not only cause a more rapid senescence of the commodity, but changes to the MA could result in the production of fermentative off-odors (Kato-Noguchi and Watada 1997) and the growth of anaerobic microorganisms (Brackett 1987). In the fresh-cut industry, it is recognized that packaged products are likely to be exposed to variable temperatures during shipping, in warehouse distribution centers, in retail store back rooms, and in refrigerated display cases, with the retail display temperature usually higher than that during shipping. MAP that has been optimized for transportation conditions is likely to result in anaerobic conditions at higher retail display temperatures, while MAP optimized for retail conditions has little effect at lower transportation temperatures. Thus, MAP for fresh-cut salads is commonly designed for an intermediate temperature of about 7°C. An ethanol sensor that would indicate whether fermentation has occurred was proposed as one way to address the problem of injurious O2 exposure (Smyth et al. 1999). A combination CA/MAP system to accommodate different temperatures during transport and retail display has been demonstrated for fresh-cut kale (Brecht et al. 2002). Such a system, when properly designed, could compensate for the different respiration rates and package gas permeation rates at two or more anticipated temperatures in the postharvest handling sequence. Vegetable and fruit tolerance of reduced O2 and elevated CO2 levels is related to skin resistance to gas permeation (Theologis and Laties 1982;

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Park et al. 1993). This has necessitated a wholesale reevaluation of the optimum atmospheres for fresh-cut vegetables and fruits (Watkins 2000; Gorny 2001). Because of the relative perishability of fresh-cut products, the atmosphere in the MAP is often actively established, either by flushing with the desired atmosphere or by pulling a slight vacuum and then injecting a desired gas mixture. Active MAP retained better color, and reduced translucency, respiration rate, and microbial population of freshcut cantaloupe compared with passive MAP (Bai et al. 2001). Chemical disinfection (Sapers and Simmons 1998), edible coatings (Baldwin et al. 1995a,b, 1996; Howard and Dewi 1996; Li and Barth 1998), natural plant products (Kato-Noguchi and Watada 1997; Leepipattanawit et al. 1997; Buta et al. 1999), ethylene absorbents (Abe and Watada 1991), gamma irradiation (Chervin and Boisseau 1994; Hagenmaier and Baker 1997), heat shock (Loaiza-Velarde et al. 1997), microbial competition (Liao 1989; Breidt and Fleming 1997), pulsed-microwave irradiation (Shin and Pyun 1997), and other nonthermal physical treatments (Hoover 1997) have all been evaluated as potential alternatives or adjuncts to MAP. 2. Heat Treatments. Brief exposures to temperature in the range of 40 to 60°C can redirect plant tissue metabolism toward production of heat shock proteins, which can, in some cases, prevent undesirable metabolic processes from occurring. For example, the synthesis of wound-induced enzymes of phenylpropanoid metabolism (e.g., PAL) can be prevented by giving lettuce tissue a brief heat shock (e.g., immersion in 45°C water for 90 s) after processing (Saltveit 2000). The heat-shocked tissue synthesizes innocuous heat-shock proteins in preference to enzymes of phenolic metabolism. By the time the tissue has recovered from the heat shock, the wound signal has dissipated and there is no further induction of enzymes of phenolic metabolism. While this technique is very effective at preventing browning in plant tissue with constitutively low levels of phenolic compounds (e.g., celery, lettuce), it is ineffective in tissue with constitutively high levels of phenolic compounds (e.g., artichokes, potatoes). Heat shock may similarly prevent enzymatic softening of fruit tissues. Mild heat treatment (45°C for 1.75 hours) of whole fruit prior to cutting retained greater fresh-cut apple firmness during storage for 21 days at 2°C (Kim et al. 1994). When muskmelons were dipped for 1 minute in 2.5% CaCl2 solutions at 20, 40, or 60°C, freshcut firmness was maintained or improved during storage at 5°C, especially with higher dip temperatures (Luna-Guzman et al. 1999). Heated water may also be useful alone or as a supplement to sanitizer treatment in reducing microbial populations on fresh-cut products. Delaquis et al. (1999) demonstrated a 3-log reduction in microbial

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(mainly pseudomonad) levels on fresh-cut lettuce washed in chlorinated (100 ppm) water at 47°C for 3 minutes compared to a 1-log reduction using 4°C chlorinated water. In contrast, the 47°C chlorinated water treatment favored the growth of E. coli O157:H7 and L. monocytogenes inoculated on the lettuce if it was stored at 10°C but not at 1°C (Delaquis et al. 2002). Li et al. (2001b) showed a 1.7- to 2.0-log reduction of mesophilic aerobic microflora upon treatment of fresh-cut iceberg lettuce with chlorinated (20 ppm) or non-chlorinated 50°C water for 90 seconds. However, they found no effect with the same heat treatment on E. coli O157:H7 (Li et al. 2001a) and enhanced growth of L. monocytogenes (Li et al. 2002) inoculated onto fresh-cut iceberg lettuce for both 5 and 15°C storage. 3. Irradiation. Irradiation has the potential to eliminate vegetative forms of bacterial pathogens as well as parasites and extend shelf life (Farkas et al. 1997; Hagenmaier and Baker 1997, 1998; Gunes et al. 2000; Prakash et al. 2000; Molins et al. 2001; Foley et al. 2002). However, irradiation doses required to eliminate some microorganisms may cause vitamin C losses, negative textural changes (Gunes et al. 2001), and enzymatic browning (Hanotel et al. 1995) in some vegetable and fruit tissues. Irradiation levels of 1.5–20 kGy are necessary to destroy yeasts and molds, that may exist as spores, and these levels are damaging to plant tissues (Kader 1986b; Brackett 1987). B. Chemical 1. Antimicrobials Sanitizers. The primary purpose of chemical sanitizers is to prevent contamination of food products by maintaining low levels of microorganisms in the processing environment. Two classes of sanitizers are recognized in terms of governmental regulation in the U.S., namely those that are expected to come in contact with the vegetables or fruits as a wash or rinse, and those that are used to control the growth of microorganisms on processing equipment, utensils, or other food contact surfaces (Beuchat 2000). The former are regulated in the United States by the Food and Drug Administration (FDA) and the Environmental Protection Agency (EPA), while the latter are regulated by the FDA. Freshcut vegetables and fruits are routinely rinsed, and sometimes also conveyed after cutting, in cold (0 to 1°C), chlorinated water (50–200 ppm free chlorine) with a pH of 7 or less. Application of chlorine is not very effective at reducing microbial levels on contaminated tissues, but rather primarily acts to reduce microbial loads in the water and prevent cross-contamination (Hurst 1995). The chlorine rinse also removes

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cellular contents at cut surfaces that may promote browning and also directly inhibits browning reactions (Brecht et al. 1993). E. coli inoculated on the surface of apples was little or not at all affected by sanitizers or washes (Annous et al. 2001). Microbial cells can become attached to plant tissues and to inert surfaces such as processing plant equipment, forming biofilms (Bartz and Tamplin 2002), and adhered cells are more resistant to sanitizers than unattached cells (Andrade et al. 1998). Vigorous cleaning is required to dislodge the microbes, which then may be eliminated. Cavitation from ultrasound improved the efficacy of chlorine in reducing S. typhimurium levels on iceberg lettuce from 1.7 to 2.7 logs, apparently by removing cells attached to the surface, rendering the pathogens more susceptible to the sanitizer (Seymour et al. 2002). Peroxyacetic acid is the next most commonly used sanitizer in fresh-cut processing plants and is relatively tolerant of organic matter and exceptionally effective against biofilms (Beuchat 2000). Other sanitizers used or proposed for use in fresh-cut plants include chlorine dioxide (ClO2), bromine and iodine compounds, hydrogen peroxide (H2O2), and ozone (Beuchat 2000). Food Additives. There are a few antimicrobial chemicals that may be applied directly to fresh-cut products. Chief among these are the weak acids, sorbic acid or potassium sorbate (Sofas and Busta 1993) and benzoic acid or sodium benzoate (Chipley 1993). These compounds are most effective against yeasts and molds, but also act against many decay and human pathogenic bacteria. They are highly lipophilic and easily cross the cell membrane in their undissociated forms, subsequently dissociating in the cytoplasm, which results in cytoplasmic acidification and inhibition of microbial growth (Gould 2000). Other organic acids such as citric acid may also be considered antimicrobial food additives, but they act mainly to acidify the surface of the vegetable or fruit tissue, thus making it inhospitable to microbial growth. Wiley (1994b) has reviewed the various preservative chemicals used in the food industry. 2. Browning Inhibition. Polyphenol oxidase, the enzyme that catalyzes the formation of o-quinones from o-diphenols, beginning the sequence of reactions leading to polymerization and formation of brown phenolic pigments in vegetable and fruit tissue, has a pH optimum of 6.0 to 6.5 and shows little activity below pH 4.5 (Whitaker 1994). Most chemical treatments that are applied to prevent browning contain an acidulant, usually citric acid, as one component to lower the product pH and inhibit PPO activity. Since browning involves oxidation reactions, another strategy for inhibiting browning is to add chemicals that act

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as reducing agents. Reducing agents, most commonly ascorbic acid or its isomer erythorbic acid, can reduce the o-quinines back to o-diphenols and prevent brown pigment formation. Being consumed in the process, however, reducing agents have a finite capacity to inhibit browning. Cysteine is a thiol amino acid that also inhibits enzymatic browning, perhaps by multiple mechanisms: reduction of o-quinone back to o-dihydroxyphenol, direct inhibition of PPO, or formation of a colorless cys-quinone adduct (Beaulieu and Gorny 2002). Ascorbic and erythorbic acids also act as acidulants. PPO includes copper as a component of its active site and chelating agents such as ethylenediamine tetraacetic acid (EDTA) can remove the copper and thus inhibit PPO activity. 3. Firmness Retention. Textural changes in fresh-cut vegetables and fruits are minimized at low temperatures. Thus, temperature management is the first step to maintain the initial, fresh textural quality of these products. The postharvest application of aqueous solutions of calcium salts as dips or sprays has long been used to control postharvest disorders in storage and maintain tissue firmness of fresh fruits and vegetables. Application of calcium salts to pears, strawberries, kiwifruit, nectarines, peaches, and melons helps to maintain tissue firmness (Morris et al. 1985; Rosen and Kader 1989; Agar et al. 1999; Gorny et al. 1999, 2002; Luna-Guzman et al. 1999; Luna-Guzman and Barrett 2000). The effects of calcium on tissue firmness are thought to be related to its dual effects of rigidifying cell wall structure by cross-linking ester groups and also preserving the structural and functional integrity of membrane systems (Poovaiah 1986). Calcium retained shredded carrot firmness by delaying senescence-related membrane lipid changes and also by augmenting membrane restructuring processes (Picchioni et al. 1996). The overall quality of carrot shreds (Izumi and Watada 1994) and zucchini slices (Izumi and Watada 1995) was improved by the application of calcium salts. Calcium treatment also reduced microbial growth on shredded carrots (Izumi and Watada 1994). Although calcium chloride has been most commonly used, calcium lactate is as effective without imparting the bitter flavor that calcium chloride can at higher concentrations (Luna-Guzman and Barrett 2000; Gorny et al. 2002). 4. Edible Coatings. Edible coatings have been formulated to prolong the shelf life and maintain quality of fresh-cut vegetables and fruits (Baldwin et al. 1996; Li and Barth 1998). Edible coatings act as barriers to water loss and gas exchange, thus creating internal MAs within tissues, and can serve as carriers for other GRAS treatments (Baldwin et al. 1995a,b). Incorporating the reducing agent ascorbic acid and the antimicrobials

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potassium sorbate and sodium benzoate into an edible coating on freshcut apple and potato improved their effectiveness compared with aqueous dips (Baldwin et al. 1996). Adjustment of coating pH to 2.5 gave optimal control of browning and microbial populations. Whitening of peeled carrot segments results from a physical phenomena involving drying of abraded cell remnants on the surface (Cisneros-Zevallos et al. 1995). Methods used to control whitening in carrots therefore concentrate on modifications to the surface of the peeled root segment (Avena-Bustillos et al. 1994; Cisneros-Zevallos et al. 1997). Edible coatings that increased water vapor resistance reduced white blush on peeled carrots (Avena-Bustillos et al. 1993; Sargent et al. 1994). An edible sodium caseinate/stearic acid emulsion also controlled white blush and in addition reduced respiration by about 20% when compared to the uncoated control (Avena-Bustillos et al. 1994). However, white blush was also controlled by treatments that modified the hydroscopic properties of the surface and did not leave a proteinaceous residue (Cisneros-Zevallos et al. 1997). Maintaining high RH around the commodity and storage at cold temperatures are effective control measures, but these measures have no residual effectiveness once the product is purchased and the package opened. A peeling process that did not leave surface debris that could form the whitish layer would effectively eliminate the problem. Physically polishing the peeled carrot sections or enzymatically digesting away the loose cellular debris would produce a smoother surface. It is increasingly clear that no single treatment such as MAP, acidulants, reducing agents, or calcium salts can be completely effective in reducing browning and maintaining firmness; rather, combination treatments are the most effective for fresh-cut products (Tapia deDaza et al. 1996; Gonzalez-Aguilar et al. 2000; Gorny et al. 2002). Edible coatings lend themselves well to this approach. However, inclusion of potentially allergenic compounds in edible coatings and the necessity of labeling the product as containing “artificial chemical compounds” may detract from their use on “natural” fresh-cut products.

VII. CONCLUSIONS Although fresh-cut products are rapidly being introduced and commercialized, our knowledge of how basic physiological processes are affected lags behind. Wounded tissues undergo accelerated deterioration and senescence. Minimizing the negative consequences of wounding in

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fresh-cut vegetables and fruits should result in increased shelf life and greater maintenance of nutritional, appearance, and flavor quality in these products. Although the effects of heat preservation and freezing on loss of nutrients in vegetables and fruits are well documented, little is known about how such losses occur in fresh-cut produce. Emerging postharvest technologies for extending the storage quality of fresh-cut produce are introduced at a rate that often precludes thorough evaluation of market and sensory quality attributes and effects on microbial growth. Knowledge of how various pre- and postharvest factors affect fresh-cut produce quality through changes in phytohormone levels or tissue sensitivity, cell walls, cell membranes, and key metabolic enzymes is largely unavailable. A concerted effort by postharvest scientists is required to reach a better understanding of the basic mechanisms of wound responses in freshcut produce in order to most effectively approach the development of treatments and handling practices that minimize the negative consequences of fresh-cut processing. Well over 100 different vegetables and fruits are or may potentially be prepared as fresh-cut products. In addition, there are many different approaches and combinations that may be taken to maintain fresh-cut produce quality, which include raw product selection, temperature management, cutting equipment and techniques, packaging to control water loss and respiratory gas concentrations, scrubbers or generator compounds to manipulate levels of respiratory gases and ethylene, heat or irradiation to control microbes and elicit beneficial physiological changes in vegetable or fruit tissues, chemical treatments to control microbes, oxidative reactions and textural changes, and edible coatings to control water and volatile movement and to carry antimicrobial or antibrowning chemicals. Thus, there is an obvious need for coordination and collaboration among the horticulturists, postharvest physiologists, engineers, food scientists, plant pathologists, and microbiologists working in this field if duplication of effort is to be avoided and the available time and resources are to be effectively applied. It may not be too strong a statement to suggest that the rise in popularity of freshcut produce is revolutionizing postharvest horticulture. LITERATURE CITED Abe, K., and A. E. Watada. 1991. Ethylene absorbent to maintain quality of lightly processed fruits and vegetables. J. Food Sci. 56:1589–1592. Abeles, F. B., P. W. Morgan, and M. E. Saltveit. 1992. Ethylene in plant biology. 2nd ed. Academic Press, San Diego, CA.

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7 Postharvest Physiology and Storage of Widely Used Root and Tuber Crops Uzi Afek Department of Postharvest Science of Fresh Produce Agricultural Research Organization Gilat-Agricultural Research Center Mobile Post Negev 85280, Israel Stanley J. Kays Department of Horticulture The University of Georgia Athens, Georgia, 30602-7273, USA I. INTRODUCTION II. CAUSES OF POSTHARVEST LOSSES A. Postharvest Stresses 1. Thermal Stress 2. Water Stress 3. Gas Stress 4. Radiation Stress 5. Chemical Stress 6. Mechanical Stress 7. Pathogenic Stress 8. Herbivory Stress B. Growth Responses C. Quality Alterations III. TUBER CROPS A. Potato 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Water Loss 4. Dormancy and Sprouting Prevention 5. Sprout Induction 6. Disorders 7. Postharvest Pathology Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 253

254 8. Chemical Changes During Storage B. Jerusalem Artichoke 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Water Loss 4. Dormancy and Sprouting 5. Disorders 6. Postharvest Pathology 7. Chemical Changes During Storage IV. ROOT CROPS A. Sweetpotato 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Water Loss 4. Sprouting 5. Disorders 6. Postharvest Pathology 7. Postharvest Entomology 8. Chemical Changes During Storage B. Carrot 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Water Loss 4. Sprouting 5. Disorders 6. Postharvest Pathology 7. Chemical Changes During Storage C. Cassava 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Water Loss 4. Sprouting and Vascular Streaking 5. Postharvest Pathology 6. Postharvest Entomology 7. Chemical Changes During Storage V. CORM AND RHIZOME CROPS A. Taro 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Weight Loss 4. Postharvest Pathology B. Ginger 1. Prestorage Treatments 2. Recommended Storage Conditions 3. Water Loss 4. Sprouting 5. Disorders 6. Postharvest Pathology 7. Chemical Changes During Storage LITERATURE CITED

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I. INTRODUCTION The expression “root and tuber crops” covers a wide cross-section of species with edible subterranean storage organs. Corms, bulbs, and rhizomes, though anatomically distinct, are also considered part of the group. The terms “tuber” and “tuberous root” were first used in the English language in 1668 by Wilkins in An Essay Towards a Real Character, and a Philosophical Language (Kays et al. 1992), although “root” was first used 518 years earlier, in 1150 (Napier 1906). Those that are commercially cultivated around the world include 38 root, 23 tuber, 14 rhizome, 11 corm, and 10 bulb crops (Kays and Silva Dias 1996), of which potato, cassava, and sweetpotato are the 4th, 6th, and 7th most important food crops in the world, collectively accounting for over 623 million t of product per year (FAO 2002). In this review, we cover the storage of the tuber crops potato and Jerusalem artichoke; the root crops sweetpotato, carrot, and cassava; the corm crop taro; and the rhizome crop ginger. The anatomical, physiological, ontological, and biochemical differences among and within the organ types lead to wide differences among these crops in the postharvest alterations they undergo, in their maximum potential longevity, and in their optimum storage conditions (Kays 1997). Plant parts that function as subterranean reproductive organs generally contain considerable stored nutrients, and typically exhibit fairly low metabolic rates and other unique features. For example, during secondary growth, the epidermis is replaced by the periderm, which forms a protective surface tissue. Periderm formation is important, not only in the normal development of these organs, but also postharvest, during which it heals wounds incurred during and after harvest and postharvest handling, and so prevents excessive water loss and microbial infection. Several of these organs contain dormant buds that under appropriate conditions can elongate to form shoots, which may affect product quality.

II. CAUSES OF POSTHARVEST LOSSES Harvested root and tuber crops are perishable; their high moisture content and metabolic rate lead to losses of both mass and quality. The primary causes of these losses are biotic and abiotic stresses (e.g., thermal, water, atmospheric composition, light, chemical, mechanical, pathological, herbivory), growth responses (e.g., sprouting, rooting), and quality alterations (e.g., diseases, normal metabolic processes).

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A. Postharvest Stresses 1. Thermal Stress. After harvest, plant parts are susceptible to injury by exposure to high and low temperatures, and considerable research has been directed toward establishing optimum storage temperatures. Since the resources available vary widely among and within geographical areas, the best storage solution for a given crop may also vary from location to location. In this review, we address the recommended storage conditions, irrespective of possible local resource limitations, and, when appropriate, alternative storage techniques. 2. Water Stress. The rate of moisture loss is modulated by the physical and chemical characteristics of the crop and the conditions to which the product is exposed after harvest. The rate of water vapor loss from the tissue depends on the magnitude of the resistance to the diffusion of water, conferred mainly by the periderm, and the forces driving movement [i.e., primarily the magnitude of the gradient in the chemical potential of water between the product and its surrounding environment, generally expressed as the vapor pressure deficit (VPD)]. The steeper the gradient, the more rapid the water movement. In highly moist root and tuber crops, movement is almost always outward from the product. Thus, minimizing water loss depends on maintaining or increasing the resistance to diffusion and/or reducing the VPD. The diffusion resistance of periderm lenticels, areas of lower resistance, can increase during storage (Banks and Kays 1988). In addition, packaging (e.g., plastic bags) and surface coating can be effective in increasing it. The standard method for retarding postharvest moisture losses is to minimize the water VPD between the product and its storage environment, and while this can be accomplished with a high storage relative humidity, it is critical that free moisture does not form on the surface of the product. Control of relative humidity (RH) generally involves the addition of water to the air and the precise monitoring of the air moisture content. The devices used to add moisture fall into two general classes: isothermal and adiabatic. Isothermal humidifiers use an external heat source to change water to steam, whereas adiabatic humidifiers use mechanical energy to generate a fog or mist of water droplets (Lefebvre 1989). Spinning disk humidifiers are the most commonly used adiabatic devices in potato storage rooms in the United States, Canada, and Israel (Brook et al. 1995); however, they tend to produce relatively large (i.e., 30–50 µm in diameter) droplets, which, at high RH (i.e., ≥93–94%), may promote condensation on the surface of the product, thus stimulating

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pathogen activity (Hide and Lapwood 1992; Afek and Warshavsky 1998). Atomizer humidifiers, whether hydraulic (water - air) or rotary (windmill or motor driven), give smaller droplets (≤10 µm in diameter), allowing higher storage humidities. 3. Gas Stress. The atmosphere within a harvested product can strongly affect its metabolism and potential storage life. Of particular interest are the concentrations of oxygen, carbon dioxide, and ethylene. Ethylene from external sources, for example, can cause bitterness in stored carrots, rendering them unfit for consumption. Controlled atmosphere (CA) storage has been tested on some root and tuber crops, but the benefits are generally not sufficient to warrant commercial use. Of critical importance are the concentrations of the respective gases within the product. The internal concentration depends on the rate of synthesis (ethylene, carbon dioxide) or utilization (oxygen) of the gas by the product, the resistance to its diffusion into or out of the product, and the difference in partial pressure between the interior and exterior. Though CA storage is little used for root and tuber crops, the use of plastic bags or surface coatings can have a pronounced effect. 4. Radiation Stress. Visible, ultraviolet (UV) and ionizing radiations can readily alter the quality of harvested products. Visible light is particularly damaging to potato tubers because it induces the synthesis of toxic glycoalkaloids. Very low levels of diffuse light, however, are recommended during the unrefrigerated storage of certain roots and tubers. 5. Chemical Stress. Chemical stresses during storage are relatively uncommon; when they occur, it is generally because of the inappropriate application of postharvest chemical treatments or inadvertent exposure to pollutants. 6. Mechanical Stress. Root and tuber crops are subjected to a wide range of mechanical stresses during harvest, postharvest handling, and storage. Mechanical stresses that cause a physical injury represent one of the most serious causes of quality loss after harvest. Physical injuries decrease the value of the product, increase its susceptibility to diseases and water loss, and often significantly shorten its life. Such damage tends to increase at each postharvest stage (e.g., harvest, transport, sorting, storage, packaging, marketing, etc.). The three most important types of mechanical stress are friction, impact, and compression, which result in tissue failure via cleavage, slip, bruising, and buckling (Kays 1997). While mechanical stresses are a significant postharvest problem for root and tuber crops, they are beyond the scope of this review.

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7. Pathogenic Stress. Large quantities of harvested root and tuber crops are lost because of a wide range of microorganisms (e.g., fungi, bacteria, viruses, mycoplasms, and nematodes), of which fungi and bacteria are the most important. These crops possess a wide array of structural and biochemical barriers to infection; for example, the periderm and surface waxes covering the organ inhibit the invasion of opportunistic pathogens, and harvest and handling procedures that break these barriers greatly increase the risk of pathogen attack during storage. Also, endogenous factors that impede invasion tend to weaken with time, increasing susceptibility to infection. Postharvest treatments or conditions that eliminate the causal organism or impede its development decrease the chances of storage rots. 8. Herbivory Stress. Serious herbivory losses during storage are relatively infrequent in root and tuber crops, except for the sweetpotato, which is attacked by the sweetpotato weevil (Cylas spp.) both before and during storage. The relatively high storage temperature for the crop and the pest’s short life cycle makes the insect a significant problem in some geographical areas. The larvae tunnel throughout the storage roots, triggering the synthesis of a toxic fruanoterpenoid, thus presenting a food safety problem as well as compromising the quality of the product.

B. Growth Responses During the storage of root and tuber crops, growth responses, such as the development of shoots, roots, and secondary storage organs (e.g., in cassava and Jerusalem artichoke), are generally undesirable (Hanover 1960; Wickham and Wilson 1988). Many subterranean storage organs are dormant at harvest (e.g., potato, yam, ginger, Jerusalem artichoke), and the duration of dormancy can determine the storage life of certain products. Products that do not have a dormancy mechanism or which have emerged from dormancy must be stored under conditions that impede growth. Sprouting, for example, decreases the dry matter content and also greatly increases the surface area and, consequently, the rate of water loss from the product. As a consequence, a number of treatments have been developed to extend dormancy and/or prevent the resumption of growth. When the storage organ is to be used as a reproductive propagule, however, sprouting is desirable and conditions and/or treatments to facilitate dormancy breaking or growth stimulation are used.

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C. Quality Alterations Most of the quality alterations that root and tuber crops undergo during storage are undesirable. They include disease development and chemical changes associated with normal metabolism (e.g., depletion of stored carbohydrates). Quality alterations are not critiqued specifically in this review but, when relevant, they are addressed under the appropriate topic heading (e.g., disorders, chemical changes).

III. TUBER CROPS A. Potato The potato (Solanum tuberosum L., Solanaceae) is the fourth most important food crop grown worldwide, with a total yield of over 308 million tonnes (t) in 2001 (FAO 2002). While predominately a temperate crop, potato is also grown in hot climates (Cargill et al. 1989, Afek and Warshavsky 1998). In most production areas, harvested tubers are stored, extending their availability for up to 10 months (Burton et al. 1992). The maximum storage duration is often determined by the propensity to sprout, which varies widely among cultivars. Tuber dormancy, therefore, is a critical component of storage potential. The value of the crop is diminished by losses in fresh weight and desirable quality attributes, losses mainly caused by respiration, disease, evaporation, mechanical damage, sprouting, chemical changes in quality attributes (e.g., color), and damage caused by abiotic stresses (e.g., temperature, gas atmosphere, light) (Es and Hartmans 1987a,b; Meijers 1987a; Rastovski 1987, Burton et al. 1992). 1. Prestorage Treatments. Potato tubers sustain mechanical damage during harvesting and transport, and often during grading and marketing after storage. Injury to the surface periderm not only accelerates moisture loss but exposes the interior of the tubers to opportunistic pathogens that cause dry and soft rots during storage. Curing is a prestorage treatment used for a number of subterranean organs where the harvested product is exposed to temperature and RH conditions that facilitate wound healing (Kays 1997). The precise conditions and their duration vary depending upon the crop in question. Under favorable curing conditions (e.g., 2 weeks at 12–16°C, 90–92% RH), potato tuber tissue forms a protective layer (wound periderm) over the damaged area (Meijers 1987b; Cargill et al. 1989; Burton et al. 1992). A thin layer of suberized

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cells is differentiated over the surface of the damaged area, followed by deposition of cork cambium (phellogen) under the sealing layer, giving rise to a densely packed network of new cells with little intercellular space. Curing is essential to limit weight loss and to prevent the penetration of microorganisms, and the temporal relationship between wound healing and microorganism penetration is critical. Tubers are routinely cured on entry into storage, a key feature of successful storage (Meijers 1987b). Sprout inhibitors and treatments to inhibit microbes, also applied prior to storage, are detailed in the Dormancy and the Postharvest Pathology sections, respectively. 2. Recommended Storage Conditions. Recommended conditions vary according to the type of potato (early-crop vs. main-crop), cultivar, intended use, and the storage facilities available (heated, refrigerated, or nonrefrigerated). After curing, potatoes are stored in sacks, pallet boxes, bulk bins or piles, depending upon the facility and the volume being handled. A major part of the potato crop in the U.S. is held in nonrefrigerated, naturally ventilated storage houses, generally in piles or bins 2.5 to 6 m deep (Sparks et al. 1968; Sparks and Summers 1974). Optimum storage conditions are similar to those in refrigerated storage, but the control is less precise. With refrigerated storage, main-crop and seed potatoes are stored at 3.5–4.5°C (4°C is considered optimum) and 90–95% RH; however, certain cultivars are best held at higher temperatures [e.g., 7°C for ‘Russett Burbank’ (Cunningham, et al. 1971), 10°C for ‘Kathahdin’ and ‘Kennebec’ (Sawyer et al. 1965)]. Early-crop potatoes are seldom stored for long, but can be held for up to 4–5 months at 4°C. Main-crop potatoes for chips (crisps) and French fries (chips) are stored at 10–13°C, 90–95% RH. For processing, it is essential that the reducing sugar content be low; if it is too high, the tubers are held at 18–20°C for 1–4 weeks until an appropriate level is reached. Ventilation is critical for heat removal and uniform gas distribution. Generally air flow rates of 0.3–0.4 m3 ⋅ min–1 ⋅ t–1 are recommended; however, in the midwest of the U.S., 0.6–0.7 m3 ⋅ min–1 ⋅ t–1 is recommended for table stock and 0.8–1.0 m3 ⋅ min–1 ⋅ t–1 for seed stock (Smith 1977). 3. Water Loss. Water loss during storage not only reduces the total mass of product and, therefore, its value (Rees et al. 1981; Es and Hartmans 1987a,b; Rastovski 1987; Brook et al. 1995), it is also a primary cause of quality loss (Villa and Bakker-Arkema 1974). Significant moisture loss renders tubers more susceptible to mechanical damage (e.g., bruising) and discoloration, and typically increases peeling losses (Rastovski 1987). The greater the water potential difference or water VPD, the more rapidly

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moisture is lost from the tubers (Es and Hartmans 1987c; Kleinkopf 1995). The periderm is the primary barrier to diffusion loss, and localized areas of lower resistance, such as lenticels, facilitate water loss. The diffusion resistance of the lenticels, however, often increases during storage (Banks and Kays 1988). While resistance primarily depends on the anatomical structure of the tubers, moisture loss is reduced by minimizing the water VPD between the tubers and their storage environment by means of a high storage RH (Es and Hartmans 1987c; Burton et al. 1992). The importance of RH is illustrated by the difference in weight loss between tubers (‘Desiree’) stored for 6 months at 96–98% or at 82–86% RH, i.e., 2 and 7%, respectively (Afek et al. 2000b). Lowering storage temperature also decreases moisture loss, though temperature fluctuations can exacerbate losses through their effect on the RH and VPD of the storage environment. The recommended storage temperature depends upon the type and/or use of the potatoes (Cargill et al. 1989; Burton et al. 1992). 4. Dormancy and Sprouting Prevention. Dormancy, a period of suspended growth (Emilsson 1949; Burton 1963; Goodwin 1966; Harkett, 1981; Hemberg 1985), often determines the maximum storage time of potato tubers, but postharvest handling and storage conditions may also be important (Espen et al. 1999a,b). In general, potato tubers are dormant at harvest and, in the absence of dormancy-breaking treatments, remain so pending fulfillment of the normal dormancy requirement, when sprouting occurs spontaneously. Sometimes sprouting can be suppressed, as described below. Thus, maintenance or extension of dormancy is an integral feature of storage procedures. The dormancy duration depends upon the cultivar, tuber maturity, and soil and weather conditions during growth (Krijthe 1962; Burton 1963). Unusually cold, wet weather can extend dormancy by about 4 weeks, whereas extremely dry, warm conditions can reduce it by up to 9 weeks (Burton 1966). Sprouting impairs the quality of the tuber in that water and other constituents are derived from the tubers for the new cells in the sprouts, which in turn are discarded prior to use. Sprouting also increases the surface area and reduces water diffusion resistance, accelerating weight loss. The primary methods for inhibiting sprouting during storage are the use of low temperatures (i.e., 2 to 4°C) and sprouting suppressants (Rastovski 1987). However, low temperatures can accelerate the conversion of starch to sugar (Rees et al. 1981; Morrell and Rees 1986b; Es and Hartmans 1987a; Ross and Davies 1992), thus reducing tuber quality

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(Rastovski 1987). Sprouting inhibitors found effective in commercial use include isopropyl N-(3-chlorophenyl) carbamate (CIPC), propham (IPC), maleic hydrazide (MH), and tecnazene (TCNB) (Hajslova and Davidek 1986; Buitelaar 1987; Es and Hartmans 1987b; Yada et al. 1991); ethylene, morphactin, nonanol, abscisic acid, and indoleacetic acid, although effective, have not been adopted (Hartmans and van Es 1979; Wang et al. 1980; Beveridge et al. 1981; Rama and Narasimham 1986; Es and Hartmans 1987b). More recently, carvone has proved an efficacious sprouting inhibitor (Oosterhaven et al. 1995; Wiltshire and Cobb 1996; Sorce et al. 1997). There are problems, however, with some sprout inhibitors. IPC and CIPC suppress suberization and the formation of wound periderm, and therefore should be used only after curing (Edgar 1968; Es and Hartmans 1987b). MH is applied as a foliar spray 4 to 6 weeks before harvest, but too early application reduces yield, while late applications do not inhibit sprouting adequately (Es and Hartmans 1987b; Yada et al. 1991). TCNB is not effective if dormancy has already been broken, the storage room is excessively ventilated, or the storage temperature is above 10°C (Es and Hartmans 1987b). Additionally, there are current or pending restrictions on the use of these compounds in several countries (Lewis et al. 1997; Afek and Warshavsky 1998). Several other compounds have proved to inhibit sprouting effectively during storage. Hydrogen peroxide (HPP) (stabilized with a mixture of substances whose patent is pending), applied with an atomizing fogger to control postharvest pathogens, was found to inhibit sprouting; after 6 months at 10°C, there were no sprouts longer than 2 mm on potatoes treated with 10% HPP at 5-week intervals (Table 7.1) or with CIPC (Afek et al. 2000a). In untreated controls, 84% of the tubers had sprouted. The effects of dimethylnaphthalene (DMN) and diisopropylnaphthalene (DIPN) on the sprouting of ‘Russet Burbank’ tubers were compared with those of CIPC (Lewis et al. 1997). Two applications of DIPN (300 mg ⋅ kg–1 as a.i. in f.w.) were as effective as one application of CIPC (22 mg ⋅ kg–1 as a.i. in f.w.) but DMN was less effective than DIPN or CIPC. After 178 days of storage, only tubers treated with CIPC and DIPN were devoid of sprouts, and after 295 days, the average tuber sprout lengths were 8 and 14 mm, respectively. In another study (Kalt et al. 1999), carvone, dimethylnaphthalene (DMN), and ethylene were compared with the commercial standard, CIPC, as sprout inhibitors. After 25 weeks at 9°C, total sprout weight and maximum sprout length were ranked CIPC ≤ carvone < ethylene < DMN; neither CIPC- nor carvone-treated tubers had sprouts. Oosterhaven et al. (1995) had previously demonstrated that carvone inhibited sprouting (‘Bintje’) and that inhibition took effect

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Table 7.1. Sprouting of ‘Desiree’ potato tubers (%) during 6 months of storage at 10°C and 95% RH, following treatment with hydrogen peroxide (HPP) (four applications), isopropyl N-(3-chlorophenyl) carbamate (CIPC), or control. The hydrogen peroxide is stabilized with additional substances (the composition of which is currently patent pending) and applied with an atomizing fogger (Afek et al. 2000a). Sprouting (%)

Treatment HPP CIPC Control z

1

2

0 az 0 az 8 bz

0a 0a 26 b

Storage period in months 3 4 0a 0a 48 b

0a 0a 63 b

5

6

0a 0a 74 b

0a 0a 84 b

Means separated by Fisher’s protected least significant difference test, (5% level).

immediately after treatment. Daniels-Lake et al. (1996) compared the effects of ozone, 1,8-cineole, and CIPC on sprouting (‘Russet Burbank’) over 25 weeks at 9°C and found that CIPC and 1,8-cineole completely inhibited sprouting, whereas ozone had little effect. Several essential oils derived from aromatic plants such as Lavandula angustifolia Miller (lavender), Mentha pulegium L. (mint), Mentha spicata L. (spearmint), Origanum onites L. (Turkish oregano), Origanum vulgare L. ssp. hirtum (Greek oregano), Rosmarinus officinalis L. (rosemary), and Salvia fruticosa Miller (sage) were assessed as sprout inhibitors for ‘Spunta’ potato (Vokou et al. 1993). Except for oregano oil, all suppressed sprout growth; however, lavender, sage, and rosemary oils were more effective. After 5 weeks of storage, lavender oil was the most effective of these in suppressing sprout emergence and elongation (i.e., ≈90%) while the other oils inhibited elongation by 72–83% (Fig. 7.1). Rama and Narasimham (1986) tested hot-water-dip and vapor-heat treatments at temperatures ranging from 50–80°C and 60–70°C, respectively, as a means of inhibiting sprouting in stored potatoes. Hot water, at temperatures and durations sufficient to inhibit sprouting, damaged the tubers, whereas vapor treatment (60°C, 95% RH for 60 min) suppressed sprouting for 3 weeks at ambient conditions (22–35°C, 50–80% RH) without any deleterious side effects. If the treatment was repeated after 3 weeks, sprouting was suppressed for an additional 3 weeks. 5. Sprout Induction. Breaking tuber dormancy is often desirable to accelerate and synchronize seed potato stand establishment. Many studies

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120

Inhibition (%)

100 80 60 40 20 0 0

10

20 Time (d)

30

40

Fig. 7.1. Percentage inhibition in the length of potato tuber sprouts after exposure to the volatile essential oils (1.0 ml ⋅ 4 l–1 air) of Lavandula angustifolia (■), Salvia fruticosa (□), Mentha pulegiuum ( ), and Mentha spicata () (after Vokou et al. 1993).

•

have addressed high-CO2 and/or low-O2 stress as dormancy breakers (Thornton 1939a,b; Burton 1958, 1968; Goodwin 1966; Burton and Wiggington 1970; Coleman 1987; Esashi 1991; Coleman et al. 1992; Wiltshire and Cobb 1996). For example, exposure of ‘Russet Burbank’ tubers to CO2 : O2 ratios of 20:40% and 60:20% for 7 days facilitated dormancy release and sprout emergence, an effect that was further enhanced by ethylene at 50 µl ⋅ l–1 (Fig. 7.2) (Coleman and McInerney 1997) . In light of the effects of CO2 and O2 on endogenous ethylene synthesis (Esashi 1991), the effect on tuber dormancy release (Rylski et al. 1974) may be related to increased synthesis of aminocyclopropane-lcarboxylic acid and subsequently the phytohormone (Esashi 1991; Mattoo and White 1991; Smith and John 1993). The elapsed time from harvest and the storage temperature were found to be important in dormancy release by CO2 and O2 (Coleman 1998). Previous research had also implicated abscisic acid (ABA) in tuber dormancy induction and maintenance (Hemberg 1985; Suttle and Hultstrand 1994; Suttle 1995). Altered CO2 - O2 environments also resulted in changes in endogenous ABA levels within the tubers, as did ethylene treatment (Fig. 7.3).

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DAP for 50% emergence

215 210 205 200 195 190 185 180 0

2

4 6 8 Duration of Treatment (d)

10

12

Fig. 7.2. The effect of exposure to 20% CO2 + 40% O2 + ethylene at 50 µl ⋅ l–1 on the number of days after planting (DAP) to reach 50% shoot emergence in field-grown ‘Kennebec’ potato tubers (after Coleman and McInerney 1997).

3.5 Gas I Ethylene Gas II Control

ABA (nmol g –1)

3.0 2.5 2.0 1.5 1.0 0.5 0 0

100

200 Time (h)

300

Fig. 7.3. Time course of changes in abscisic acid content on a dry weight basis in the apical eye region of ‘Russet Burbank’ potato tubers from the late dormancy phase (150–220 DAP), removed from 13°C storage and exposed for 7 d to Gas I (60% CO2 + 20% O2), Gas II (20% CO2 + 40% O2), C2H4 at 1.74 µmol ⋅ 1–1, or air controls. Treatments began 162 days after planting (DAP) and continued for 168 h (after Coleman 1998).

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6. Disorders Greening. Chlorophyll synthesis is triggered when potato tubers are exposed to light after harvest. Light-skinned cultivars tend to be more susceptible than russet types. The green coloration of the skin and underlying flesh is not in itself harmful, but there can be a concurrent synthesis and accumulation of glycoalkaloids (predominately solanine) that are toxic in large quantities (Jadhav and Salunkhe 1975). Greening is prevented by minimizing the exposure to light throughout the postharvest period. Blackheart. Tubers with blackheart display a blackened center from which cavities may eventually develop. The disorder is caused by lack of oxygen within the tuber, a condition that is exacerbated by elevated temperatures (Stewart and Mix 1917). Control measures include maintenance of adequate ventilation and appropriate storage temperatures (Snowdon 1992). Mahogany Browning. Exposure of certain cultivars to low temperatures (0°C for 20 weeks or longer) causes an irregular reddish-brown discoloration within the tubers (Hilborn and Bonde 1942). Stem-End Browning. A dark brown or black discoloration develops at the stem end of the tubers of certain cultivars (Ramsey et al. 1949); it is thought to be related to storage temperature. Tubers can be temperature conditioned (e.g., 0°C for 60 days) as a means of control. 7. Postharvest Pathology. During storage, potatoes may be affected by fungal or bacterial diseases that can spread readily under favorable conditions. Initial infection or inoculation almost always occurs in the field and the organism is then brought into storage. The most common fungal diseases of stored potatoes are early blight—Alternaria solani (Ell and Mart.) Sol.; gray mold—Botrytis cinerea Fr; black rot—Colletotrichum coccodes (Waller.) Hughes; dry rot—Fusarium spp.; silver scurf— Helminthosporium solani Dur. & Mont.; gangrene—Phoma spp.; soft rot—Phythium spp.; potato blight—Phytophthora infestans (Mont.) De Bary; black scurf—Rhizoctonia solani Kuhn; powdery scab—Spongospora subterranae (Waller.) Laregh; and common scab—Streptomyces scabies (Thaxter) Waksman & Henrici. Bacterial diseases include ring rot—Corynebacterium sepedonicum; soft rot—Erwinia carotovora subsp. carotovora (Jones) Bergey et al.; soft rot—Erwinia carotovora subsp. atroseptica (van Hall) Dye, Blackleg; and brown rot—Pseudomonas

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267

solanacearum (E.F. Sm.) E. F. Sm. (Perombelon et al. 1987a,b; Hide and Lapwood 1992; Tsror et al. 1993, 1999; Afek and Warshavsky 1998). Erwinia carotovora (soft rot), Helminthosporium solani (silver scurf), and Fusarium spp. (dry rot) are particularly serious postharvest pathogens that can readily spread in storage, causing severe losses (Rich 1968; Meijers 1987a; Hide and Lapwood 1992; Wastie et al. 1994). Lack of effective chemical controls exacerbates the problem within cold storage rooms, but control of E. carotovora and H. solani has been achieved with a fog of hydrogen peroxide containing a stabilizing component (HPP) (Afek et al. 1999a, 2001). Following disinfection, the decay of ‘Desiree’ tubers caused by E. carotovora after 5 months of storage was 4% compared with 26% in control tubers (Table 7.2). Decay caused by H. solani after 6 months was reduced to 2% following five monthly treatments with a 10% HPP fog, compared with 38% rot in the non-treated control. A single treatment reduced decay from 38% to 16%; however, multiple treatments were decidedly superior (Table 7.3) (Afek et al. 2001). Hydrogen peroxide is a relatively environmentally safe disinfectant, thought to act through oxidative damage to the fungi and bacteria. The lack of effective chemicals impedes control of Fusarium dry rot in stored tubers. However, several means of biological control have been found effective in laboratory studies. They were based on bacterial antagonists (Kiewnick and Jacobsen 1997; Schisler and Slininger 1994; Schisler et al. 1997), yeasts (Schisler et al. 1995), and arbuscular mycorrhizae (Niemira et al. 1996). In commercial-scale storage experiments, Schisler et al. (2000) found that Pseudomonas fluorescens S22:T.04 decreased dry rot in pathogen-coinoculated tubers by 19%, compared

Table 7.2. Percentage of ‘Desiree’ potato tubers with decay, either with (+) or without (–) Erwinia carotovora inoculation, and with (+) or without (–) subsequent treatments with 10% hydrogen peroxide (HPP) during 5 months of storage at 8°C and 95% RH. The hydrogen peroxide is stabilized with additional substances (the composition of which is currently patent pending) and applied with an atomizing fogger (Afek et al. 1999a). Decay (%) Treatment Inoc

HPP

1

2

+ + – –

+ – + –

1 bz 4 cz 0 az 2 bz

2b 7c 0a 3b

z

Storage period in months 3 4 2b 12 d 0a 6c

3b 18 d 1a 10 c

Means separated by Fisher’s protected least significant difference test, (5% level).

5 4b 26 d 1a 15 c

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Table 7.3. Percentage decay of ‘Desiree’ potato tubers caused by Helminthosporium solani following 0, 1, or 5 treatments with 10% hydrogen peroxide (HPP) during 6 months of storage at 9°C and 95% RH. The hydrogen peroxide was stabilized with additional substances (the composition of which is currently patent pending) and applied with an atomizing fogger (Afek et al. 2001). Decay (%)

No. treatments

1

2

5 1 0

0 az 0 az 5 bz

0a 3b 9c

Storage period in months 3 4 1a 7b 16 c

1a 10 b 24 c

5

6

2a 14 b 31 c

2a 16 b 38 c

z

Means separated by Fisher’s protected least significant difference test, (5% level).

with controls or the fungicide thiabendazole (TBZ); in subsequent tests, P. fluorescens P22.Y:05 and Enterobacter cloacae SI I:T:07 reduced the severity of the disease by 25 and 17%, respectively, when the antagonists were applied after the pathogen inoculum. Prestorage exposure to ultraviolet (UV) irradiation suppressed diseases in potatoes stored for 3 months at 8°C (Ranganna et al. 1997). Dry rot caused by Fusarium solani in tubers inoculated with conidia and incubated at 28°C for 24 h was completely suppressed at a UV dose of 15 kJ ⋅ m–2. Soft rot caused by Erwinia carotovora was suppressed by a UV dose of 15 kJ ⋅ m–2 after the tubers had been inoculated with the bacterium and incubated at 37°C for 6 h. When inoculated tubers were not incubated before the UV treatment, dry rot was completely suppressed at only 12.5 kJ ⋅ m–2, but soft rot was not. Prestorage steam treatment has also been found effective in reducing the incidence of various pathogens in stored seed tubers (i.e., 2–3% vs. 35–52% in untreated controls) (Afek and Orenstein 2002). In addition, the presence of pathogens in the daughter tubers 120 days post-planting was only 3–4% in steam-treated tubers compared with 26–31% in the untreated controls. 8. Chemical Changes During Storage. Depending upon the cultivar, mature tubers contain 16–23% dry matter, of which starch is the predominant component (~70%) (Burton 1966; Augustin 1975). Potato starch is comprised of 21–25% amylose and 75–79% amylopectin. The rate of starch hydrolysis during storage has a critical impact on tuber quality. Also present are sucrose, glucose, fructose, and substantially smaller amounts of several other sugars. The reducing sugar content is

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269

A

120 100

200

80

150

60

100

40

50

20

0

0

25 Sucrose (u mol g –1)

B

250

C

D

20

70 60 50

15

40

10

30 20

5 0 –60

10 0 –30

0

30 60 Time (d)

90

120

–60

–30

0

30 60 Time (d)

90

Amino Acids (u mol g –1)

Glucose-6-P (nmol g –1)

300

Reducing sugars (u mol g –1)

important in potatoes that are to be fried (Es and Hartmans 1987a; Burton et al. 1992); tubers that are high in reducing sugars (principally glucose and fructose) darken because of the reaction of aldehyde groups with amino groups of amino acids or other sources (Schaaf 1974), and intense discoloration may reduce product marketability. Typically 2.5 to 3 mg of reducing sugar per gram fresh wt is the maximum permissible level for potato chips (crisps) and ~5 mg per gram for French fries. During storage, starch is progressively hydrolyzed to provide energy and carbon skeletons for maintenance and synthetic reactions. Under certain conditions, there is a pronounced increase in hydrolysis and formation of reducing sugars, the amount of which varies with cultivar, tuber age, injury, decay, moisture status, sprouting, and exposure to temperature extremes (Burton and Wilson 1978; Burton et al. 1992; Espen et al. 1999a,b). Tuber response to low temperatures depends on its initial metabolic status. Storage of potatoes at 0–5°C increases the sugar concentration and may damage membranes (Workman et al. 1976); storage at 25–36°C also results in a significant increase in sugar, probably because of the onset of sprouting (Ludwig 1970; Verma et al. 1974a,b). Storage temperature does not appear to affect the amino acids concentration (Fig. 7.4). Most stress factors that disturb the metabolic

120

Fig. 7.4. Changes in the concentrations of glucose-6-phosphate (A), reducing sugars (B), sucrose (C), and amino acids (D) on a fresh weight basis in the parenchymatic tissue of potato tubers before normal harvest (■) and in tubers stored at 23°C (□) or 3°C ( ) for various periods. Time scale is in days before or after normal harvest (after Espen et al. 1999a,b).

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equilibrium in the tubers appear to increase the sugar concentration (Burton 1969; Samotus et al. 1974a,b; Sowokinos 1973; Vliet and Schriemer 1960). Under appropriate storage temperature conditions, the sugar concentration remains relatively constant for an interval after harvest and then increases, at first slowly and finally very sharply. Sugar formation during senescence (i.e., “senescence sweetening”) (Burton 1966) is associated with a decline in the condition of the cellular membranes and differs from sugar increases caused by low temperatures; the latter can be remedied by reconditioning (Isherwood 1973, 1976; Ohad et al. 1971), whereas age-induced sugar formation is not reversible and reconditioning is ineffective (Isherwood 1976). When potato tubers are stored at or below 10°C, they accumulate sugars, primarily glucose, fructose (reducing sugars), and sucrose (Sowokinos 1990) through “cold sweetening.” Reducing sugars accumulate because of up-regulation of the gene encoding sucrose phosphate synthase (SPS) (Hill et al. 1996). Along with the activation of sucrose synthesis, de novo amylolytic activity induced in the cold-stored tubers accelerates amylopectin degradation enhancing sweetening (Isherwood 1976). Starch-degrading enzymes reported in potato tubers include α-amylase, isoamylase, β-amylase, α-glucosidase, and starch phosphorylase (Fan 1975; Gerbrandy et al. 1975; Kennedy and Isherwood 1975; Killilea and Clancy 1978; Schneider et al. 1981; Cochrane et al. 1991a,b; Cottrell et al. 1993). However, it is not clear whether the degradation is primarily amylolytic or phosphorolytic; Morrell and Rees (1986a) concluded that it was phosphorolytic because they detected no amylase activity in the tubers, but several other authors (Sowokinos et al. 1985; Cochrane et al. 1991b; Cottrell et al. 1993) have detected substantial activity. Low storage temperatures result in increased α-amylase, β-amylase (Cochrane et al. 1991b; Cottrel et al. 1993; Nielsen et al. 1997) and phosphorylase (Claassen et al. 1993) activities, although the latter has not been universally found (Kennedy and Isherwood 1975; Hill et al. 1996). Alpha-glycosidase activity was not influenced (Nielsen et al. 1997), whereas β-amylase activity increased as the temperature decreased from 5 to 3°C; the increase began by day 3 and the activity had increased fourto fivefold within 10 days. The onset of sugar accumulation coincides with activation of SPS and the appearance of a new form of amylase (Hill et al. 1996; Nielsen et al. 1997). After 10 days, accumulation of sugars was negligible at 11, 9, or 7°C, but considerable at 5 and 3°C (Fig. 7.5). Total starch hydrolysing enzyme activity was unaltered at 7°C, increased at 5°C, and increased further (i.e., up to seven- to eightfold) at 3°C. The increase in amylolytic activity correlated with the appearance of a new amylase,

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271

50 Glucose Fructose Sucrose Total

u mol hexose

40 30 20 10 0 3

5

7 9 11 Storage Temperature (°C)

20

Fig. 7.5. Sugar concentration in potato tubers after storage at various temperatures. Tubers were harvested and stored for 4 wk at 20°C and then held at 11, 9, 7, 5, or 3°C for 10 d (after Deiting et al. 1998).

while increases in acid invertase activity did not correlate with increased sugar concentration. Cold-induced changes in SPS and amylase are reversed if the tubers are returned to a higher temperature (Deiting et al. 1998). SPS and invertase increased 2.2- and 7.7-fold, respectively, during 28 days at 1°C (Charmara et al. 1998). Sucrose synthase (SS) activity remained constant at 1°C and was similar to that in tubers kept continuously at 10°C. With the transfer of tubers from 1 to 10°C, there was a sharp rise in respiration, which peaked at day 7, and then declined. During reconditioning, sucrose declined rapidly, while glucose and fructose declined more slowly. Sucrose synthase activity increased sharply during 7 days at 10°C and both SPS and invertase decreased. Low O2 inhibited the decrease in sugar content and suppressed the rise in SS activity, but it did not alter the decreases in SPS and invertase activities. B. Jerusalem Artichoke Jerusalem artichoke (Helianthus tuberosus L., Asteraceae) is a perennial that is grown as an annual. International production statistics are not collected, but it is a significant crop in some Eastern European countries.

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The aerial plant parts die in the early winter, at which time the tubers are harvested. There are many cultivars with selection depending upon latitude and other factors (McCarter and Kays 1984). Increased interest in the crop has stemmed from the fact that carbon is stored in the Jerusalem artichoke as inulin, a straight chain fructan that is minimally digested by humans and can be used as a bulking agent in foods in which sugar is replaced with an artificial sweetener. Thus, the volume previously occupied by sugar is filled with an extremely low-calorie material, greatly reducing the total caloric content of the product. With little reformulation, inulin, though not sweet, functions similarly to sugar (i.e., browning reactions, aroma synthesis, textural properties) in many foods. Also, inulin, whether ingested in Jerusalem artichoke tubers or as a bulking agent, is a dietary fiber and confers a number of health benefits: for example, it lowers blood cholesterol level; promotes Bifido bacteria in the large intestine; reduces the blood levels of sugar, lowdensity lipoproteins, and triglycerides; and is beneficial to certain heart diseases (Farnworth 1993; Hirayama and Hidaka 1993; Sakun et al. 1996; Varlamova et al. 1996). Tuber size and shape are critical attributes that are strongly modulated by cultivar and production conditions. Many clones have an irregular and undesirable tuber surface topography due to branching, an objectionable trait. The tubers are harvested in the late fall, generally after the first frost. In production areas where the crop can be harvested throughout the winter, it can be field stored until needed. Elsewhere, harvest is followed by cold storage. 1. Prestorage Treatments. We found no references to prestorage treatments. The tubers are typically not cleaned before storage unless they are to be held under refrigeration and have significant amounts of adhering soil. The surface of the tubers should be devoid of free water to discourage the growth of pathogens. 2. Recommended Storage Conditions. The three primary storage options are refrigerated storage, common storage [e.g., root cellars, clamps or pits (Shoemaker 1927) which utilize natural cooling], and in situ field storage (Sibley 1924; Cormany 1928). Cold storage is highly effective but expensive; nevertheless, it is routinely used for seed and fresh-market tubers, especially where field storage is not practicable. Root cellars, clamps, and pits are used when the tubers must be harvested in the fall, before the ground freezes or other adverse conditions set in, and where refrigeration is not available or is too expensive.

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273

Field storage is a viable option in northern hemisphere locations that are sufficiently far north to ensure cold soil throughout the winter, but not so far that the surface of the soil freezes solid and prevents harvesting. Another requisite is relatively sandy, well-drained soils that allow the use of harvesting machinery throughout the winter. Locations that have a maximum number of potential harvest days are preferable, in that they increase harvest continuity. Locations that do not meet these criteria generally require the use of refrigerated or some other form of indoor storage. Jerusalem artichoke tubers can be stored for 6–12 months at 0 to 2°C and under a high RH (90–95%). Some cultivars are much more susceptible to storage losses than others (Steinbauer 1932). At low humidities, the tubers shrivel readily and are more likely to decay than if kept in a moist atmosphere. Tubers have relatively low respiratory rates when held at low temperatures (e.g., 10.2 mg CO2 ⋅ kg–1 ⋅ h–1 at 0°C), but they produce heat (vital or respiratory heat) (e.g., 111 J ⋅ kg–1 ⋅ h–1 at 0°C) that must be removed if the desired low temperature is to be maintained (Peiris et al. 1997). The tubers can withstand low temperatures but they freeze below –2.2°C (Whiteman 1957). Freezing inflicts little damage above –10°C, but rapid deterioration occurs at lower temperatures; significant chemical and physical alterations occur in the plasma membrane, most notably losses in sterols and phosphatidylethanolamine (Uemura and Yoshida 1986) with a concurrent loss of membrane function. As with most fleshy plant products, the temperature at which freeze damage occurs and the extent of the damage vary with cultivar, season, preconditioning, rate of freezing, and so on (Kays 1997). The potential of controlled atmosphere storage has not been adequately assessed. It has been shown to impede inulin depolymerization, apparently through an effect on enzyme activity. Storage of tubers in a 22.5% CO2/20% O2 atmosphere significantly retarded inulin degradation (Denny et al. 1944). Gamma irradiation of Jerusalem artichoke tubers greatly accelerates inulin depolymerization (Salunkhe 1959) and it offers no known advantage to offset this disadvantage. 3. Water Loss. While desiccation losses can be relatively easily prevented with proper storage conditions, they remain a significant storage problem, because the tubers lack a surface layer of corky cells with a high water diffusion resistance (Decaisne 1880). In addition, their surface cells can be readily injured, which facilitates desiccation (Traub et al.

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1929a). The thin periderm causes the tubers to lose moisture at a rate depending on the water VPD. Therefore, storage at a high RH (90–95%) is essential (Shoemaker 1927; Traub et al. 1929a; Johnson 1931; Steinbauer 1932). 4. Dormancy and Sprouting. The dormancy period of Jerusalem artichoke tubers varies among cultivars and even among the tubers from a single plant. The dormancy mechanism within the tubers responds to an environmental signal, in this case low temperatures. Sufficient exposure duration to the appropriate temperature (i.e., below a specific maximum and generally near 0°C) fulfills the dormancy requirement, and under appropriate environmental conditions, the cells within the tuber begin to divide and the tuber sprouts. Tuber dormancy also has significant agricultural implications. Production of the crop in regions where the cold period does not fulfill the dormancy requirement can be greatly impaired by the lack of or uneven sprouting in the spring; also, insufficient cold exposure can lead to spotty sprouting with a significant percentage of tubers remaining dormant. When this occurs, the carry-over of unsprouted weed tubers into a succeeding crop makes their eradication difficult. The tubers become dormant in the fall, prior to the actual completion of their development. Steinbauer (1939) observed the onset of dormancy (two cultivars) between Aug. 28 and Sept. 7, and found that after this time, freshly dug tubers did not sprout even under suitable environmental conditions. The larger, more mature tubers were the last to enter dormancy. The onset of dormancy appeared to be a gradual process; it was initially established in the stolons and small, younger tubers, well before the completion of the maturation process and the first frost. The depth of dormancy varies considerably among cultivars and tubers within a cultivar, so that some tubers will sprout as soon as they are exposed to conducive conditions, while others are delayed considerably. In a study of 145 cultivars, Boswell (1932) found the time required for 50% of the tubers to sprout when not subjected to a cold treatment ranged from 54 to 200 days; 150 to 180 days was typical for most cultivars. Also, the degree of dormancy varied among seasons. Cutting the tubers did not alter the depth of the dormancy. Steinbauer (1939) found that treatment with chemicals, e.g., ethylene chlorohydrin, could shorten the dormancy, although some of the chemicals tested also slowed the subsequent sprout growth. The optimum temperature range for dormancy breaking is 0 to 5°C; higher temperatures, such as 10°C, result in very slow dormancy breaking (Steinbauer 1939) and lead to increased rotting (Steinbauer 1932) and

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moisture loss (Traub et al. 1929a). Also, at the higher temperature, the emerging sprouts were less vigorous. Fluctuating low temperatures (–1.1 to 4.4°C) were less effective than a constant 0°C. Typically, 30 to 45 days at 0°C was sufficient to break dormancy in the two cultivars tested (‘Chicago’ and ‘Blanc Ameliore’). Dormancy completion sets off a cascade of reactions that leads to sprouting. Any treatment that breaks dormancy (e.g., 4°C for 12 to 16 weeks) results in modification of the apical bud and its conversion into an elongating shoot (Courduroux 1967; Tort et al. 1985). With the onset of shoot development, there is an increase in the rate of protein synthesis (Masuda 1965, 1967), a shift in the metabolism of purine nucleotides (Le Floc’h et al. 1982; Le Floc’h and Lafleuriel 1983a,b), and an overall acceleration of the rate of metabolism. With sprouting, the number of ribosomes, present almost exclusively as monosomes, decreased considerably (Bagni et al. 1972). As dormancy is broken, there is an increase in RNA synthesis (Gendraud and Prévôt 1973; Gendraud 1975a,b), enhanced incorporation of amino acids (Cocucci and Bagni 1968), and alterations in free and bound amino acids (Scoccianti 1983). In addition, with the onset of development, there are significant alterations in the activities of certain enzymes, e.g., phosphoenolpyruvate carboxylase activity increased fourfold (Dubost and Gendraud 1987). Significant changes in water status within the tuber accompany sprouting, with water moving from subtending regions into the growing bud. The reallocation of existing constituents was also indicated by the findings that the parenchyma cells of dormant tubers took up sucrose more readily and that the tetraphenylphosphonium concentration and the intercellular pH was higher than in non-dormant tubers (Gendraud and Lafleuriel 1983). Gendraud and Lafleuriel (1983) interpreted these findings to indicate the possibility that an H+-sucrose co-transport mechanism was involved in dormancy. In addition, Ottono and Charnay (1986) found that the uptake of abscisic acid differed between dormant and non-dormant tubers. 5. Disorders. Storage losses are due primarily to desiccation, disease, sprouting, freezing, and inulin depolymerization. No physiological disorders have been reported. 6. Postharvest Pathology. Storage rots can be a serious problem (Johnson 1931; McCarter and Kays 1984; Barloy 1988; Cassells et al. 1988) and their development is usually strongly and positively temperature dependent. The disease organisms most frequently isolated from Jerusalem

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artichoke tubers were Botrytis cinerea Pers. and Rhizopus stolonifer (Ehrenb.: Fr) Vuill, though R. stolonifer and Sclerotinia sclerotiorum (Lib.) de Bary are the most serious rot-causing organisms at low storage temperatures (Johnson 1931). In contrast, Sclerotium rolfsii Sacc. and Erwinia carotovora spp. (Jones) Bergey et al. are not significant pathogens below 20°C. Control of postharvest rot organisms is facilitated by storage at low temperatures (i.e., 0 to 2°C), removal of diseased tubers prior to storage, minimizing mechanical damage to the tubers, and proper humidity control. 7. Chemical Changes During Storage. Stored tubers undergo significant changes in carbohydrate chemistry which, depending upon the intended use, can have a pronounced effect on their quality. It is important to note that inulin is not one compound but a series of molecules of various chain lengths (Tanret 1893) which begin to depolymerize during storage (Thaysen et al. 1929; Traub et al. 1929b; Bacon and Loxley 1952; Jefford and Edelman 1960; Jefford and Edelman 1963; Rutherford and Weston 1968; Modler et al. 1993a,b; Ben Chekroun et al. 1994; SchorrGalindo and Guiraud 1997), whether the tubers are harvested or left in situ. The degree of polymerization is critical for uses such as fat replacement or high fructose syrups. With the former, as the chain length decreases, the ability of inulin to mimic a lipid in foods diminishes. Likewise, with progressive depolymerization, the ratio of fructose to glucose decreases and, upon hydrolysis, yields a progressively less pure fructose syrup. For example, during winter storage, the ratio of fructose to glucose decreased from 11 to 3 (Schorr-Galindo and Guiraud 1997); thus, syrups derived from stored tubers would contain substantially more glucose.

IV. ROOT CROPS A. Sweetpotato Sweetpotato (Ipomoea batatas (L.) Lam., Convolvulaceae) is grown for its fleshy storage roots. Though a perennial, the crop is grown as an annual. The sweetpotato is the seventh most important food crop in the world, with an annual production of 136 million t (FAO 2002), however, in the United States it is used primarily as an occasional vegetable. The sweetpotato confers a wide range of health benefits (Kays and Kays 1998) that have recently enhanced its popularity.

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Table 7.4. Weight loss (percentage) of sweetpotato roots stored in the open (control) and in sand, soil, or sawdust, under tropical conditions (adapted from Ray et al. 1994). Weight loss (%) Storage medium Open (control) Sand Soil Saw dust

0

15

Storage period in days 30

45

60

0 az 0 az 0 az 0 az

7.7 b 6.2 b 9.4 b 10.8 b

10.4 b 8.8 b 11.8 b 15.0 c

19.9 d 20.2 d 16.5 e 17.6 c

43.9 f 28.4 g 28.2 g 29.4 g

z

Means separation by Duncan’s multiple range test, (5% level).

The sweetpotato does not have a developmental stage at which it is mature; the storage roots continue to grow and under favorable field conditions will enlarge until the interior becomes anaerobic and/or rots. Therefore, the crop is harvested when the majority of the roots in a field have reached the desired size. 1. Prestorage Treatments Curing. Roots should be cured by being kept at 30°C and 90%–97% RH for 4–7 days immediately after harvest (Lutz 1945; Lutz and Simons 1958; Dempsey et al. 1970; Kushman 1975). During curing, ventilation is required to remove CO2 and replenish O2. Curing heals wounds inflicted during harvest and handling, helps to reduce moisture loss during storage and decreases the potential for decay. In addition, curing facilitates the synthesis of enzymes that improve the flavor during cooking (Wang et al. 1998; Kays and Wang 2000). The effects of temperature and relative humidity on wound healing have been investigated extensively (Morris and Mann 1955; Strider and McCombs 1958; McClure 1960). As curing begins, the outermost parenchyma cells at the wound site desiccate. The subtending parenchyma cells then become suberized (Morris and Mann 1955; Wagner et al. 1983; Walter and Schadel 1983) and a lignin-like wound periderm forms beneath the suberized layer. Healing is adequate when the wound periderm is three to seven cells thick, which can be verified with a simple color test (Walter and Schadel 1982). Walter and Schadel (1983) characterized the structure and chemical composition of suberin and lignin in both the epidermis and healed wounds. Amand and Randle (1989) studied the relationship between ethylene production, wound lignification, and wound periderm formation

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following wounding of ‘Centennial’. Ethylene production preceded wound lignification and wound periderm formation by 24 to 48 h, respectively. Blocking ethylene action with 2,5-norbornadiene increased ethylene production, blocked wound periderm formation for the 12day duration of the test, and strongly suppressed and delayed lignification. Blocking ethylene synthesis with aminooxyacetic acid or CoCl2 decreased ethylene production to 10% of that in the control. Lignification and wound periderm formation were also suppressed and their initiation delayed, suggesting the involvement of ethylene in lignification and wound periderm formation Radiation. Sweetpotato shelf life is not extended by gamma irradiation treatment. Ascorbic acid and starch concentrations decreased after exposure to 1.5–2.0 kGy, while those of sucrose and total sugars increased with increasing radiation dosage (Ajlouni and Hamdy 1988). Gamma irradiation also enhanced softening (Lu et al. 1986). 2. Recommended Storage Conditions. Cured sweetpotatoes should be moved carefully (usually in palletized containers) to a separate storage room and held at 14 ± 1°C and 85–90% RH (Dempsey et al. 1970; Kushman 1975). Long-term storage experiments have shown that roots can be stored successfully under these conditions for up to a year without sprouting (Picha 1986a,b), though sensory quality declines with extended storage. Air flow in the storage room should be about 0.3 m ⋅ s–1 at optimal temperature and relative humidity (Dempsey et al. 1970). Storage of sweetpotatoes at or above 19°C results in considerable sprouting after several months, and an associated loss in root quality and marketability, but storage below 12°C results in chilling injury. Storage of sweetpotatoes under controlled atmosphere (CA) reduces the rate of respiratory losses and increases total sugars (Chang and Kays 1981), but additional research on O2 and CO2 concentrations, timing, and cultivar requirements is needed. Uncured roots have been shown to decay rapidly when stored in low-O2 environments, though 2 and 4% O2 did not appear to be harmful to cured roots (Delate and Brecht 1989). To date, the beneficial effects of CA storage for sweetpotatoes have not been shown to outweigh the cost. 3. Water Loss. Evaporation is a major cause of weight loss during sweetpotato storage; its rate is closely tied to the RH of the surrounding air (Afek and Kays 2002; Afek and Wiseblum 1995). When ‘Beauregard’ sweetpotatoes were stored for 4 months at 85 or 95% RH and 15°C, the weight losses were 11% and 2.4%, respectively. Thus losses can be sub-

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stantially reduced by storing under high RH (Afek and Kays 2002). Ray et al. (1994) in India compared the fresh weight of roots stored in the open (control) with that of those covered with sand, soil, or sawdust, and found that after 2 months the control roots lost approximately 44% of their fresh weight compared with 30% in the other treatments. 4. Sprouting. In temperate growing areas, the storage root is used to produce planting material (slips) for the new crop; in the tropics, vine cuttings are typically used. When slips are required, the potential to sprout and the number of sprouts per root are critical selection traits in breeding programs for acceptable new cultivars. However, precocious sprouting during storage is highly undesirable, since it appreciably shortens the storage life of the roots. Sprouting roots exhibit a distinct proximal dominance (Kays and Stutte 1979); aging in storage increases the sprouting. Sweetpotato storage roots do not exhibit dormancy; under favorable conditions they sprout readily immediately after harvest. Sprouting can be inhibited by proper temperature management (i.e., 14°C); at 19°C or above, the roots sprout after several months. Sprouting can also be inhibited by a postharvest application of CIPC (Scott et al. 1970), however, the chemical is not currently cleared for use and should not be considered a substitute for proper temperature management. Storage in a medium with sufficient moisture for fibrous root formation encourages sprouting, which utilizes the stored nutrients and moisture in the roots, and thus compromises root quality; it also increases the surface area of the root, accelerating water loss. 5. Disorders Hardcore. Hardcore is a physiological disorder manifested by the failure of parts of the root to soften during cooking; it is believed to be caused by chilling effects on the cellular membranes (Yamaki and Uritani 1972, 1973, 1974). All cultivars are susceptible to hardcore, but they vary in susceptibility (Buescher et al. 1975a; Daines et al. 1976; Porter et al. 1976; Broadus et al. 1980; Picha 1987) and non-cured roots are more susceptible than cured ones (Lutz 1945; Daines et al. 1976; Picha 1987). Souring. Roots may be lost during curing and/or storage, following preharvest exposure to anaerobic conditions (Ahn et al. 1980a,b; Chang et al. 1982, 1983) caused by excessive soil moisture. The roots may initially appear sound, but they decompose rapidly in storage, emitting a distinctive sour, fermented odor. The surviving roots undergo greater

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shrinkage than sound ones during subsequent storage and typically yield a low-quality baked product (Ton and Hernandez 1978; Ahn et al. 1980a,b; Corey et al. 1982). Internal Breakdown or Pithiness. Pithiness, found in apparently sound roots, is characterized by a significantly reduced density, and sponginess (Harter et al. 1923; Artschwager 1924; Kushman and Pope 1972); the intercellular air space exceeds 12%. The disorder has been attributed to high respiratory and water losses, and susceptibility varies with cultivar. Curing and storage conditions that are conducive to a rapid metabolism favor pithiness, as storage carbohydrates are depleted rapidly. Sprouting in storage and preharvest exposure to low soil temperatures (5–10°C) also increase pithiness. Cracking. Storage root cracking may develop during growth or in storage. Cracks formed during storage are typically longitudinal splits near the end of the root and are generally shallower than growth cracks (Clark and Moyer 1988). Distal End Rot. Distal end rot develops at the root end of the storage organ. Its occurrence is cultivar dependent, and ‘Acadian’ is highly susceptible (Martin 1958). No pathogenic organism has been isolated and the cause remains undetermined. Chilling Injury. Sweetpotato storage roots are susceptible to chilling injury when stored below 12°C (Dempsey et al. 1970; Lewis and Morris 1956; Picha 1987; Whiteman and Wright 1946), and they freeze at –1.9°C (Whiteman 1957). Symptoms of chilling injury include root shriveling, surface pitting, abnormal wound periderm formation, fungal decay, internal tissue browning (Whiteman and Wright 1946; Lewis and Morris 1956; Dempsey et al. 1970; Picha 1987), and hardcore formation (Daines et al. 1974, 1976; Buescher et al. 1975a; Broadus et al. 1980). Synthesis of chlorogenic acid and other phenolic compounds has been associated with tissue browning (Dempsey et al. 1970; Lieberman et al. 1958; Porter et al. 1976; Walter and Purcell 1980). The severity of chilling injury depends on the temperature and the duration of exposure to temperatures below 12°C (Dempsey et al. 1970; Picha 1987). After exposure to chilling, the respiratory rate of roots at 16°C increased linearly with the duration of the preceding exposure to the lower temperature (Dempsey et al. 1970; Lewis and Morris 1956; Picha 1987). The total sugar content of roots stored at 7°C was signifi-

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cantly greater than that in those stored at 16°C (Dempsey et al. 1970; Picha 1987), though the effect was highly cultivar dependent. Effects of Ethylene. Exposure of sweetpotatoes to ethylene should be avoided during storage and handling. Exposure of roots to ethylene at 10 µl ⋅ l–1 reduced their β-amylase activity (Buescher et al. 1975b). When roots of ‘Tainung’ and ‘Chailai’ were exposed to ethylene (100 µl ⋅ l–1), their β-amylase activity increased threefold during the first day and then decreased rapidly to the original level (Chang et al. 1996). Ethylene also enhanced the synthesis of phenolic compounds and phenolic oxidizing enzymes that can result in increased discoloration of the roots. The effect, however, requires the roots to be exposed to ambient concentrations of ethylene that would normally not be encountered in properly ventilated storage rooms. 6. Postharvest Pathology. Among the more commonly encountered microorganisms that cause storage rots are Lasiodiplodia theobromae (Java black rot) (synonymous with Botryodiplodia theobromae and Diplodia gossypina), Ceratocystis fimbriata (black rot), Erwinia chrysanthemi (bacterial soft rot), Fusarium oxysporum (surface rot), Fusarium solani (root rot), Macrophomina phaseolina (charcoal rot), Monilochaetes infitscans (scurf), and Rhizopus stolonifer (soft rot) (Clark and Moyer 1988; Clark 1992; Clark et al. 1992). Timing of infection varies with the organism and field/harvest/storage conditions (Moyer 1982). Black rot, fusarium root rot, scurf, and bacterial soft rot infections can occur before, during, or after harvest. In contrast, soft rot infections tend to be induced at or after harvest, while charcoal rot, dry rot, surface rot, and root rot occur during harvest. Harvest and postharvest pathogens are typically opportunistic, entering the root via an injury. Internal cork is a virus-mediated disorder in which the root tissue develops necrotic lesions during storage (Nusbaum 1946, 1950; Martin 1949; Kushman and Pope 1972). The number and size of lesions vary widely and increase with increasing storage duration and storage temperature (Nielsen 1952). The lesions are found primarily in the interior but may also be present on the surface. Control of postharvest diseases centers on prevention because little can be done once the root is infected. During harvest, care must be taken to minimize damage to the roots and proper sanitation is important. After harvest, the roots should be cured immediately and then stored at the appropriate temperature. Mechanical damage should be carefully prevented during movement from curing to storage rooms, and then

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during washing, sorting, and grading prior to marketing. Wash water should be frequently changed to prevent accumulation of inoculum, and calcium hypochlorite should be added to the water. Postharvest pesticides, if used, must be in accordance with the appropriate laws. In Israel, ‘Georgia Jet’ is more susceptible to storage pathogens than cultivars with higher dry matter contents, such as ‘Jewel’ and ‘Beauregard’ (Picha 1986a,b; Rolston et al. 1987; Stevens et al. 1990). Exposure to low temperatures in the field (e.g., ≤8°C) leads to subsequent rapid deterioration in storage, via Rhizopus spp. and Fusarium spp. (Afek et al. 1998a; Clark and Moyer 1988; Clark 1992). In situ treatment of the stored roots by applying a fog of 1% iprodione from an atomizing humidifier substantially reduces rot incidence (e.g., 5% vs. 61% in controls) (Table 7.5) (Afek et al. 1999a). Isolates taken from rotten areas indicated that the decay was caused by Rhizopus spp. and Fusarium spp. 7. Postharvest Entomology. The sweetpotato weevil (Cylas formicarius (F.), Coleoptera: Brentidae) is the most devastating insect pest of the crop worldwide, both in the field and in storage. The adult can find the roots in total darkness by sensing their volatile emissions (Wang and Kays 2002). To date, there are no adequate field or storage control measures available (Nottingham and Kays 2002), therefore, infested roots should not be placed in storage. CA storage may have promise (Delate and Brecht 1989) and some success has been achieved by storing the roots at low temperature or immersing them in hot water (52–62°C for 10 min) (Hahn and Anota 1982). Fruit flies (Drosophila spp.) and soldier flies [Hermetia illucens (Diptera: Stratiomyidae)] can pose problems where there are diseased, soured, or damaged roots, but both can be controlled with sanitation and/or appropriate insecticide treatment (Boyette et al. 1997). Table 7.5. Percentage of ‘Georgia Jet’ sweetpotato roots rotting during 5 months of storage (13°C, 90% RH) with (+) or without (–) a prestorage treatment of 1% iprodione (Afek et al. 1999a). Rot (%)

Iprodione

1

2

Storage period in months 3

4

5

+ –

1 az 6 bz

2a 22 b

2a 38 b

3a 50 b

5a 61 b

z

Mean separation by Fisher’s protected least significant difference test, (5% level).

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283

8. Chemical Changes During Storage. Storage roots undergo significant chemical changes during curing and storage. Respiration is highest immediately after harvest and decreases during the first few months of storage (Chang and Kays 1981; Picha 1986b). The concentration of starch, the predominant form of stored carbon in the roots, also decreases during storage (Dempsey et al. 1970; Scott et al. 1970). About 75% of the total starch in the roots at harvest is amylopectin, which increases to about 80% during curing, the remaining 20% being amylose (Scott et al. 1970). Only small amounts of dextrins are present at harvest, but their concentration increases during curing. The primary sugars present, in descending order of abundance, are sucrose, glucose, and fructose (Kays and Horvat 1983; Picha 1986a; Walter and Hoover 1984). There are significant quantitative differences among cultivars in their patterns of carbohydrate change during curing and storage. Typically, reducing (Jenkins and Gieger 1957; Picha 1986a;), nonreducing (Morris and Mann 1955; Jenkins and Gieger 1957; Picha 1986a), and total sugars (Morris and Mann 1955; Picha 1986b) increase during curing and the first few months of storage. However, nonreducing sugars have been reported to decrease in some cultivars (Morris and Mann 1955; Lambou 1958; Picha 1986a), and in some cultivars reducing sugars do not increase (Picha 1986a). Likewise, there is no increase in total sugar concentration in some cultivars (Dempsey et al. 1970; Picha 1986a). Storage temperature also influences the sugar concentration in the roots; low temperatures (e.g., 7°C) stimulate sucrose synthesis (Picha 1987). The percent dry matter in the roots decreases during long-term storage, as starch is utilized as a respiratory substrate. Alpha-amylase activity increases during storage (Deobald et al. 1971); β-amylase activity increases during storage in some cultivars (Morrison et al. 1988), whereas inconsistent changes in activity were found in others (Walter et al. 1975). The concentration of pectic substances decreases by as much as 40% by the 6th month in storage (Scott et al. 1970). A decrease in protopectin and an increase in soluble pectin concentrations occur during curing, with the opposite during storage (Heinze and Appleman 1943). In another study, sweetpotatoes stored at 13°C for 3 months displayed minor fluctuations in soluble pectin and protopectin (Daines et al. 1976). Protein was degraded during storage (‘Jewel’) and non-protein nitrogen (NPN) concentration decreased during the first 14–15 weeks, followed by an increase (Purcell et al. 1978). As much as 40% of the total N in the roots may be NPN (Purcell et al. 1978), the major components of which, after 107 days in storage, were asparagine (61%), aspartic acid (11%), glutamic acid (4%), serine (4%), and threonine (3%). The

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concentration of individual amino acids also changed during storage (Purcell and Walter 1980). The primary changes in fatty acids after curing and during several months of storage are an increase in tetracosanenoic acid concentration and a decrease in the concentration of short-chain saturated fatty acids (Dempsey et al. 1970). The orange flesh color in sweetpotato is due to carotenoid pigments, primarily β-carotene, a precursor of vitamin A. The concentration of carotenoids increased slightly during curing and shortterm storage (Daines et al. 1974; Hammett and Miller 1982). The vitamin C concentration generally decreases during curing and storage (Ezell and Wilcox 1952; Speirs et al. 1953; Hammett and Miller 1982). B. Carrot Carrot (Daucus carota L., Apiaceae) is a biennial temperate crop grown for its fleshy tap root. Over 20 million t were produced worldwide in 2001 (FAO 2002). Storage techniques range from field storage to refrigerated storage rooms. Harvestable maturity of carrots depends upon their intended use. Most carrots are stored as mature roots, but immature bunched roots, with or without their tops, and small, fresh-cut (i.e., minimally processed) roots are also stored for short periods to facilitate marketing. Optimum handling and storage conditions vary accordingly. 1. Prestorage Treatments Washing. Prestorage washing is desirable if the carrots have much soil or organic matter adhering to the roots (e.g., when harvested during wet conditions or from sandy soils). Washing can decrease the population of decay-causing organisms and help to facilitate air circulation around the roots in storage. Precooling. Prompt precooling to or below 5°C after harvest is essential for extended storage because delays increase decay incidence during storage. Hydrocooling is commonly used; loose carrots can be cooled from 25 to 5°C in about 9 min in 1°C water, but it takes about 11 min for those packed in mesh bags (23 kg) (Ryall and Lipton 1979). The precise cooling time varies with root size and temperature, and type of hydrocooler. The half-cooling time should be determined for the specific conditions at each site to maximize the throughput. 2. Recommended Storage Conditions. Mature topped carrots can be stored for 7 to 9 months at 0–1°C, 98–100% RH (Berg and Lentz 1966, 1973; Kirki 1971). Even under optimum conditions, however, 10–20%

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of the roots will show some decay after 7 months. At higher storage temperatures (e.g., 5–10°C), sprouting and decay increase appreciably within a few months (Platenius et al. 1934; Kirki 1971; Sherf 1972). Under typical commercial conditions (0–5° C; 90–95% RH), carrots can be successfully stored for only 5–6 months (Ryall and Lipton 1979). The maximum storage duration for immature carrots with their tops attached is about 2 weeks at 0°C, 95–100% RH. Removal of the tops significantly extends the potential storage duration. Contact icing is recommended during transit, especially with loose or bunched carrots with their tops, to retard water loss and maintain freshness. Temperatures below 0°C should be avoided since carrots can freeze at –1.2° C (Whiteman 1957). Freezing causes cracking and blistering of the surface; after thawing, discoloration, a water soaked appearance, and a flaccid texture develop (Parsons and Day 1970). Air circulation between crates or pallet boxes in which carrots are stored is desirable to remove respiratory heat, to maintain uniform temperatures, and to help prevent condensation. An air velocity of about 7 to 10 cm ⋅ s–1 is adequate at low storage temperatures (Berg and Lentz 1966). Controlled atmosphere storage is rarely used for carrots, but modified atmosphere packages are used for fresh-cut carrots. Storage of intact carrots in atmospheres of 5–10% CO2 and 2.5–6% O2 can lead to mold growth and rotting that is greater than that occurring in conventional storage conditions (Berg and Lentz 1966; Weichmann 1977). The oxygen concentration is critical because quality declines rapidly under anaerobic conditions; therefore, selection of packaging materials with appropriate oxygen transfer rates is imperative (Sode and Kuhn 1998). The importance of preventing low-oxygen stress in fresh-cut carrots has stimulated interest in ethanol biosensors (Smyth et al. 1999). Ozone has been tested as a volatile fungicide, applied during storage to repress postharvest pathogens. Ozone reduced decay but also increased the rates of respiration and electolyte leakage and decreased the color intensity of the roots (Liew and Prange 1994). Gamma irradiation at levels that did not cause significant damage has been shown to alter the respiration rate of grated carrots but not of intact roots (Chervin et al. 1992); it is not used commercially. 3. Water Loss. Carrots lose moisture and shrivel if not stored under high RH (i.e., 98–100%) (Hurschka 1977); lower RH (90–95%) results in greater moisture loss, increased decay, and loss of crispness and other quality attributes (Kirki 1971; Berg and Lentz 1973, 1977; Krahn 1974). Cooling as rapidly as possible after harvest also has a pronounced influence on the root’s moisture status. For example, the water potential

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decreased by more than 200% within 48 h when freshly harvested roots were stored at 18°C, >98% RH (Herppich et al. 1999). Cultivars vary in their propensity to lose moisture after harvest (Shibairo et al. 1997). Water VPD, air movement, storage temperature, and product surface to volume ratio are the predominant controlling factors. Immature and partially mature carrots are routinely topped and packed in polyethylene consumer bags or 23-kg mesh bags for marketing. If they were promptly precooled and trimmed of all traces of leaf growth before packaging, they can be held for 4–6 weeks at 0°C, 98–100% RH. The roots should be packed in low-density polyethylene bags, whose thickness depends on the quantity contained (Afek et al. 1998b; Suojala 1999). The bags should be perforated to allow ventilation and to prevent the development of off-flavors; 3–6-mm holes are spaced evenly over the surface (e.g., twelve 3 mm holes for 1-kg bags) (Hardenburg et al. 1953; Afek et al. 1998b, 1999b). 4. Sprouting. The enlarged tap root serves as a storage site for the carbon and nutrients needed to form the flower stalk during the second year. Sprouting, which often occurs during prolonged storage, impairs the quality of the roots and increases water loss and decay. The propensity to sprout increases with storage duration and temperature, and cultivars vary in their susceptibility to sprouting. 5. Disorders Bitterness. Bitterness, caused by exposure of carrots to ethylene (as little as 0.5 µl ⋅ l–1) during storage, is quite common. The bitter compound is isocoumarin (8-hydroxy-3-methyl-6-methoxy-3,4-dihydroisocoumarin) (Carlton et al. 1961; Sarkar and Phan 1979), which is a phytoalexin synthesized by the tissue (Condon and Kuc 1960). Sources of ethylene range from other stored products and microorganisms to equipment driven by internal combustion engines. Isocoumarin synthesis is modulated by ethylene and oxygen concentrations, temperature, storage duration, and the maturity and physical condition of the roots (Lafuente et al. 1996). Preventive measures include exclusion of ethylene sources, appropriate ventilation, and low storage temperatures (Carlton et al. 1961). Splitting. Roots frequently split during growth, harvest, and storage, decreasing the value of the product (Millington 1984; Kokooras 1989; Vincent 1990). For example, 30% of the shipments (n = 2,425) of carrots arriving in New York over a 14-year period had significant numbers of

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broken or split roots (Cappellini et al. 1987). Splitting is caused by a combination of mechanical weakness and the water status of the tissues, with splitting being inversely proportional to the water content of the cells (McGarry 1993, 1995). A strain is created during water uptake when the expansion potential differs between neighboring cells (Sorensen and Harker 2000); as the root grows, the frequency of splitting increases (Hole et al. 1999). The susceptibility to splitting varies among cultivars, ranging from 3.8 to 73% (McGarry 1993; Hole et al. 1999). Discoloration. Surface browning may develop during storage, with immature carrots being more susceptible than mature (Chubey and Nylund 1970). Ozone treatment during storage can also decrease the orange coloration of the roots (Liew and Prange 1994). 6. Postharvest Pathology. Postharvest losses due to disease can be a serious problem. For example, eleven parasitic diseases were found in shipments of carrots to New York (Cappellini et al. 1987), with bacterial soft rot being the most prevalent, i.e., present in 33% of the shipments (n = 2,425). Factors that can influence the incidence of pathological losses during storage include the maturity of the roots at harvest (Suojala 1999), timing of harvest (Davies and Lewis 1980; Villeneuve et al. 1993; Suojala 1999), and weather conditions (humidity and precipitation) before and during harvest (Fritz and Weichman 1979; Villeneuve et al. 1993). The major storage fungi and bacteria of carrot are (a) fungi: black rot— Alternaria alternata (Fr.:Fr.) Keissler; black rot—Alternaria dauci (Kuhn) Groves & Skolko; black rot—Alternaria radicina (Meier); gray mold— Botrytis cinerea Pers.; sour rot—Geothichum candidum Link; licorice rot—Mycocentrospora acerina (Hartig) Deighton; cavity spot—Pythium spp.; violet root rot—Rhizoctonia crocorum DC. ex. Fr.; Rhizopus rot— Rhizopus spp.; watery soft rot—Sclerotinia sclerotiorum [(Lib.) De Bary]; Sclerotium rot—Sclerotium rolfsii Sacc.; black mold—Thielaviopsis basicola (Berk & Br.) Ferraris; and (b) bacteria: soft rot—Erwinia carotovora subsp. carotovora (Jones) Bergey et al.; soft rot—Erwinia carotovora subsp. atroseptica (van Hall) Dye, Blackleg; soft rot—Erwinia chrysanthemi pv. chrysanthemi Burkh., McFadden & Dimock; soft rot— Pseudomonas marginalis pv. marginalis (Brown) Stevens; soft rot— Pseudomonas marginalis pv. pastinacae (Burkh.) Young, Dye & Wilkie (Adams and Kropp 1996; Snowdon 1992; Thorne 1972). The infecting organisms vary with location and production conditions. In Israel, the fungi A. alternata, A. radicina, and S. sclerotiorum, and the bacterium E. carotovora subsp. carotovora can pose serious problems (Afek et al. 1998b). Several chemical treatments have been

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Table 7.6. Decay incidence (percentage) of organically grown carrots after storage (60 days at 0.5°C plus 7 days at 20°C) in retail (1 kg), wholesale (18 kg), and lined (15 kg) packages, following prestorage treatment with steam, fungicide (iprodione + chlorane), or neither, with (+) and without (–) inoculation with Alternaria alternata, A. radicina, Sclerotinia sclerotiiorum, and Erwinia carotovora (Afek et al. 1999b). Decay incidence (%) Prestorage treatment

Package type Wholesale

Inoc

Retail

Control

+ –

66 ez 23 d

Steam

+ –

9c 6c

7c 5 bc

5 bc 8c

Iprod+Chlor

+ –

5b 3 ab

3 ab 3 ab

3 ab 5 bc

61 e 25 d

Lining 71 e 21 d

z

Mean separation in columns by Fisher’s protected least significant difference test, (5% level).

tested (e.g., thiabendazole, iprodione, sodium-o-penylphenate); their use in individual countries depends upon government approval (Wells and Merwarth 1973). Among non-chemical treatments, a prestorage steam treatment has shown benefits (Afek et al. 1999b). After 60 days of storage at 0.5°C and 7 days poststorage at 20°C, steam-treated roots had much less spoilage than untreated controls (Table 7.6). 7. Chemical Changes During Storage. Mono- and disaccharides stored in the vacuoles account for 34–70% of the dry weight of carrot roots (Goris 1969; Ricardo and Sovia 1974; Nilsson 1987a). Sucrose is the dominant form at maturity (Daie 1984), however, its absolute concentration and its ratio to other sugars depend on cultivar and production conditions (Goris 1969; Phan and Hsu 1973; Ricardo and Sovia 1974; Nilsson 1987a; Suojala 2000). During storage, hexoses increase and sucrose declines, especially during the first months (Phan et al. 1973; Nilsson 1987b; Olden and Nilsson 1992; Le Dily et al. 1993). Under appropriate conditions, there are usually only minor changes in the total sugar content, but the sugar composition changes continuously throughout the storage period, irrespective of harvest date (Nilsson 1987b). C. Cassava Cassava (Manihot esculenta Crantz, Euphorbiaceae) is a primary or secondary food source for more than 500 million people in the tropics

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(Bokanga et al. 1994; Hillocks et al. 2002; Padmaja 1995) and is also used as animal feed (Gomez 1979). Worldwide production in 2001 was 189 million t (FAO 2002). Much cassava contains cyanogenic glucosides (principally linamarin and lotaustratin) that degrade to highly toxic hydrogen cyanide (HCN). The concentration of cyanogenic glucosides varies among cultivars, which are separated into bitter cassava, which contains high levels of the toxic glucosides throughout the storage roots, and sweet cassava, in which the much lower concentrations are confined largely to the peel. The terminology “bitter” vs. “sweet” is misleading, since it has nothing to do with the taste of the roots, and there is a continuum of glycosides concentrations across cultivars, from extremely low to extremely high. The roots, especially those of bitter cultivars, must be processed to remove the HCN, and properly treated cassava is a safe food source. Inadequate processing, however, can yield a toxic product, especially for the very young, elderly, and individuals with compromised health. A variety of detoxification methods are used, of which drying is the most common in many tropical countries, where cassava is traded as chips or pellets (Padmaja 1995). Sun drying eliminates more cyanide than oven drying because it prolongs the contact between linamarase and the glucosides. The most common technique used for dietary cassava involves mashing, squeezing, fermenting, and then roasting/drying. Soaking followed by boiling removes HCN better than either alone. The storage root is the most used plant part, though the young leaves are eaten as a green vegetable in many parts of the world. The storage roots are predominately carbohydrate (i.e., starch, 28–33% of fresh weight) and have a total dry matter content of 33–39%. The carbohydrate concentration varies with cultivar, stage of maturity, and growing conditions. The protein concentration of the roots is very low (0.4–0.6% of fresh weight) (Bradbury and Holloway 1988), therefore cassava is mainly a carbohydrate source. When used as a staple food, cassava often provides approximately one-half of the total dietary caloric intake (Rickard and Coursey 1981). 1. Prestorage Treatments Curing. Cassava roots can be cured by exposure to relatively high temperatures and humidities, a process that heals wounds and impedes the onset of vascular deterioration (Booth and Coursey 1974; Booth 1977). Curing promotes the development of meristematic tissue and suberization beneath the wound, as in other root crops. At 80–85% RH, meristem formation accelerates as the temperature increases from 25 to 40°C, but substantially more deterioration occurs at 40°C than at 35°C. At

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35°C a complete meristem is formed around cuts in 4–7 days, whereas at 45°C the roots do not heal and undergo rapid bacterial breakdown. When the roots were held at 95% RH, the wounds rapidly became infected by a wide range of pathogens, whereas at 75% RH they dried out rapidly, especially at wound sites (Booth 1974, 1976). Waxing. The effect of waxing on the storage life of cassava roots was first studied in the 1940s (Castagnino 1943) and the technique was subsequently refined. Dipping the roots in a fungicidal wax followed by storage at ambient temperatures substantially increased the storage potential (Subramanyam and Mathur 1956). Waxing approximately halved the weight loss during the first 2 weeks of storage and extended the useful storage time period (i.e., <10% loss) from 2 to 10 days. An increase in respiration was also delayed. The principal benefit of waxing seems to be derived from reduced moisture loss rather than the pathogen inhibition. Paraffin wax dips (90–95°C for 45 s) avert serious quality losses for 1–2 months (Anonymous 1972), ensuring sufficient time for export or storage (Burton 1970; de Buckle et al. 1973; Zapata 1978). Water-based carnauba and paraffin waxes are comparable in root quality maintenance (Sargent et al. 1995). 2. Recommended Storage Conditions. Without proper handling, fresh cassava deteriorates rapidly, often within 2–3 days, under tropical conditions, so that losses during storage and shipping can be a serious problem. Several means are available to extend the potential storage period; the choice depends upon the level of technology available and the relative value of the crop. Options include refrigerated, nonrefrigerated (e.g., boxes, pits, clamps), and field storage. Refrigerated Storage. Cassava can be effectively stored at 0–5°C, 85–90% RH for 1 to 2 months (Normanha and Pereira 1963; Averre 1967; Ingram and Humphries 1972). Storage potential depends significantly on the cultivar, production conditions, mechanical damage sustained during harvest and handling, and prestorage treatments. Czyhrinciw and Jaffe (1951) monitored changes in several properties of fresh cassava stored for 4 weeks at 3, 12, and 25°C. Storage resulted in a substantial reduction in vitamin C concentration by the 4th week of storage, as well as changes in peroxidase, dehydrogenase, and catalase activity, especially at 12°C. Roots stored for 2 weeks at 0–2°C showed no internal browning, but after 4 weeks a blue mold was observed that increased during subsequent storage (Singh and Mathur 1953). Above 4°C, the roots developed the same symptoms more rapidly

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Table 7.7. Effect of temperature and duration on the weight loss of cassava roots in storage (Singh and Mathur 1953). Weight loss (%) Storage temp. (°C)

1

2

3

0–2 2–4 4–6 6–8 8–10 11–13 19–21 22–30z

5.6 5.1 3.7 3.4 5.0 6.7 12.1 11.7

11.0 11.0 8.3 6.6 9.2 13.3 25.0 22.5

15.0 15.0 — — — — — —

Storage period in weeks 4 5 19.2 18.0 — — — — — —

21.7 21.7 — — — — — —

6

7

8

34.1 34.1 — — — — — —

37.5 40.3 — — — — — —

38.1 41.1 — — — — — —

z

ambient

and were unmarketable after only 2 weeks of storage. After 7 to 8 weeks, the weight loss in roots held at 0–2°C was somewhat lower than that at 2–4°C (Table 7.7). Nonrefrigerated Storage. Storage systems for fresh cassava roots include wooden buildings, bamboo and palm thatch buildings, cellars, pits, clamps, trenches, and boxes (Tracy 1903; Bayday 1922; Booth 1977; Rickard and Coursey 1981). Roots intended for storage should be harvested at the proper maturity, brushed cleaned (not washed), handled so as to minimize injury, and the surface air-dried before storage. Clamps are built by laying a bed of rice or other straw, 1–5 m in diameter, on dry ground and placing 300–500 kg of freshly harvested roots on it in a conical pile. The roots are covered with additional straw and then with soil, taken from around the clamp, so as to leave a drainage ditch. Various thicknesses of soil covering are used and basal or vertical ventilators may be inserted. Properly constructed clamps can preserve cassava roots for 1–2 months, with only modest desiccation and deterioration losses (Booth 1977; Rickard and Coursey 1981). The design of the clamp varies with the season, since it is important to maintain the internal temperature below 40°C. During the hot dry season, extra covering soil and ventilation are used. Even with such modifications results can be unsatisfactory (Booth 1976), so clamps have not been widely adopted for commercial storage (Lozano et al. 1978). Storage in boxes packed with moist sawdust or other material can be satisfactory. If the sawdust is too dry, the roots desiccate; if too moist,

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fungal and bacterial rots develop. Delays between harvesting and packing increase losses. If properly handled, about 90% of the roots, even of susceptible cultivars, are acceptable after 8 weeks of storage (Booth 1977; Sivan 1979; Rickard and Coursey 1981; Cooke et al. 1988). Moist coir dust (coconut husk) can be used in place of sawdust (Marriott et al. 1974) or the roots can be layered between fresh cassava leaves (Aiyer et al. 1978). A plastic box liner can prevent excessive drying of the packing material. The primary limitations to using boxes are the cost of the box and the labor required for packing. Nevertheless, storage boxes are used commercially for fresh cassava (Booth 1977; Rickard and Coursey 1981; Cooke et al. 1988). Cassava treated with a fungicide (thiabendazole) has been successfully stored in perforated polyethylene bags for 2–3 weeks in Colombia (Wheatley 1989). A similar technique has been less successful in Ghana (Bancroft and Crentsil 1995), where tightly woven fiber bags are used without a fungicide; the roots can be stored for only 7–10 days, which is generally sufficient for marketing in Ghana (Gallat et al. 1998). Field Storage. In technology-limited locations, such as on farms or in rural villages, cassava is either left unharvested (i.e., “stored” in the field) or processed into a dried product (Lancaster et al. 1982), to minimize losses. Roots stored in the ground continue to increase in size, often become fibrous and woody, and suffer a concurrent decline in starch content. It is difficult to hold freshly harvested cassava for even a few days. The poor storage life of the roots is a major weakness of the crop and forms an economic constraint in developing countries (Rickard and Coursey 1981). 3. Water Loss. In spite of the relatively thick periderm, the loss of moisture from the harvested roots is a serious problem that greatly aggravates losses due to pathogens. Moisture losses are particularly severe if the periderm is broken, which is unavoidable during harvest. Waxes, plastic bags, and film wraps have been used to reduce moisture loss. Although they all impede the outward diffusion of water vapor, they also impede respiration. Wrapping the roots in moist paper before placing them in plastic bags inhibits the development of vascular discoloration, especially below 10° or above 40°C (Averre 1967). A variety of polyethylene bags and sacks, and polyvinyl chloride cling and shrink films, have been tested on cassava (Oudit 1976; Thompson and Arango 1977; Lozano et al. 1978). Weight losses were considerably reduced by both film wraps and plastic bags, though perforated bags were less effective. Film-wrapped cassava showed signif-

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293

icantly reduced vascular streaking during storage, but the incidence of bacterial infection of the roots was greater than that in unwrapped controls. The use of plastics to impede water loss, particularly when combined with curing, antimicrobial treatments, and low-temperature storage, is effective. 4. Sprouting and Vascular Streaking. Sprouting of cassava storage roots requires the formation of adventitious buds. Due to the relatively short storage potential of cassava, sprouting is not a problem. Vascular streaking or discoloration is characterized by a dark bluish or blue-black discoloration of the vascular bundles; it usually starts at cut surfaces and progresses along the root, gradually becoming more prominent and turning brown or black over a few days (Castagnino 1943; Pacheco 1952; Drummond 1953; Normanha and Pereira 1963; Averre 1967; Montaldo 1973). The potential for vascular discoloration varies among cassava cultivars (Montaldo 1973). Initially faint blue streaks, caused by a darkening of areas within the xylem vessels and the formation of black occlusions within the vessels, develop near the surface. Discoloration subsequently spreads to neighboring parenchyma cells, where the structure of the starch grains changes (Drummond 1953). The disorder is thought to be enzymatically mediated and has been attributed to several enzymes (e.g., dehydrogenases, peroxidases, phosphorylases, and catalases (Czyhrinciw and Jaffe 1951; Murthy et al. 1956; Nair and Kurup 1963). The onset of vascular discoloration is closely associated with mechanical damage (Booth 1976) and there is a positive correlation between the degree of damage and the weight loss and deterioration (Rickard and Coursey 1981). The most severe damage typically occurs during harvest, at the point of attachment of the root to the parent plant. The damage and, therefore, discoloration, can be minimized by leaving a short segment of the stem attached to the root, a technique often used by farmers (Drummond 1953; Lozano et al. 1978). Avoidance of mechanical damage and proper cultivar selection retard development of the disorder and several treatments have been found effective. For example, hot water treatment (53°C for 45 min) or holding the roots under water or in anaerobic conditions inhibits development (Averre 1967). Low storage temperatures (0 or 5°C) also inhibited discoloration (Montaldo 1973). The particular importance of vascular discoloration is that it appears to predispose the roots to subsequent attack by many fungal and bacterial wound pathogens that cause a variety of wet and dry rots (Plumbley and Rickard 1991).

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5. Postharvest Pathology. The poor storage potential of cassava has long been recognized as one of the most critical deficits of the crop. Both fungal and bacterial rots play a major role in postharvest losses (Bayday 1922; Anonymous 1952; Majumder et al. 1956; Subramanyam and Mathur 1956; Normanha and Pereira 1963; Affran 1968; Oudit, 1976). Postharvest fungal pathogens include Botryodiplodia rot—Botryodiplodia theobrpmae Pat.; Fusarium rot—Fusarium solani (Mart.) Sacc.; Aspergillus rot—Aspergillus spp; Mucor rot—Mucor spp.; Phytophthora rot—Phytophthora spp.; dry rot—Rhizopus spp.; Sclerotium rot—Sclerotium rolfsii Sacc.; and Trichoderma rot—Trichoderma harzianum Rifai. Postharvest bacterial pathogens include soft rot—Erwinia carotovora subsp. carotovora (Jones) Bergey et al. and soft rot—Bacillus sp. (Plumbley and Rickard 1991; Snowdon 1992). Several chemical treatments for the control of postharvest pathogens have been tested. Fumigation with an ethylene dibromide/ethyl bromide mixture gave a maximum storage life of 19 days (Majumder 1955; Majumder et al. 1956) with bromide residues ranging from 13 to 19 ppm. Some reduction in postharvest pathogens was also achieved by using a 45 s dip in 1% sodium o-phenyl phenate with 900 ppm of 2,6 dichloro-4-nitroaniline followed by rinsing with water (Burton 1970). Manzate and sodium hypochlorite were also tested; manzate at 8 × 104 ppm a.i. inhibited the rotting of roots stored in polyethylene-lined paper bags (Lozano et al. 1978). Benomyl gave positive results in several studies (Booth 1976); it reduced surface fungal growth on roots stored within plastic films. Washing the roots with chlorinated water reduced bacterial soft rot, though neither treatment mitigated vascular streaking (Thompson and Arango 1977). Benomyl was also found to reduce the soft rot complex responsible for the later stages of decay of cassava (Ekundayo and Daniel 1973). Pathogen control measures must be initiated as soon as possible after harvest because their effectiveness decreases if the application is delayed. 6. Postharvest Entomology. Insect damage to stored fresh cassava is relatively uncommon, partly because of the short storage life. In dried cassava, however, losses to the larger grain borer (Prostephanus truncatus Horn.) have been reported in South America and Africa (Golob 1988; Hodges 1986). 7. Chemical Changes During Storage. The quality changes of cassava roots stored in moist sawdust and in clamps have been studied by Booth et al. (1976). Starch was rapidly converted to glucose, fructose, and sucrose, raising the original free sugar levels two- or threefold, during

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the first 2 weeks of storage. At the same time, the root tissue, especially the central portion, softened considerably.

V. CORM AND RHIZOME CROPS A. Taro Taro (Colocasia esculenta (L.) Schott, Araceae) is produced mainly in Nigeria, China, Ghana, Japan, the Ivory Coast, Papua New Guinea, Burundi, the Philippines, Egypt, and Madagascar (Wang and Higa 1983; Pardales 1987). World production is about 9 million t (FAO 2002). Two types of taro are usually recognized, distinguished by the way in which the corms are formed. In dasheen (Colocasia esculenta var. esculenta) there is a large edible main corm (e.g., cylindrical, about 30 × 15 cm) to which are attached a few lateral “cormels.” In eddoe (C. esculenta var. antiquorum), numerous edible cormels surround a small, bitter main corm. The names “eddoe” and “dasheen” are sometimes used interchangeably, which causes confusion since the two types differ in their postharvest characteristics, partly because of their differing structures. The harvested corm of dasheen carries several wounds after removal of the cormels and it sustains further injury if the basal portion is removed to provide propagation material (Snowdon 1992). The extensive wounding predisposes the corms to pathogen invasion. Eddoe cormels, in contrast, have only a single small wound, following separation from the mother corm. Furthermore, the cormels of certain cultivars of eddoe possess some degree of dormancy that confers additional storage life. Thus, eddoe may be stored for up to 3 months at ambient temperature, but dasheen is more perishable; in warm moist storage environments, dasheen corms cannot usually be held for longer than about a month without sprouting or decaying (Snowdon 1992). Passam (1982) reports a very much shorter postharvest life for both dasheen and eddoe. The corms and cormels, as well as the petioles and leaves, are consumed after cooking, a process that eliminates the acridity caused by calcium oxalate crystals (raphides) (Paull et al. 1999). 1. Prestorage Treatments. The corms/cormels may be exposed to warm (20–30°C) moist conditions to facilitate the curing of wounds incurred during harvest. High RH favors curing (Been et al. 1975), which minimizes the entry of disease-causing microorganisms. After curing, the product is room cooled to the appropriate storage temperature.

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2. Recommended Storage Conditions. Storage between 11 and 13°C, 80–95% RH can extend the longevity of the product significantly (i.e., up to 8 weeks) compared with that under ambient tropical conditions. At higher temperatures the corms perish rapidly; for example, in the Philippines corms are no longer fit for human consumption after 7 to 14 days in ambient conditions (27–32°C) because of microbial rotting (Quevedo and Ramos 1992). Taro is sometimes stored/shipped at temperatures lower than 11–13°C (e.g., 7–10°C, 80–95% RH for up to 18 weeks) but it must be consumed within a day or two after removal from refrigeration because the subsequent shelf life is significantly impaired. The corms are susceptible to chilling injury, the symptoms of which are surface pitting and an increased incidence of disease. 3. Weight Loss. Corms stored in clamps lost less weight than those stored in huts, because there was less evaporation and respiration. After 2 weeks of storage under ambient conditions, the weight losses of corms with intact roots and petiole, stored in a hut and in a clamp were 25 and 12%, respectively (Quevedo and Ramos 1992). 4. Postharvest Pathology. Decay of the corms is the most serious problem of taro during storage (Gollifer and Booth 1973; Passam 1982; Quevedo et al. 1992; Quevedo and Ramos 1992; Snowdon 1992). The following postharvest pathogens have been identified: (a) fungal pathogens include Botryodiplodia rot—Botryodiplodia theobromae Pat.; gray mold—Botrytis spp.; dry rot—Fusarium spp.; sour rot—Geothichum candidum Link; Phytophthora rot—Phytophthora colocasiae Racib.; Pythium rot—Pythium spp.; Rhizoctonia rot—Rhizoctonia solani Kuhn; dry rot—Rhizopus spp.; Rosellinia rot—Rosellinia bunodes (Berk & Br.) Sacc.; Sclerotium rot—Sclerotium rolfsii Sacc.; black rot—Thielaviopsis spp.; pink mold rot—Trichothecium roseum Link; and (b) bacterial: soft rot caused by Erwinia sp. (Gollifer and Booth 1973; Passam 1982; Quevedo and Ramos 1992; Quevedo et al. 1992; Snowdon 1992). Several prestorage treatments for the control of storage pathogens have been tested. For example, dipping the roots in hot water (50°C) containing 200 ppm (a.i.) benomyl for 5 min reduced storage decay. After 2 weeks under ambient conditions, only 12% of the treated corms were lost compared with 65% for the controls (Quevedo et al. 1992). Corms from which the shoot apices and petiole bases had been removed had a shorter storage life than untreated ones (Wilson 1983); decay incidence was lower in the latter corms and was less still when they were stored in clamps (lower temperature and higher relative humidity). After 2

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weeks, corms stored in clamps suffered only 6% losses vs. 22% among those in huts (Quevedo and Ramos 1992). B. Ginger Ginger (Zingiber officinale Rosc., Zingiberaceae) is grown for its underground rhizomes that are used raw (green) or processed as an aromatic condiment. A significant portion of the crop is processed, generally preserved in a brine solution or sugar syrup or as a dried product (Vasala 2001). The world production in 2001 was 835,000 t (FAO 2002), with India and China the leading producers. The unique aroma of ginger is due to a complex mixture of monoterpenes and sesquiterpenes (Govindarajan 1982a,b), with the dominant odorant being 6-gingerol (Connell and Sutherland 1969). The best rhizomes are those that are harvested immediately after they mature, i.e., when the above-ground plant parts die (Akamine 1962). Premature or delayed harvest increases postharvest losses. Factors that decrease the quality of the ginger during storage include surface shriveling and weight loss due to desiccation, decay, physiological breakdown, sprouting, and discoloration. 1. Prestorage Treatments. After harvest, the rhizomes are washed, air dried, and cured at 20°C, 70% RH for 7 days, after which they are cooled to the appropriate storage temperature using forced-air or room precooling. 2. Recommended Storage Conditions. Mature ginger rhizomes can be stored for 2–3 months at 12–14°C, 85–90% RH with only minor losses. Losses due to chilling injury and sprouting are avoided at this temperature range. Lower RH (e.g., 65%) results in excessive dehydration and a diminished appearance (Akamine 1962). Storage in polyethylene bags is not recommended because the high humidity increases sprouting, the development of fibrous roots, rotting, and discoloration. When refrigerated storage is not available, the rhizomes can be stored in pits covered with sand or dry grass in a shaded barn (Oti et al. 1988), but their maximum longevity is substantially less than under refrigeration. 3. Water Loss. Storage at a high relative humidity (i.e., 85–90%) is essential for preventing desiccation; rhizomes held at 65% RH lost approximately 16% of their water content in 6 months (Akamine 1962). Low RHs result in excessive moisture loss, while very high RHs promote pathogen attack. Moisture is readily lost from cut surfaces, so proper

298

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curing is essential. Waxing does not appear to impede water loss, and the beneficial effects of polyethylene bags in decreasing desiccation are negated by increased decay (Akamine 1962). 4. Sprouting. At 21°C, 65% RH, sprouting limits the maximum storage potential of the rhizomes to about 1 month. Preharvest application of maleic hydrazide and postharvest application of CIPC reduced sprouting (Paull et al. 1988b), as did exposure to ionizing radiation (gamma or X-rays) (Mukherjee et al. 1995; Paull et al. 1988b). Excessively high exposures increase pathogen development (Akamine 1962). 5. Disorders Chilling Injury. Exposure of the rhizomes to temperatures below 10°C results in chilling injury. Rhizomes that have been chilled soften and shrivel more readily. The degree of damage is a function of the temperature to which the rhizomes were exposed and the duration of exposure. For example, 2–3 wks storage at or below 7°C seriously damages the rhizomes (Akamine 1962). Physiological breakdown of the rhizomes is enhanced by exposure to chilling. Rhizomes that have been frozen readily degrade upon thawing. Discoloration. Stored rhizomes may develop a purple discoloration on the cut surfaces, and possibly also, to a lesser degree, on the intact surfaces (Akamine 1962). Pigment development appears to be related to the presence of free moisture on the surface of the rhizomes, and storage in plastic bags accentuates the problem. 6. Postharvest Pathology. Many storage disease organisms attack ginger. They include Fusarium rot—Fusarium spp., Pythium rot—Pythium spp., Armillaria rot—Armillaria mellea (Vahl:Fr) Kummer, bacterial soft rot—Erwinia carotovora ssp. carotovora (Jones) Bergey et al., bacterial wilt—Pseudomonas solanacearum (E. F. Sm.) E. F. Sm., black rot— Memnoniella echinata (Rev.) Gall., blue mold rot—Penicillium spp., Botryodiplodia rot—Botryodiplodia theobromae Pat., charcoal rot— Macrophomina phaseolina (Tassi) Goid, gray rot—Trichurus spiralis Hasselbr., red rot—Nectria inventa Pethybr., Rosellina rot—Rosellinia bunodes (Berk and Br.) Sacc., and Sclerotium rot—Sclerotium rolfsii Sacc. (Snowdon 1992). Benomyl has been shown to decrease rotting (Okwuowulu and Nnodu 1988) and an antagonistic microorganism (an isolate of Trichoderma) was found to suppress the growth of Sclerotium rolfsii (Mukherjee et al. 1995). Treatment of the rhizomes with hot water,

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sodium hypochlorite, and low-oxygen storage atmospheres each failed to control storage pathogens (Akamine 1962). Postharvest pathogens are best controlled by storing the rhizomes at the recommended temperature and RH. 7. Chemical Changes During Storage. The chemical composition of rhizomes stored at 12.5°C for 32 weeks remained remarkedly stable, with the exception of their gingerol concentration, which increased fivefold (Paull et al. 1988a). Fiber, oil, total phenolics, and protein concentrations did not change significantly, though the color of the rhizomes darkened from a very light yellow at harvest to a grayish yellow after 2 months. The concentration of total sugars increased on a fresh weight basis, but only after extended storage (28 weeks).

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8 Metabolic Control of Low-Temperature Sweetening in Potato Tubers During Postharvest Storage R. W. Blenkinsop, R. Y. Yada, and A. G. Marangoni Department of Food Science University of Guelph Guelph, Ontario, Canada N1G 2W1

I. INTRODUCTION II. STARCH METABOLISM A. Starch Synthesis B. Starch Degradation C. Starch-Sucrose Interconversion III. SUCROSE METABOLISM A. Sucrose Synthesis B. Sucrose Degradation C. Futile Carbon Cycling IV. GLYCOLYSIS V. OXIDATIVE PENTOSE PHOSPHATE PATHWAY VI. MITOCHONDRIAL RESPIRATION VII. METABOLIC FACTORS AFFECTING CHIP COLOR DEVELOPMENT VIII. CONCLUSION LITERATURE CITED

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LIST OF ABBREVIATIONS ADP-Glc ADP AGPase ATP ATP-PFK Fru-1,6-P2 Fru-2,6-P2 FBPase Fru-6-P Glc-1-P Glc-6-P G6PDH LTS NADH NADPH PEP 3-PGA 6PGDH PGM PHI PK PPi PPi-PFK PPP RNA SPS Suc-6-P S6PTase SuSy UDP-Glc UGPase

adenine diphosphate glucose adenosine diphosphate ADP-glucose pyrophosphorylase adenosine triphosphate ATP-dependent phosphofructokinase fructose-1,6-bisphosphate fructose-2,6-bisphosphate fructose-1,6-bisphosphatase fructose-6-phosphate glucose-1-phosphate glucose-6-phosphate glucose-6-phosphate dehydrogenase low-temperature sweetening nicotinamide adenine dinucleotide (reduced form) nicotinamide adenine dinucleotide phosphate (reduced form) phosphoenolpyruvate 3-phosphoglyceric acid 6-phosphogluconate dehydrogenase phosphoglucomutase phosphohexose isomerase pyruvate kinase pyrophosphate pyrophosphate-dependent phosphofructokinase oxidative pentose phosphate pathway ribonucleic acid sucrose-6-phosphate synthase sucrose-6-phosphate sucrose-6-phosphate phosphatase sucrose synthase uridine diphosphate glucose UDP-glucose pyrophosphorylase

I. INTRODUCTION Following exposure to low temperatures (i.e., <9–10°C), tubers of potato (Solanum tuberosum) undergo a phenomenon known as lowtemperature sweetening (LTS) (Burton 1969; ap Rees et al. 1981; Coffin et al. 1987). This process occurs in various parts of higher plants exposed

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to lower than optimum growth or storage temperatures, and, in stored potato tubers, results in the accumulation of starch breakdown products, primarily sucrose (Suc) and the reducing sugars glucose (Glc) and fructose (Fru) (ap Rees et al. 1981). Sugar accumulation associated with LTS in potato tubers develops within a few days of transfer/exposure to cold (Pollock and ap Rees 1975; Coffin et al. 1987; Hill et al. 1996). Factors other than low temperature are also known to cause sugar accumulation in potato tubers, including drought, excess nitrogen during growth, increased temperature at harvest, handling, aging, and anaerobic conditions during storage (Sowokinos 1990a). High levels of reducing sugars accumulated from starch reserves in cold-stored potato tubers lead to undesirable Maillard browning during potato chip frying operations, resulting in the production of dark-colored chips that are unacceptable to the consumer due to their appearance and bitter taste (Burton 1969; Roe et al. 1990). Therefore, processing potatoes are generally stored at temperatures around 10°C in order to maintain low levels of sugars during long-term storage. At this storage temperature, potato tubers will sprout. Thus, to prevent sprouting during storage, the tubers are treated with dormancy-prolonging chemicals (sprout inhibitors). Due to health and environmental concerns among consumer groups, there is increasing pressure to reduce this practice. In recent years, there has been great interest in the development of potato cultivars that can process with an acceptable chip color directly from low temperature storage (e.g., 4°C). Advantages to storing tubers at low temperature include natural control of sprout growth, minimization of physiological weight loss (i.e., H2O and dry matter) due to decreased respiration, and a reduction in losses associated with bacterial and fungal pathogens (Burton 1969). Thus, the ability to store potato tubers at low temperature long-term would alleviate environmental and consumer concerns regarding the use of chemicals for the prevention of sprouting and the control of storage pathogens. Despite the many advantages of low temperature storage, the associated hexose accumulation in most cultivars is a major drawback, as this results in potato tubers that are unsuitable for processing. The mechanism(s) responsible for the initiation and subsequent regulation of the LTS process in potato tubers remain to be fully elucidated. The accelerated accumulation of sucrose, fructose, and glucose that occurs during LTS is an extremely complex process, involving the interaction of a number of pathways of carbohydrate metabolism, including starch degradative and synthetic pathways, sucrose synthesis and degradation, glycolysis, the oxidative pentose phosphate pathway (PPP), and mitochondrial respiration (Fig. 8.1) (Sowokinos 1994; Wismer et al.

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Fig. 8.1. A generalized scheme of the reactions involved in starch-sugar interconversion in potato tubers. Adapted from Duplessis et al. (1996) and Sowokinos (2001a). Note that both cytochrome-mediated and alternative pathway respiration occur in the mitochondrion. AcInv (acid invertase); ADP-Glc (ADP-glucose); AGPase (ADP-glucose pyrophosphorylase); Fru-6-P (fructose-6-phosphate); Glc-1-P (glucose-1-phosphate); Glc-6-P (glucose-6-phosphate); PEP (phosphoenolpyruvate); PGM (phosphoglucomutase); PHI (phosphohexose isomerase); SPS (sucrose phosphate synthase); Suc-6-P (sucrose-6phosphate); S6PTase (Suc-6-P phosphatase); UDP-Glc (UDP-glucose); UGPase (UDPglucose pyrophosphorylase).

1995). In addition to carbohydrate metabolism, electrolyte leakage and membrane lipid peroxidation have also been implicated in LTS (Workman et al. 1979; Sowokinos 1990a; Spychalla and Desborough 1990; Wismer et al. 1998). Fine metabolic control exerted by allosteric enzymes, coarse metabolic control due to enzyme induction, and intracellular transport of metabolites may all play a role in the observed metabolic response to low temperature stress (Marangoni et al. 1996). A phenomenological kinetic model of carbohydrate metabolism in potato tubers stored at 2°C, describing starch degradation to sucrose, reducing sugars, and carbon dioxide in mature, cold-stored potato tubers (Marangoni et al. 1997), suggests that glycolytic/respiratory capacity plays a key role in the ability of a potato to regulate its tissue sugar concentration. Although it remains to be elucidated at the molecular level,

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the mechanism by which cold stress influences cellular regulation may involve one or more of the following: (1) hormones; (2) membrane structure and function; (3) compartmentalization and concentration of particular ions, substrates, enzymes and other effectors; and (4) enzyme synthesis and activity (Sowokinos 1990a). Carbohydrate metabolism in both developing and stored potato tubers is well documented and many differing theories have been postulated to explain the LTS phenomenon (reviewed in ap Rees et al. 1981; Sowokinos 1990a,b; Wismer et al. 1995; Sowokinos 2001b). This review focuses on the roles of the major metabolic pathways of tuber carbohydrate metabolism in response to low temperature stress during postharvest storage, evaluating a number of the proposed mechanisms of LTS. Emphasis is placed on research concerning the effects of low temperature storage on the pathways of starch synthesis, starch breakdown, sucrose synthesis, hexogenesis, glycolysis, the PPP, and mitochondrial respiration. The metabolic factors contributing to chip color development will be discussed in a later section of this review.

II. STARCH METABOLISM In potato tubers, starch is considered to be the main source of carbon for the synthesis of sugars during sweetening at low temperatures (Isherwood 1973, 1976). The sugars accumulated represent only a fraction of the starch present (Isherwood 1973). On a dry weight basis, potato tubers contain 60 to 80% starch (Burton 1966), whereby 21 to 25% of this starch is amylose and 75 to 79% is amylopectin (van Es and Hartmans 1981). The sugar content of potato tubers is markedly affected by growing conditions, maturity, and storage temperature; in mature tubers stored at low temperature, the reducing sugar concentration may accumulate to levels exceeding 2.0% of tuber fresh weight (Isherwood 1973). An ideal reducing sugar content for chipping is generally accepted to be 0.1% of tuber fresh weight, with 0.3% as the upper limit (Burton and Wilson 1970; Davies and Viola 1992). A. Starch Synthesis Starch synthesis is localized in the amyloplasts of potato cells (Fig. 8.1), and is catalyzed by the concerted action of ADP-glucose pyrophosphorylase (AGPase) and the isoforms of starch synthase and starch branching enzyme (Smith et al. 1997). Following the conversion of sucrose into hexose-phosphates in the cytosol, glucose-6-phosphate (Glc-6-P) is

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transported into the amyloplast (Schott et al. 1995; Kammerer et al. 1998; Tauberger et al. 2000), where it is converted to glucose-1phosphate (Glc-1-P) by phosphoglucomutase. Glc-1-P is subsequently converted to ADP-glucose (ADP-Glc) via the reaction catalyzed by AGPase. The starch synthases catalyze the polymerization of the glucose monomers into α-1,4-glucans using ADP-Glc as a substrate, while the starch branching enzyme catalyzes the formation of the α-1,6-linkages of amylopectin (Smith et al. 1997). Classically, AGPase is considered to be a key regulatory step in the synthesis of starch (Preiss 1988; Smith et al. 1997). In both potato leaves and tubers, this enzyme is under allosteric regulation, activated by 3phosphoglyceric acid (3-PGA) and inhibited by inorganic phosphate (Pi) (Sowokinos and Preiss 1982; Preiss 1988). There is evidence that changes in 3-PGA concentrations in potato tuber discs are strongly correlated with the levels of ADP-Glc and the rate of starch synthesis in discs of wild-type tubers under a range of environmental conditions (water deficit, heat stress) (Geigenberger et al. 1997, 1998). This not only suggests that 3-PGA may potentially be a physiological regulator of AGPase in potato tubers, but that AGPase exerts control over the starch biosynthetic flux. Antisense and overexpression techniques to alter AGPase have been performed in an attempt to study the role of AGPase in the control of starch synthesis. Transgenic tubers with an 80–98% reduction in the activity of AGPase have been observed to have a dramatically reduced starch content relative to wild-type tubers (Müller-Röber et al. 1992; Sweetlove et al. 1999). The reduction in AGPase activity resulted in a major redirection of carbon flux, with increased flux to sucrose and decreased flux to starch (Sweetlove et al. 1999). A bacterial form of AGPase (glgC16 from Escherichia coli) that is less sensitive to allosteric regulation has been overexpressed in potato tubers and was observed to increase rates of starch synthesis (Stark et al. 1992; Sweetlove et al. 1996a,b) and increase the maximum catalytic activity of AGPase (Sweetlove et al. 1996a,b), suggesting an important regulatory role for this enzyme in controlling carbon flux into starch. However, evidence from radiolabeling studies using 14C-sucrose suggests that the increased synthesis is accompanied by an increased breakdown of starch (Sweetlove et al. 1996b), such that at most, minor changes in starch accumulation are observed (Stark et al. 1992; Sweetlove et al. 1996b). Strategies designed to alter starch metabolism in tubers may be successful in reducing the concentration of hexoses in cold-stored potato tubers. Stark et al. (1996) revealed that hexose accumulation was greatly reduced in cold-stored tubers with overexpression of the glgC16 AGPase gene from E. coli. The reason for the observed decrease in hexose con-

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centrations is thought to be the higher starch biosynthetic capacity of the transgenic tubers. Lorberth et al. (1998) developed transgenic plants with decreased levels of R1 protein, a starch granule-bound protein capable of introducing phosphate into starch-like glucans. By reducing the activity of the R1 protein using antisense technology, the phosphate content of the potato starch was reduced, resulting in a starch that was less susceptible to degradation at low temperatures relative to the starch of wild-type tubers. Following two months of storage at 4°C, the transgenic tubers contained lower (up to nine-fold) concentrations of reducing sugars (Lorberth et al. 1998). The authors did not explore how modifying the starch composition may affect potato processing quality. However, as Greiner et al. (1999) suggest, such a modification is of limited value if either the quality or quantity of starch is altered. B. Starch Degradation Starch mobilization occurs within the amyloplast and is mediated by a number of enzymes, including α-amylase (endoamylase), β-amylase (exoamylase), α-glucosidase and α-glucan phosphorylase (starch phosphorylase) (Steup 1988). These starch-degrading enzymes are also present in the cytosol. The hydrolytic cleavage of internal α-1,4-glucan bonds is catalyzed by α-amylase, while β-amylase catalyzes the cleavage of maltose from the nonreducing end of an α-glucan. An additional hydrolytic enzyme, α-glucosidase, catalyzes the cleavage of α-1,4 or α1,6 bonds in maltose and other oligosaccharides to produce glucose. Starch phosphorylase is responsible for the formation of Glc-1-P and a 1,4-α-glucan from amylose and orthophosphate (Steup 1988). The degradation of starch in cold-stored potato tubers is thought to occur mainly via starch phosphorylase (Morrell and ap Rees 1986a; Sowokinos 1990b; Davies and Viola 1992; Claassen et al. 1993), although amylases may have an important supportive role as shown by increases in their activities in cold-stored tubers (Cochrane et al. 1991; Cottrell et al. 1993). Starch breakdown is thought to be mainly phosphorolytic because: (1) sucrose is the first sugar to accumulate upon transfer of the tubers to chilling temperatures (Isherwood 1973); (2) amylase activities are considered too low to catalyze the required rate of starch degradation (Morrell and ap Rees 1986a); and (3) no increases in either maltose nor polymers of glucose larger than maltose, the common products of amylolytic starch degradation (Preiss and Levi 1980), have been observed during sweetening at low temperatures (Isherwood 1973; Zhou and Solomos 1998). However, there is evidence from other studies indicating that the observed changes in starch phosphorylase activity in response to changes in temperature are subtle (Kennedy and Isherwood 1975; Morrell and ap

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Rees 1986a), occur after sucrose has started to accumulate (Claassen et al. 1993), or that phosphorylase activity does not change (Hill et al. 1996). Davies (1990) concluded that there was little convincing evidence that starch breakdown in potato tubers during LTS is accompanied by increases in either phosphorolytic or amylolytic activity. Using clones containing antisense constructs of starch phosphorylase, Kumar et al. (2000) demonstrated that the activities of the cytosolic and plastidic isozymes of starch phosphorylase were reduced by up to 70%. However, this transformation did not affect the accumulation of reducing sugars during 4°C storage. Furthermore, no correlation was found between starch phosphorylase activity and reducing sugar levels in clones displaying a wide range in susceptibility to LTS. Recent studies on tubers of the cultivar Desirée (Hill et al. 1996; Nielsen et al. 1997; Deiting et al. 1998) have demonstrated that the onset of sugar accumulation during low temperature storage coincides with an increase in the activity of one specific isoform of amylase, and thus suggests that this cold-induced amylase isoform may contribute to cold sweetening. Using zymograms, Hill et al. (1996) separated the isoforms of amylase and found that the onset of sugar accumulation in Desirée tubers coincided with the appearance of a new amylase band between 2 and 4 days of storage at 4°C. In contrast to other studies (Morrell and ap Rees 1986a; Claassen et al. 1993), there was no change in the activity or banding patterns of starch phosphorylase. As a continuation of this study, Nielsen et al. (1997) separated the cold-induced amylase isoform from the other amylolytic activities. They demonstrated that the coldinduced amylolytic activity observed by Hill et al. (1996) represented a β-amylase, as confirmed by identification of the hydrolysis product as maltose. This β-amylase isoform was present at low activity in tubers stored at 20°C, and increased 4- to 5-fold within 10 days of storage at 3°C. In addition, Nielsen et al. (1997) noted that the activities of α-glucosidase and α-amylase were not affected by low storage temperature. The results of Nielsen et al. (1997) and subsequently Deiting et al. (1998) provide evidence of a correlation between the appearance of a cold-induced β-amylase isoform and cold sweetening, suggesting that starch degradation in potato tubers is not exclusively phosphorolytic. However, a specific role for this cold-induced isozyme in cold sweetening has not been established. It is evident that studies concerning the effect of low temperature storage on the activities of tuber starch-degrading enzymes have provided contradictory results. These inconsistencies may be attributed in part to differences among cultivars. Additionally, a complicating factor in the measurement of starch-degrading enzymes is the presence of multiple isoforms (Beck and Ziegler 1989). Consequently, changes in the activity

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of one isoform may be obscured in overall measurements for a given enzyme, due to the presence of multiple isoforms with overlapping activity. As Nielsen et al. (1997) have noted, the assays used to measure amylase activities in some studies do not always fully distinguish between α- and β-amylase activity (e.g., Sowokinos et al. 1985), and/or will not detect separately the activities of individual isoforms of each of these amylases. This complicates the interpretation of previous experiments in which amylases have not been separated and characterized. Research to date suggests that starch phosphorylase alone is not responsible for the regulation of starch degradation, while similarly, a complete amylolytic degradation of starch to glucose is not likely. It would seem probable that starch degradation is due to the concerted action of these enzymes. C. Starch-Sucrose Interconversion In stored tubers, pathways of starch synthesis and breakdown occur simultaneously, and the net flux of carbohydrate is thought to be regulated by fine control mechanisms (Davies and Viola 1994). There is strong evidence that Glc-6-P is transported into the amyloplast of potato tubers to support starch synthesis (Schott et al. 1995; Kammerer et al. 1998; Tauberger et al. 2000). Thus, the pathways of both starch and sucrose biosynthesis compete for the same pool of precursors. While a net flux of carbon from starch into sucrose occurs in coldstored tubers, radiolabeling experiments have shown that the capacity for starch biosynthesis is still present. Viola and Davies (1994) found that in potato discs incubated with 14 C glucose at 3° and 15°C, a large proportion of label is recovered in starch. At low temperature, the ratio of 14 C recovered in sucrose to that recovered in starch increased in a coldsensitive (high sugar-accumulating) cultivar but was unaffected in a cold-tolerant (low sugar-accumulating) cultivar. Davies and Viola (1992) suggest that genotypic variation in the capacity to maintain an active starch synthesizing system may play a role in determining the rate of sucrose accumulation. The loss of starch synthesizing potential may indicate the onset of the irreversible senescent sweetening process (Davies and Viola 1992). III. SUCROSE METABOLISM A. Sucrose Synthesis The hexose phosphates produced from the mobilization of starch by phosphorolytic and amylolytic activity are exported from the amyloplast to the cytosol via a phosphate translocator that accepts hexose

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phosphates (Schott et al. 1995; Kammerer et al. 1998; Tauberger et al. 2000). Subsequently, the hexose phosphates are converted to sucrose primarily via UDP-glucose pyrophosphorylase and sucrose phosphate synthase (SPS) (Pollock and ap Rees 1975). Sucrose synthesis may also be catalyzed by sucrose synthase (SuSy). SPS catalyzes the reaction of UDP-glucose (UDP-Glc) and fructose-6-phosphate (Fru-6-P) to produce sucrose-6-phosphate (Suc-6-P), which is then converted to sucrose by sucrose phosphatase. SuSy produces sucrose via the conversion of UDPGlc and Fru to form Suc and UDP. Both SPS and SuSy are cytosolic enzymes that catalyze freely reversible reactions in vitro. However, the rapid removal of Suc-6-P by a high-activity sucrose phosphatase keeps the cytosolic concentration of Suc-6-P low and thus renders the SPS reaction essentially irreversible in vivo, in the direction of sucrose synthesis (Huber and Huber 1996). SPS plays an important role in the biosynthesis of sucrose in a wide variety of plant tissues. Sucrose is the major transport form of carbon in most plants, and as such, SPS is present at high activities in source tissues (e.g., mature leaves, germinating seeds) (Huber and Huber 1996). It is also found in sink tissues, where it is thought to contribute to a number of important processes, including the accumulation of sucrose in the cold (Guy et al. 1992) and regulation of sucrose import and breakdown via a futile cycle of synthesis and degradation (Dancer et al. 1990; Geigenberger and Stitt 1991, 1993). SuSy catalyzes a near-equilibrium reaction in vivo (Geigenberger and Stitt 1993; Geigenberger et al. 1994) and thus can participate in sucrose synthesis or degradation. The activity of SuSy has been shown to be substantially lower in stored tubers relative to developing tubers (Pressey 1970; Ross and Davies 1992; Geigenberger and Stitt 1993). Geigenberger and Stitt (1993) reported that SuSy activity in stored tubers decreased 87% relative to growing tubers, while SPS activity increased by 44%. Therefore, it is not surprising that in contrast to SPS, the role of SuSy in sucrose accumulation in tubers stored at low temperatures is relatively minor. Substantial evidence from a number of studies suggests that SPS is the primary enzyme of sucrose biosynthesis in cold-stored potato tubers. Pressey (1970) observed that SPS activity in tubers stored at 4°C was substantially greater than that of SuSy and that the changes in SPS show much better correlation with sugar accumulation. In fact, tuber SPS activity exceeded that of SuSy regardless of storage temperature (4° or 18°C). Pollock and ap Rees (1975) reported that sucrose synthesis during cold sweetening is catalyzed by SPS and not by SuSy, but is not due to changes in the maximum catalytic activities of these enzymes. The

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suggestion that SPS is the enzyme responsible for sucrose formation in cold-stored potatoes has been confirmed by 13C NMR (Viola et al. 1991). A good measure of the relative contributions of SPS and SuSy to sucrose synthesis during low temperature storage is through radiolabeling studies (using 14C glucose and 14C fructose). The formation of sucrose by SuSy leads to asymmetrical labeling of the glucosyl and fructosyl moieties of sucrose, due to the fact that the glucosyl units are derived from the pool of phosphorylated intermediates, while the fructosyl units are derived from free sugars (Geigenberger and Stitt 1993). Results reported by Hill et al. (1996) indicate that the ratio of radiolabeled carbon (14C) in the glucosyl moiety to that of the fructosyl moiety was very close to 1:1 throughout the duration of storage at 4°C. This provides strong evidence that SPS is responsible for the increased rate of sucrose synthesis in cold-stored tubers, and confirms previous observations that the activity of SuSy is low in stored tubers (Pollock and ap Rees 1975). SPS from potato tubers has been shown to be subject to fine regulation by allosteric effectors and protein phosphorylation (Reimholz et al. 1994), much like leaf SPS (Huber and Huber 1991). Potato tuber SPS is allosterically activated by Glc-6-P and inhibited by inorganic phosphate (Pi) (Reimholz et al. 1994). These effectors are responsible for the changes in the affinity of SPS for its substrates UDP-Glc and Fru-6-P. Phosphorylation leads to a lowering of the substrate affinity of the enzyme, and hence a decreased rate of sucrose synthesis. Dephosphorylation results in activation of the enzyme and increased sucrose accumulation. Earlier studies of sucrose synthesis in potato tubers indicate that SPS activity did not increase when potato tubers were introduced to cold temperatures (Pollock and ap Rees 1975; Sowokinos et al. 1985). In a species survey (Sowokinos 1990a), high SPS activity was correlated with sugar accumulation at 9°C. However, in the same study, there was no substantial evidence for an increase of SPS activity following transfer to low temperatures. The increase in SPS at 3°C was very gradual, with SPS activity diverging from that at 9°C, but only after 4 months. After 8 months of 3°C storage, only 4 of 7 cultivars evaluated showed an increase in SPS activity relative to 9°C storage. More recent results from a number of related studies (Hill et al. 1996; Reimholz et al. 1997; Deiting et al. 1998; Krause et al. 1998) have suggested that cold-induced alterations in the kinetic properties of SPS play an important regulatory role in starch-sugar conversion in coldstored potato tubers. Similar to previous studies, Hill et al. (1996) determined that the maximum activity of SPS and the total amount of SPS protein did not change following the transfer of Desirée tubers to 4°C. A

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notable change in the kinetic properties of SPS was observed after 2– 4 days at 4°C, with an increased affinity for its substrates and a decreased sensitivity to inhibition by phosphate. This was accompanied by a 2-fold decline in hexose-phosphates as well as a 3- to 4-fold stimulation of sucrose synthesis (Fig. 8.2) (Hill et al. 1996). It is possible that the change in kinetic properties may have been due to dephosphorylation of the enzyme. The activation of sucrose synthesis upon transferring tubers to low temperature has also been associated with the increased expression of a 127 kDa isoform of SPS (SPS-1b), which has a slightly higher molecular weight than SPS-1a (125 kDa), the major isoform found in tubers stored at room temperature (i.e., 20°C) (Reimholz et al. 1997; Deiting et al. 1998). The cold-induced increase in the SPS-1b isoform was found to correlate well with the change in the kinetic properties of the enzyme. Reconditioning of the tubers at 20°C resulted in the disappearance of this coldinduced SPS isoform after 2–4 days (Deiting et al. 1998). An increase in the amount of SPS transcript was also observed at low temperature in each of these studies. To further investigate the regulatory role of SPS on sugar accumulation in cold-stored tubers, Krause et al. (1998) conducted experiments on transgenic tubers with 65–80% reduced expression of SPS. Their results show that cold sweetening is reduced in transformants in which an increase in the cold-induced SPS isoform is prevented. A 70–80% decrease of SPS expression resulted in a reproducible but nonproportional decrease of soluble sugars in cold-stored tubers. Krause et al. (1998) also observed that the Vmax of SPS was 50 times higher than the net rate of sugar accumulation in wild-type tubers, and determined that SPS is strongly substrate limited, particularly for UDP-Glc. These results confirm that the rate of cold sweetening in wild-type tubers is not strongly controlled by the overall SPS activity or the overall amount of SPS protein. Alterations in the kinetic properties of SPS, which occur in response to low temperature, were more effective in stimulating sucrose synthesis than changes in SPS expression. Therefore, there is evidence of a regulatory role for SPS in sugar accumulation at low temperature. The observation that changes in the kinetic properties of potato tuber SPS coincide with the onset of sucrose accumulation implies that the fine regulation of SPS may be more critical than coarse regulation in controlling the relative ability of a given cultivar to sweeten in storage. However, SPS is likely not the only step at which sugar accumulation at low temperature is regulated. For instance, enzymes that influence the levels of hexose phosphates and UDP-Glc likely also play an important role in regulating the levels of sucrose in cold-stored potato tubers.

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Fig. 8.2. Levels of sucrose (a) and hexose phosphates (b–d) in tubers stored at 4°C (•–•) and 20°C ( -- ). These results illustrate the relationship between the levels of sucrose and hexose phosphates during the first 10 days of the storage experiment. Adapted from Hill et al. (1996).

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UDP-glucose pyrophosphorylase (UGPase) is a cytosolic enzyme that catalyzes the first step committed to the sweetening pathway in potato tubers, via the formation of UDP-Glc. This enzyme regulates the reversible reaction in which glucose-1-phosphate (Glc-1-P) and UTP are converted to UDP-Glc and PPi. Depending on the physiological state of the tubers (i.e., growth or postharvest storage), the UGPase reaction may be directed toward the synthesis of Glc-1-P (starch synthesis) or UDPGlc (starch degradation) (Sowokinos 1994). During the process of cold sweetening, it has been suggested that UDP-Glc and PPi (products of the UGPase reaction in the sucroneogenic direction) have regulatory roles in directing carbon flux into the pathways of glycolysis, starch synthesis and/or hexose formation (Sowokinos 1990b; Jelitto et al. 1992). The activity of this enzyme has been shown to be correlated with the amount of glucose that tubers of diverse genotypes accumulate in cold storage (Sowokinos 1990a), leading to the suggestion that this enzyme is a control point for low temperature sweetening, regulating the rate of SPS and sucroneogenesis by controlling the levels of UDP-Glc (Sowokinos 1990b; Sowokinos et al. 1993). The use of antisense technology to down-regulate the expression of UGPase in potato tubers has yielded contrasting results, depending on the physiological state of the tubers. Zrenner et al. (1993) employed antisense RNA technology to evaluate the role of UGPase in growing tubers. It was observed that carbohydrate metabolism was not affected when potato plants had a 96% reduction in UGPase activity when compared with wild-type plants. The results of Zrenner et al. (1993) revealed that only 4% of activity was sufficient for the enzyme to function normally. No statistically significant changes in the levels of fresh mass, dry mass, starch, hexose phosphates, or UDP-Glc were noted at harvest relative to control (wild-type) tubers. The reason for the excess levels of this enzyme during tuber growth remains to be resolved. In contrast, two separate antisense inhibition studies (Spychalla et al. 1994; Borovkov et al. 1996) in which UGPase activity was reduced by 30 to 50% (relative to that of wild-type plants) yielded transgenic potato tubers that accumulated lower levels of sucrose during storage relative to control (wild-type) tubers, at 4° and 12°C (Spychalla et al. 1994) and at 6° and 10°C (Borovkov et al. 1996). Spychalla et al. (1994) suggested that by limiting the rate of UDP-Glc synthesis, UGPase may exert control over the flux of carbon toward sucrose during the cold storage of tubers. These results are supported by Hill et al. (1996), who observed that following the initiation of cold-sweetening, the concentration of UDP-Glc changed in parallel with the concentration of sucrose. It is important to note that Zrenner et al. (1993) monitored sugar con-

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centrations in developing tubers, whereas the studies of Spychalla et al. (1994) and Borovkov et al. (1996) monitored sugar metabolism in stored tubers. The flow of carbon is very different in growing and stored tubers. In the growing tuber, most of the incoming sucrose is used for the synthesis of starch, while in the stored tuber, the hexose-phosphates produced from starch degradation are converted into sucrose. In cold-stored tubers, when the rate of starch breakdown exceeds the rates of glycolysis and respiration, the conversion of Glc-1-P to UDP-Glc is the only means of controlling the level of hexose-phosphates. Therefore, it is possible that a significant effect of reduced UGPase activity may be observed only in tubers acting in the direction of sucrose synthesis, such as during postharvest storage. Two UGPase alleles have been identified in potato tubers: UgpA and UgpB (Spychalla et al. 1994). Sowokinos et al. (1997) suggested that a relationship existed between the allelic polymorphism of UGPase and the degree of sweetening in a survey of a number of American and European cultivars and selections stored at 4°C. UGPase is a single-copy gene in potato tubers (Borovkov et al. 1996), and since most cultivated species are tetraploid, there are five possible combinations or ratios of the two UGPase alleles. Potato genotypes with some ability to resist sweetening at low temperatures all demonstrated a predominance (3:1) of the allele UgpA. Cultivars that accumulated high levels of sugars in the cold demonstrated a predominance of the allele UgpB. As an extension of this study, UGPase was cloned from 16 American potato cultivars and selections that differed in their cold sweetening ability during storage at 3°C (Sowokinos 2001a). The cultivars and selections that were resistant to low temperature sweetening possessed a UgpA:UgpB allelic ratio of 4:0 or 3:1. The cold-sensitive cultivars revealed a ratio in favor of the UgpB allele (1:3 or 0:4). Sowokinos (2001a) also found that the cold-sensitive potato cultivars in the study expressed up to three acidic isozymes of UGPase (UGP1, UGP2, UGP3) with UGP3 being the most abundant. Along with these isozymes, the cold-resistant cultivars also contained two additional isozymes of UGPase that were more basic in charge, designated as UGP4 and UGP5. Based on preliminary results analyzing the physicochemical and catalytic properties of the purified isozymes found in cold-resistant clones (UGP4 and UGP5), Sowokinos (2001b) suggested that the variation in sugar accumulation between cold-resistant clones and cold-sensitive cultivars may be partially due to differences in the expression of isoforms in the cold-resistant clones with unique catalytic properties (i.e., pH optimum, substrate affinities for Glc-1-P and UTP, Vmax, and the magnitude of product inhibition with UDP-Glc). The overall effect of

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these differences in isozyme expression may decrease the rate of UDPGlc formation, resulting in a lower accumulation of reducing sugars in the cold-resistant clones. B. Sucrose Degradation Hexose accumulation at low temperatures is thought to be largely due to the degradation of sucrose (ap Rees 1988), and as a result, this area has received much attention as a regulatory point in LTS. In plants, there are two different types of sucrolytic enzymes that can catalyze the breakdown of sucrose (Morrell and ap Rees 1986b). Sucrose can either be hydrolyzed by invertase, resulting in the reducing sugars glucose and fructose, or converted into UDP-Glc and fructose by SuSy, in the presence of UDP (Ross and Davies 1992). Most plant species, including potato tubers, contain both acid and alkaline (neutral) invertases (Sturm 1999). Acid invertase is compartmentalized and stored in vacuoles, whereas alkaline (neutral) invertase is a cytosolic enzyme (ap Rees 1988). Acid invertase isoforms that are ionically bound to the cell wall have also been identified (Sturm 1999). The vacuolar and cell wall invertases have pH optima between pH 4.5 and 5.0 and cleave sucrose at the Fru residue (Sturm 1999). These acid invertases can also hydrolyze other β-Fru-containing oligosaccharides such as raffinose and stachiose. The neutral or alkaline invertases are less well-characterized, but are generally believed to be cytosolic enzymes; pH optima have been reported to be in the neutral or slightly alkaline range (pH 7.0 to 8.0) (Avigad 1982; Sturm 1999). In contrast to the acid invertases, alkaline invertases appear to be sucrose specific (Sturm 1999). In developing tubers, incoming sucrose is degraded predominantly via the sucrose synthase pathway, toward starch synthesis. This is supported by the observation that the sugar content of developing tubers is low, and that SuSy activity is considerably higher than that of the invertases (ap Rees and Morrell 1990). However, no connection has been demonstrated between sucrose synthase and hexose accumulation in mature tubers. Sucrose synthase activity declines as tubers mature on the plant (Pressey 1969a) and in mature, stored tubers, acid invertase activity is prevalent (Pressey and Shaw 1966). Pressey (1970) showed that SuSy activity decreased sharply after tuber harvest and remained low after storage at both 4° and 18°C. Following the detachment of tubers from the mother plant, Ross and Davies (1992) reported a substantial and relatively rapid increase (within 2 days) in both hexose concentrations

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and acid invertase activity along with a substantial decrease (up to 84%) in SuSy activity. Furthermore, evidence suggests that alkaline invertase may also be more important in developing tubers relative to mature tubers (ap Rees and Morrell 1990). On the basis of these observations and given that sucrose, the major reserve sugar of plants, is stored mainly in the vacuole (Avigad 1982), acid invertase is believed to be the principal enzyme associated with the breakdown of sucrose into hexoses. There is strong suggestion that sucrose is hydrolyzed by acid invertase in the vacuole to produce hexoses that move into the cytosol for conversion to hexose phosphate by hexokinases. This is based on the widely established inverse correlation between sucrose content and vacuolar acid invertase activity (ap Rees 1974; ap Rees 1988; Davies et al. 1989; Richardson et al. 1990). Early studies regarding the potential regulatory role of invertase provided evidence for the existence of an endogenous invertase inhibitor (Schwimmer et al. 1961). A method of removing the inhibitor was developed by Pressey (1966), enabling a true measurement of total invertase activity. The level of invertase inhibitor was shown to decrease in tubers placed in 4°C storage, and increase when these tubers were transferred back to 18°C (Pressey and Shaw 1966). Pressey (1966, 1969b) and Pressey and Shaw (1966) measured the levels of hexoses, acid invertase, and an endogenous invertase inhibitor in cold-stored tubers and demonstrated that sucrose hydrolysis was regulated by the interaction of acid invertase (pH optimum 4.7) and an endogenous proteinaceous inhibitor. Total invertase activity was observed to be 3-fold higher at 4° than at 18°C (Pressey and Shaw 1966), however, the hexose content did not correlate with invertase activity. The lack of correlation between reducing sugar levels and invertase activity following storage at low temperature was suggested to be due to the inhibitor concentration, which regulated invertase activity and hexose formation in vitro (Pressey 1969b). Isla et al. (1992) identified the cellular location of acid invertase, its proteinaceous inhibitor, agglutinin, and lectin. Lectins are proteins that bind specifically to sugar moieties and have been shown to be effectors of higher plant invertases, including S. tuberosum invertase (Isla et al. 1991), and therefore lectin was proposed as an in vivo inhibitor of acid invertase activity in stored tubers. Acid invertase was found to be located in the vacuole where its substrate and products are also located. However, the proteinaceous inhibitor, S. tuberosum agglutinin and the lectin were not found in the vacuole, but were instead located in the cell wall. As a result, the in vivo role of the invertase inhibitor in the regulation of hexose accumulation in potato tubers is still unclear.

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In a study of 24 different potato cultivars, Zrenner et al. (1996) reported a strong correlation between acid invertase activity and the hexose to sucrose ratio in tubers stored at 4°C. Inhibition of acid invertase activity using antisense technology (ranging from 12% to 58% of wild-type tubers) resulted in an accumulation of sucrose and a decrease in the concentration of hexoses (Zrenner et al. 1996). However, a comparison of cultivars revealed no correlation between acid invertase activity and total reducing sugar accumulation, confirming the results of a previous study by Richardson et al. (1990). In addition, antisense inhibition of acid invertase did not result in a statistically significant decrease in the total amount of sugar accumulation (both hexoses and sucrose) during cold storage, although the transgenic tubers did have significantly reduced hexose:sucrose ratios (Zrenner et al. 1996). Since the total accumulation of sugars did not change in either the cultivar survey or the transgenic study, Zrenner et al. (1996) concluded that acid invertase does not control the accumulation of sucrose, fructose, and glucose in cold-stored tubers, but is involved in the control of the hexose:sucrose ratio. Although acid invertase is the dominant, if not the sole sucrolytic enzyme in stored tubers (the natural decline in the extractable activity of SuSy can be rapid and complete or partial and prolonged), the glucose:fructose ratio is rarely 1:1; ratios of 2:1 or 3:1 are common (Davies and Viola 1994). Davies and Viola (1994) suggest that these ratios may be due to genotypic differences, partial or complete starch degradation by amylases and the starch synthesizing potential of the tuber. Ross and Davies (1992) demonstrated that there is a consistent difference in the rate and extent of hexose accumulation in a variety of genotypes; however, changes in sucrose content were quite variable. The decline in sucrose content did not always coincide with hexose accumulation, thereby implying that the sucrose pool may be replenished as a result of starch degradation, as suggested by Isherwood (1973). The loss of starch required to provide the observed increases in hexoses is not measurable with any accuracy, since on average 70% of tuber dry matter is starch, but less than 1–2% is soluble sugar (Ross and Davies 1992). Due to the lack of a consistent relationship between acid invertase activity and reducing sugar content, it is apparent that factors other than acid invertase are responsible for reducing sugar accumulation in cold-stored tubers and for differentiating among LTS-susceptible and resistant cultivars. Acid invertase may be one of the central enzymes in the starch-sugar conversion, but the regulation of the overall transformation is not related solely to the level of this enzyme. Other cultivardependent factors such as starch degradation, hexose phosphate export

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from the amyloplast, or sucrose biosynthesis may be responsible for regulating the total accumulation of soluble sugars (i.e., Glc, Fru and Suc) during the cold storage of potato tubers.

C. Futile Carbon Cycling The onset of sugar accumulation in cold-stored potato tubers may be controlled by a “futile” metabolic cycle of simultaneous synthesis and degradation of sucrose. Hill et al. (1996) have observed that in the first 2 weeks of 4°C storage, the initial rates of sucrose accumulation corresponded closely with the estimated rates of sucrose synthesis. With increasing duration of cold storage, the rate of total soluble sugar accumulation decreased. This may be partially due to a decreased rate of sucrose synthesis; however, the increasing discrepancy between the net rate of total sugar accumulation and the estimated rate of unidirectional sucrose synthesis (using 14C glucose) demonstrates that considerable recycling of sugars occurred (Hill et al. 1996). Therefore, sugar accumulation ceases because the rate of recycling equals the rate of synthesis. This phenomenon of carbon recycling/sucrose turnover has also been reported in Chenopodium rubrum (red goosefoot) cell suspension cultures (Dancer et al. 1990), Ricinus communis L. (castor bean) seedlings (Geigenberger and Stitt 1991), ripening kiwifruit (MacRae et al. 1992), developing potato tubers (Geigenberger and Stitt 1993), and ripening bananas (Hill and ap Rees 1995). This metabolic cycle is thought to be highly important in contributing to the regulation of sucrose import and mobilization, allowing sucrose metabolism to respond sensitively to small changes in enzyme activities or metabolite levels (Dancer et al. 1990; Geigenberger and Stitt 1991).

IV. GLYCOLYSIS One of the initial theories put forward to explain the phenomenon of low temperature sweetening was that cold-lability of key glycolytic enzymes may lead to an accumulation of hexose-phosphates, resulting in a stimulation of sucrose synthesis (Pollock and ap Rees 1975; Dixon and ap Rees 1980a,b; ap Rees et al. 1981; Dixon et al. 1981; ap Rees 1988; Hammond et al. 1990). The main enzymes of the glycolytic pathway that have been studied in relation to LTS are fructose-1,6-bisphosphatase (FBPase), ATP-dependent phosphofructokinase (ATP-PFK), PPi-dependent phosphofructokinase (PPi-PFK), and pyruvate kinase (PK).

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FBPase is localized in plastids and in the cytosol. In chloroplasts, FBPase plays a central role in the synthesis of starch via the Calvin cycle (C-3 photosynthetic pathway) (Kossmann et al. 1994). A cytosolic FBPase is involved in gluconeogenesis, converting fructose 1,6-bisphosphate to Fru-6-P, which is used by SPS as one of the substrates for the production of Suc-6-P. FBPase is potently inhibited by Fru-2,6-P2 (Stitt 1987, 1990), a metabolite which is also a potent activator of PPi-PFK (Van Schaftingen et al. 1982). The role of FBPase in LTS was investigated by Claassen and Budde (1996) in a comparison of tubers stored at 2° and 8°C. Although there was a rapid increase in levels of sucrose and reducing sugars in tubers stored at 2°C, there was no change in FBPase activity, relative to 8°C storage. It was, therefore, concluded that there was no correlation between the coarse control of FBPase and sugar accumulation at 2°C. ATP-PFK is responsible for the irreversible, ATP-dependent conversion of Fru-6-P to Fru-1,6-P2. Four isoforms of ATP-PFK have been identified in potato tubers (Kruger et al. 1988). A number of studies have proposed a role for this enzyme in the regulation of LTS. Bredemeijer et al. (1991) observed that the accumulation of sucrose and reducing sugars in tubers during storage at 2°C coincided with a decrease in the maximum activity of ATP-PFK. Based on these observations, it was suggested that a coldinduced decrease in ATP-PFK activity reduced the rate of glycolysis, ultimately leading to the rapid accumulation of sugars. Consistent with the theory that cold-induced inactivation of ATP-PFK results in the accumulation of hexose phosphate and increased sucrose synthesis, Hammond et al. (1990) observed that the temperature coefficients (Q10) of three of the four isoforms were higher at 2–6°C than at 12–16°C. It was proposed that cold storage of potato tubers could decrease the proportion of hexose-phosphates that enters glycolysis, resulting in their accumulation (Pollock and ap Rees 1975), and subsequently an increase in reducing sugar content (ap Rees et al. 1981). This would support the argument of Bryce and Hill (1993) that ATP-PFK dominates the control of glycolysis and hence respiration in plants. However, these results are not in agreement with the observation that respiration of potato tubers increases concomitantly with the initial increase in sugar concentration (Isherwood 1973; Amir et al. 1977). In addition, the conversion of Fru-6-P to Fru-1,6-P2 is not under the exclusive control of ATP-PFK; this reaction is also catalyzed by PPi-PFK. Genetic modification of ATP-PFK was performed by Burrell et al. (1994), who reported that expression of the E. coli pfkA gene resulted in a 14- to 21-fold increase in the maximum catalytic activity of the enzyme, without affecting the activities of other glycolytic enzymes. No corresponding decrease in the content of hexose 6-monophosphates was

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observed, while the pool sizes of other glycolytic intermediates increased three- to eight-fold. Furthermore, the substantial increase in ATP-PFK activity did not affect the flux through glycolysis, nor the flux between glycolysis and the PPP (Thomas et al. 1997a). Based on these observations, it would appear that ATP-PFK does not limit the rate of respiration of potato tubers. Based on these observations, it would appear that ATP-PFK does not limit the rate of respiration of potato tubers. Additional evidence suggests that the glycolysis is controlled from the ‘bottom up,’ with primary and secondary control exerted at the level of phosphoenolpyruvate (PEP) and Fru-6-P utilization, respectively (reviewed in Plaxton, 1996). ATP-PFK is potently inhibited by PEP and therefore, ATP-PFK may ultimately be dependent upon the activity of enzymes that metabolize PEP (e.g., pyruvate kinase, PEP carboxylase). This is supported by the work of Thomas et al. (1997b), who applied Metabolic Control Analysis (MCA) to tuber glycolysis, and demonstrated that ATP-PFK exerts little control over glycolytic flux, while far more control of flux resides in the dephosphorylation of PEP. As mentioned above, in addition to ATP-PFK, plants contain PPiPFK, a strictly cytosolic enzyme that catalyzes an inorganic pyrophosphate (PPi)-dependent phosphorylation of Fru-6-P (ap Rees 1988). PPi-PFK is activated by fructose-2,6-bisphosphate (Fru-2,6-P2), which does not affect ATP-PFK (Stitt 1990). This reaction is reversible; stimulation of PPi-PFK in the direction of Fru-1,6-P2 synthesis (the forward direction) favors glycolysis, while the formation of Fru-6-P (the reverse direction) favors sucrose formation. The precise role of this enzyme is still unclear; functions in glycolysis (Hatzfeld et al. 1989), regulation of the cytosolic PPi concentration during sucrose synthesis and degradation (ap Rees 1988), equilibration of the hexose-phosphate and triose-phosphate pools (Dennis and Greyson 1987), and adaptability to stresses such as low temperature (Claassen et al. 1991) have all been proposed. The activity of PPi-PFK is often equal to or exceeds that of ATP-PFK (ap Rees 1988; Stitt 1990). Morrell and ap Rees (1986b) reported that the activity of PPi-PFK was 10 times that of ATP-PFK in developing potato tubers, which raises the possibility that glycolysis may proceed regardless of the activity of ATPPFK. Similar to ATP-PFK, PPi-PFK activity has also been shown to be greatly reduced in tubers stored at low temperature (Trevanion and Kruger 1991). The reduction in the maximum catalytic activity of PPi-PFK at 5°C, was attributed to a decrease in affinity for Fru-2,6-P2, an increase in sensitivity to Fru-2,6-P2 as an activator, and a decreased Fru-2,6-P2 concentration at decreasing temperature. Trevanion and Kruger (1991)

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concluded that by restricting the interconversion of Fru-6-P and Fru-1,6P2, these effects may contribute to the accumulation of hexosephosphates and subsequently lead to increased sucrose synthesis during storage at low temperatures. However, in a study of the maximum catalytic activity of PPi-PFK and concentrations of Fru-2,6-P2 and PPi in tubers stored at 2 and 8°C by Claassen et al. (1991), little evidence was found for a cold-induced inhibition of PPi-PFK. Based on their results, Claassen et al. (1991) postulated that PPi-PFK contributes to LTS by regulating the PPi concentration below inhibitory levels, which thereby facilitates UDP-Glc production and subsequently sucrose synthesis. In a more recent study, Hajirezaei et al. (1994) employed antisense technology to reduce the expression of PPi-PFK in stored tubers by 88–99%. Despite the fact that the transformation resulted in higher levels of hexose-phosphates in the antisense tubers relative to the wild-type tubers, rates of sucrose and hexose accumulation, and the total amounts of sugars accumulated at 4°C were similar. There was no change in the maximum catalytic activities of ATP-PFK or other enzymes of glycolysis (pyruvate kinase) or sucrose breakdown (invertase, SuSy) in the transgenic tubers, suggesting that compensation occurs at the level of (fine) metabolic regulation, rather than gene expression. In addition, no evidence was found that the antisense and wild-type tubers contained different PPi concentrations and thus results do not support the theory proposed by Claassen et al. (1991) that PPi-PFK is involved in regulating the PPi concentration. Results from Hajirezaei et al. (1994) suggest that PPi-PFK does not control the rate of glycolysis at low temperatures and that tubers contain excessive capacity to phosphorylate Fru-6-P. Pyruvate kinase (PK) has also been suggested as an enzyme involved in the control of glycolytic flux (Dixon and ap Rees 1980a; Copeland and Turner 1987; Plaxton, 1996). As the last enzymatic step of glycolysis, this enzyme catalyzes the irreversible synthesis of pyruvate and ATP from PEP and ADP. Pyruvate kinase is found in plastids and in the cytosol. The pyruvate formed may be metabolized by several biosynthetic pathways, or can be oxidized in the mitochondria. Gottlob-McHugh et al. (1992) transformed tobacco plants with potato tuber cytosolic PK, and unexpectedly produced two transformants in which PK activity was greatly reduced, a result of gene silencing. Leaves from these transformant plants had normal respiration and adenylate energy charge. This result suggests that the conversion of PEP to pyruvate in the cytosol may not be essential for leaf respiration, and/or that alternative pathways may be used to bypass PK. However, subsequent studies have demonstrated that while alternative enzymes can catalyze the conversion of PEP to pyruvate (i.e., plastidic PK, PEP phosphatase or the combined activities

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of PEP carboxylase, malate dehydrogenase and NAD-malic enzyme), cytosolic PK plays a critical role in regulating glycolytic flux (Grodzinski et al. 1999). Dunford (1992) transformed potato plants with antisense constructs to the gene encoding cytosolic PK and observed that these plants developed normal tubers. This further demonstrates the highly flexible nature of plant respiratory metabolism, and indicates that the supply of substrates to the mitochondrion must not be impeded by the lack of cytosolic PK. Based on the research presented to date, no conclusive evidence exists to support the theory that a cold-labile step in glycolysis is involved in triggering or regulating cold-induced sugar accumulation in potato tubers. This theory predicts that the onset of sucrose accumulation should be accompanied by an accumulation of hexose-phosphates, as well as an inhibition of respiration. The accumulation of hexosephosphates cannot be the immediate trigger for sugar accumulation in the cold, since this accumulation occurs within 6–10 h of exposure to cold, while sugar accumulation does not start until several days later (Isherwood 1973; Hill et al. 1996), by which time the hexose-phosphates have decreased again (Isherwood 1976; Hill et al. 1996). In addition, the onset of LTS is accompanied by an increase, rather than a decrease, in respiration (Isherwood 1973; Amir et al. 1977).

V. OXIDATIVE PENTOSE PHOSPHATE PATHWAY (PPP) Glycolysis and the oxidative pentose phosphate pathway (PPP) share the common intermediates glyceraldehyde-3-phosphate, Fru-6-P, and Glc6-P. The principal function of the PPP is presumed to be the generation of NADPH for various biosynthetic reactions (Dennis et al. 1997). Two of the principal enzymes in this pathway are glucose-6-phosphate dehydrogenase (G6PDH) and 6-phosphogluconate dehydrogenase (6PGDH). G6PDH occurs at a branch point in glycolysis where hexose-phosphate may be redirected into the PPP. This enzyme catalyzes the irreversible oxidation of Glc-6-P to 6-phosphoglucono-lactone with the reduction of NADP+. A lactonase rapidly hydrolyzes this compound to 6-phosphogluconate, and 6PGDH subsequently catalyzes the oxidative decarboxylation of 6-phosphogluconate to D-ribulose-5-phosphate and CO2, generating NADPH in the process. Wagner et al. (1987) proposed that for low sugar-accumulating cultivars, the PPP may provide a means of preventing the accumulation of high levels of sugars when tubers are stored below 10°C (by bypassing phosphofructokinase). However, Pollock and ap Rees (1975) found no

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differences in the maximum catalytic activities of G6PDH in Record tubers stored at 2° and 10°C. Barichello et al. (1990) reported that the maximum catalytic activity of G6PDH was similar at 4° and 12°C in both ND 860-2 (cold-resistant) and Norchip (cold-sensitive) tubers. In addition, storage temperature did not affect the maximum catalytic activity of 6PGDH in either genotype. However, it was observed that ND 860-2 tubers exhibited higher activities of G6PDH and 6PGDH, relative to Norchip. Radiolabeling studies of carbon partitioning revealed that the PPP pathway does not play an important role in affecting sugar accumulation at low temperatures (Barichello et al. 1990).

VI. MITOCHONDRIAL RESPIRATION In general, potato tuber respiration declines with decreasing storage temperature (Schippers 1977; Workman et al. 1979). At storage temperatures below 5°C, a brief respiratory “burst” is observed, followed by a decrease in respiration to a new steady state (Isherwood 1973; Amir et al. 1977). Dwelle and Stallknecht (1978) did not find a correlation between total sugars or reducing sugars and whole tuber respiration rate at a series of five storage temperatures ranging from 1.7° to 10°C, indicating that the higher rate of respiration observed at chilling temperatures cannot be simply attributed to the increase in sugars (i.e., sugars are not limiting for respiration). Sherman and Ewing (1983) attributed the initial rapid increase in respiration to the combination of the cytochromemediated (cyanide-sensitive) and alternative (cyanide-resistant) respiratory pathways. The capacity of the alternative pathway increases in the tissues of a wide variety of plants when exposed to low temperatures (Elthon et al. 1986). Additionally, cold-resistant cultivars and chilling-resistant plant tissues have been shown to develop a greater potential for respiratory electron flux through the alternative pathway than do cold-sensitive cultivars and tissues, as reported in wheat (McCaig and Hill 1977) and grapefruit (Purvis 1985). There is evidence that the alternative oxidase is synthesized de novo in potato tuber slices upon aging (Hiser and McIntosh 1990). However, evidence for the cold-induced synthesis of alternative oxidase protein in intact potato tubers has not been presented. Enhanced synthesis of alternative oxidase protein has been reported in tobacco leaves transferred to low temperature (Vanlerberghe and McIntosh 1992). Earlier studies of respiration in potato tubers indicated a role for the alternative oxidase in LTS. Amir et al. (1977) performed a kinetic study of the relationship between respiration rate, sugar content, and ATP lev-

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els in cold-stored potato tubers. Upon storage at 4°C, a decrease in respiration rate was observed, which coincided with a rapid increase in ATP concentration. Following the increase in ATP concentration, there was a respiratory burst and an increase in sucrose and reducing sugar concentrations. However, the increase in ATP content could not be directly attributed to the respiration burst, as this sharp rise preceded the increase in respiration by a few days and levels decreased rapidly during the respiratory burst (Fig. 8.3) (Amir et al. 1977). Solomos and

Fig. 8.3. The effect of 4°C storage on respiration (a), sugar accumulation (b), and ATP concentration (c) of freshly harvested tubers. Adapted from Amir et al. (1977).

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Laties (1975) suggested that sucrose formation could serve as an effective sink for excess ATP via the alternative pathway (i.e., the higher the respiration rate, the larger the accumulation of sugars). In agreement with this theory, Sherman and Ewing (1982) observed that low O2 levels, which inhibit the cyanide-resistant pathway, were effective in suppressing sugar accumulation in tubers stored at 1°C, leading to the suggestion that low temperature sweetening may be directly linked to the onset of cyanide-resistant respiration. The alternative oxidase may also play a protective role in the mitochondrion, by preventing both an over-reduction of the respiratory chain and the consequent production of reactive oxygen species that can cause organelle and cell damage. The flow of electrons through the alternative pathway could enhance oxygen utilization when energy demands of the tissues are low and levels of respiratory substrates are high. Thus, the alternative pathway could reduce the potential for the generation of oxygen-derived free radicals when the availability of respiratory electrons to the dehydrogenase complexes exceeds the capacity of the cytochrome oxidase (Purvis and Shewfelt 1993). This has been discussed by Purvis and Shewfelt (1993) in the context of chilling injury, but alternative respiration may be a more general protective mechanism allowing the plant cell to cope with large variations in carbon flux through respiratory pathways, which can commonly occur in plant tissues exposed to environmental stresses. The integrity of the mitochondrial membrane changes during tuber aging (Hiser and McIntosh 1990) and is of great importance to the successful functioning of the cytochrome and alternative oxidase respiratory processes. Decreased fluidity and increased leakiness of cellular membranes has been observed when potato tubers are subjected to cold stress (Shekar et al. 1979; Workman et al. 1979). Changes in membrane permeability due to lipid oxidation have been reported to play a role at low temperatures; LTS has been suggested to be a peroxidative stress (Wismer et al. 1998). Although it has been shown that a relationship indeed exists between the starch-to-sugar conversion and membrane permeability during LTS, the subject of membrane lipid dynamics will not be discussed here. For more detail, the reader is referred to studies by Workman et al. (1979), Sowokinos et al. (1987), Spychalla and Desborough (1990), O’Donoghue et al. (1995), and Wismer et al. (1998). These studies of the alternative oxidase involve the use of inhibitors of the cyanide-sensitive and cyanide-resistant pathways, cyanide (KCN) and salicylhydroxamic acid (SHAM), respectively. The measurement of the alternative pathway by inhibitors relies on the assumption that the alternative pathway only operates when the cytochrome pathway is saturated. The usefulness of this approach for assessing respiratory activ-

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ities in vivo has recently been called into question by work showing that electron flow to the alternative pathway can occur when the cytochrome pathway is not fully saturated (Hoefnagel et al. 1995; Ribas-Carbo et al. 1995). Therefore, the partitioning of electrons to the alternative oxidase, when determined using inhibitors, may have been considerably underestimated in the past. As a result, the exact quantitative contribution of the alternative oxidase to potato tuber respiration during low temperature storage remains to be unequivocally established.

VII. METABOLIC FACTORS AFFECTING CHIP COLOR DEVELOPMENT The ability to maintain satisfactory chip color is a major challenge for the potato chip industry. Color is an important characteristic of potato chip quality; however, its control is complicated due to the fact that color is determined by the chemical composition of the tubers, which not only varies by season and cultivar, but changes over the storage period (Smith 1987). The color and flavor of potato chips is attributed to the products of the Maillard reaction between the carbonyl groups of reducing sugars and the α-amino groups of amino acids (Habib and Brown 1956; Shallenberger et al. 1959). Excessive browning during frying produces an unacceptable color and an undesirable bitter taste. Reducing sugar content (i.e., Glc and Fru) is generally used to predict the suitability of potato tubers destined for processing into chips, as levels of reducing sugars have typically been considered the most influential factor in color development (Marquez and Añon 1986; Sowokinos et al. 1987; Roe et al. 1990). Although sucrose does not participate directly in the Maillard reaction, it does contribute to this reaction via its hydrolysis into fructose and glucose during the frying process (Shallenberger et al. 1959; Leszkowiat et al. 1990). While sugar levels are without question important in determining chip color, there is evidence that anomalies in the relationship between reducing sugars and chip color do occur (Habib and Brown 1956), and suggestion that free amino acids may also play a significant role in the determination of chip color (Roe et al. 1990; Khanbari and Thompson 1993; Brierley et al. 1996). Hughes and Fuller (1984) reported that chip samples from potato tubers grown under different levels of nitrogen can have different chip colors for the same amount of reducing sugars. Roe et al. (1990) also reported greater browning per unit reducing sugar in tubers grown under high nitrogen conditions. Increasing nitrogen fertilization has been shown to reduce the amount of reducing sugars in potatoes (Hughes 1986), and has also been found to lead to an increase

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in free amino acid content (Roe et al. 1990). In addition, storage conditions and the length of storage period are known to influence the sugar content as well as the free amino acid content, which increases as a result of protein breakdown (Fitzpatrick and Porter 1966; Brierley et al. 1996). The free amino acid pool of harvested tubers consistently contains a high proportion of the amides glutamine and asparagine (Davies 1977; Millard 1986; Leszkowiat et al. 1991; Brierley et al. 1996). Brierley et al. (1996) reported that the amides asparagine and glutamine have been observed to account for 50–90% of the total free amino acid content of tubers. As these two amino acids form the largest part of the free amino acid pool, it would be expected that the amides influence processing quality to a similar extent as the total free amino acid content (Roe et al. 1990). Using leached potato slices infiltrated with fixed concentrations of amino acids and varying concentrations of glucose, Khanbari and Thompson (1993) found that asparagine and glutamine were important amino acids in the development of chip color at low concentrations of glucose. Other compounds that have been proposed to contribute to the nonenzymatic browning of potato chips include ascorbic acid and phenolic acids. Ascorbic acid can react with amino acids during frying to form brown pigments, as shown in a model system of filter paper discs (Smith 1987). Results from compositional studies of tubers involving measurement of a number of parameters (including ascorbic acid) have provided mixed results: Rodriguez-Saona and Wrolstad (1997) found a very good negative correlation between ascorbic acid and chip color, while Mazza (1983) reported a weak negative correlation between ascorbic acid content and color development. The problem with interpreting such results is that it is not possible to determine the individual effect of each component on chip color. This issue was addressed by Rodriguez-Saona et al. (1997) using a model system of leached potato slices infiltrated with different concentrations of ascorbic acid, where it was observed that the ascorbic acid concentration did affect chip color browning, although only at low concentrations of reducing sugars (i.e., 40 mg/100g fresh weight). Browning may also result from the nonenzymatic autoxidation of polyphenolic compounds such as caffeic acid, producing quinones that may react further with amino groups of amino acids and proteins (Kalyanaraman et al. 1987) and generate brown pigments (Cilliers and Singleton 1989). In their compositional study, Rodriguez-Saona and Wrolstad (1997) observed a negative correlation between chlorogenic acid, the major phenolic acid in potato tubers, and chip color. However, this relationship was not significant in a model study of potato slices in which individual

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effects were isolated (Rodriguez-Saona et al. 1997), suggesting that phenolic acids do not contribute significantly to chip color development.

VIII. CONCLUSION The sugar balance of the potato tuber is mediated by many interrelated metabolic pathways and is subject to significant genetic and environmental control. As this review outlines, the effects of low temperature storage on tuber carbohydrate metabolism are extremely complex; as such it is highly improbable that there is any single cause of LTS. Plant cell metabolism is highly regulated and compartmentalized, and it is quite apparent that attempts to determine the cause(s) of LTS are confounded by the complex and flexible nature of plant carbohydrate metabolism. Evidence presented to date suggests that LTS may be a combination of starch degradation, alterations in the biochemical pathways of sucrose synthesis, glycolysis, hexogenesis, and mitochondrial respiration, as well as loss of permeability of membranes. Through the use of genetic engineering and modern molecular techniques, a more detailed understanding of tuber carbohydrate metabolism at the molecular level has been achieved in recent years, such as the elucidation of cold-induced isoforms of enzymes involved in starch and sucrose metabolism. Isozymes unique to tubers that resist sweetening have also been identified, for instance, the isozymes UGP4 and UGP5 of UGPase (Sowokinos 2001a). It is important to emphasize that for the majority of the enzymes involved in tuber carbohydrate metabolism, several isoforms exist, therefore extreme caution should be exercised when interpreting results from genetic manipulation experiments. For instance, antisense inhibition/ down-regulation of a specific isozyme that does not have a regulatory function can lead to incorrect conclusions regarding the importance that other isoforms may have on the sweetening process. As Deiting et al. (1998) alluded to (in reference to the observation of a cold-induced isoform of β-amylase), it is extremely difficult to determine whether the biochemical changes associated with cold sweetening serve to initiate and/or regulate the process. Many metabolic changes observed during cold sweetening may actually be a part of the general sweetening process, being an effect or response rather than playing a role in initiation or regulation. The complexity of the sweetening phenomenon is further illustrated by the down-regulation of enzymes early in the starch-sugar interconversion pathway, such as the isozymes of starch phosphorylase, which have been shown to have minimal effect on the accumulation of reducing sugars (Kumar et al. 2000).

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It is evident that recent findings have advanced our understanding of the molecular and biochemical changes associated with the LTS phenomenon in potato tubers. For the potato processing industry, there is great incentive to fully elucidate the physicochemical properties responsible for the initiation and regulation of LTS. Solving this problem could lead to the development of cultivars with high yielding potential and resistance to cold sweetening during long-term storage, which could be obtained through traditional breeding and selection methods and/or through the use of molecular techniques (genetic manipulation). Meeting this objective would also result in improved quality of processed product and a reduction in the use of sprout inhibitors, with obvious economic gains for both growers and the potato processing industry.

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9 Cassava-based Multiple Cropping Systems V. Ravi and C. R. Mohankumar Central Tuber Crops Research Institute Sreekariyam, Trivandrum India, 695 017

I. INTRODUCTION A. Definitions B. Multiple Cropping Systems C. Intercropping Productivity D. Economics of Intercropping Systems II. GROWTH AND PRODUCTIVITY OF CASSAVA A. Stem Branching B. Leaf Area C. Storage Roots D. Dry Matter Production E. Dry Matter Partitioning F. Plant Population G. Starch Yield III. GROWTH AND PRODUCTIVITY OF ASSOCIATE CROPS A. Cowpea B. Peanut C. Soybean D. Pigeonpea E. Common Bean F. Mungbean G. Maize H. Rice IV. INTERCROPPING CASSAVA A. Cassava + Legumes 1. Cassava + Cowpea 2. Cassava + Peanut 3. Cassava + Soybean

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4. Cassava + Pigeonpea 5. Cassava + Mungbean 6. Cassava + Vegetable Legumes B. Cassava + Non-Legumes 1. Cassava + Okra 2. Cassava + Maize 3. Cassava + Rice C. Cassava + Legumes and Non-Legumes D. Cassava + Perennials 1. Growth and Productivity 2. Nutrient Management and Soil Fertility V. RELAY SEQUENTIAL CROPPING CASSAVA A. Lowlands B. Uplands VI. MULTI-CROPPING MANAGEMENT A. Plant Type B. Planting Schedule C. Plant Density and Spatial Arrangement D. Nutrient Management 1. Fertilization 2. Nutrient Competition 3. Problem Soils 4. Green Manuring E. Weed Control F. Irrigation VII. CONCLUSIONS AND FUTURE PROSPECTS LITERATURE CITED

I. INTRODUCTION A. Definitions Land can be either monocropped, in which case only one crop is grown annually, or multiple cropped, in which case two or more crops are grown annually either simultaneously or sequentially. Multiple cropping may be an effective way of intensifying agricultural production through the efficient use of resources (light, water, nutrients, space) and duration available for cultivation. There are two types of multiple cropping: (1) intercropping, in which two or more crops are grown simultaneously in the same field: crop intensification is in both the temporal and spatial dimensions and the component crops compete for resources during the entire or part of their growth period, and (2) sequential cropping, in which two or more crops are grown as pure stands in sequence in the same piece of land during the same year, with the succeeding crop planted only after the previous crop has been harvested: crop intensifi-

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cation is only in the temporal dimension and there is no competition among the component crops (Francis 1989). Intercropping can be practiced in four different ways (Andrews and Kassam 1976; Francis 1989) as follows: 1. Mixed intercropping—two or more crops are grown simultaneously in an irregular arrangement without a well-defined planting pattern. 2. Row intercropping—two or more crops are grown simultaneously in a well-defined row arrangement. 3. Strip intercropping—two or more crops are grown simultaneously, and singly in strips wide enough to allow independent cultivation, but at the same time, sufficiently narrow to induce crop interaction. 4. Relay intercropping—one or more alternate crops are planted within an established crop in a way that the reproductive stage of the first crop coincides with the initial development of the other(s). Double, triple, and quadruple cropping are sequential cropping with two, three, and four crops, respectively. Ratoon cropping is a sequential cropping with a ratooned crop, that is, the cultivation of sprouts from the mother plant that remains from the previous crop (Francis 1989). In this paper, intercropping will be denoted with a plus sign (+) between two crops grown simultaneously, e.g., cassava + peanut. A sequential cropping is denoted with a hyphen (-), e.g., rice - rice - sweet potato. Thus, an intercrop of cassava and peanut followed by cowpea will be written as cassava + peanut - cowpea. Relay cropping is denoted with a slash sign (/), e.g., rice / mung bean, where rice is the first crop. B. Multiple Cropping Systems Multiple cropping is often practiced in long-duration crops in order to make use of the light and space available during the early growth period. It is one of the means of risk management used to overcome the vagaries of nature and market fluctuations. In farming families having an excess of labor resources, multiple cropping can provide increased employment potential and thereby generate more income per unit area per unit time. Another advantage of multiple cropping is the hedging of risks, that is, when there is a fall in price of the main crop in the system, it may be partially compensated by the additional income obtained from intercrops. Multiple cropping is also an excellent strategy for reducing soil

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erosion, leaching of nutrients, and rapid growth of weeds by rapidly providing adequate vegetative cover. It is also a natural strategy for maximizing land use through the proper choice of crops that fit in with changes in water regimes. In multiple cropping, component crops normally show less variability in total biomass and yield than do pure stands in monocropping. Reasons for this greater stability may be due to the reduced pressure of diseases, insect pests, and weeds as a result of greater vegetative diversity and the better and earlier soil cover provided by the intercrops. Multiple cropping systems are largely practiced in humid tropics where a relatively long favorable growing season prevails. This ensures greater stability and reduces the risk of total crop failure, makes the best use of land and labor, and increases food production at different times during the year. When small farmers adopt multiple cropping as the production system, root and tuber crops such as cassava, sweet potato, yams, and aroids can be the source of carbohydrates to diets. Legume intercrops such as bean, cowpea, mung bean, peanut, and pigeonpea can contribute protein. Legumes can add nitrogen or at least produce N to support their growth, and typically do not have great demand for phosphorus and potassium. So as pure stands, multiple cropping systems may be highly productive and more suitable for small and subsistence farmers, as they can provide the family with a balanced diet. This review describes and analyzes various multiple cropping systems based on cassava (Manihot esculenta). C. Intercropping Productivity In an intercropping system, the component crops experience different microenvironments due to the differences of their morphology and physiology. As a result, resources are unevenly shared between the component crops, and their yields deviate from their pure stand yields due to mutual competition or cooperation (Trenbath 1974). Here, the aggressive crop utilizes a greater share of resources than the less aggressive crop. The interaction between the component crops may be “competitive” where an increase in productivity of one crop (dominant) causes a decline in productivity of an another crop (dominated), “complementary” where an increase in productivity of one crop causes an increase in productivity of another crop, “supplementary” where an increase in productivity of one crop has no influence on the productivity of another crop, or “mutual inhibition” where the productivity of both crops in an intercropping system are less than their pure stands (Willey 1979). Intercrop productivity can be estimated through the Land Equivalent Ratio

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(LER, Willey and Osiru 1972). LER is the sum of the Partial Land Equivalent Ratios (PLERs), where PLER of a crop is the ratio of the yield of a crop in an intercropping system to the yield of the same crop when grown as pure stand in a unit area of land. Because of the dependency of LER on the relative economic yield of the component crops in a pure stand, and in an intercropping system, several factors, including the morphology of cultivars such as plant height and canopy width, plant spacing, plant population, planting pattern, crop duration, and the period of their competition for resources, water, soil fertility, fertilizer applied, and response of the crop to fertilizers, are likely to influence and alter the LER in different intercropping systems. Further, when there is a considerable difference in length of growing period of the component crops, LER overestimates intercropping advantage (Hiebsch and McCollum 1987; Fukai 1993). However, to estimate the efficiency of the cassavabased intercropping systems, researchers are still conveniently using LER. If an intercropping system involves two component crops A and B, and if both the component crops produce less than 50% of their pure stand yield, in the same unit area, LER of less than 1.0 (PLER less than 0.5 for each crop) is achieved, which means that it is not an efficient intercropping system. For example, in a cassava + pigeonpea system where cassava and pigeonpea produced less than 50% of its pure stand yield, LER of less than 1.0 was achieved, and therefore it is not an efficient system (Cenpukdee and Fukai 1992a,b). If both component crops A and B produce more than 50% of its pure stand yield (PLER more than 0.5 for each crop), LER more than 1.5 can be achieved, which means that it is an efficient intercropping system. If crop A produces more than 50–100% of its pure stand yield (PLER 0.5 to values 1.0 or more than 1.0), and crop B produces less than 50% of its pure stand yield (PLER less than 0.5), LER 1.0 or more than 1.0 will be achieved. For example, in a cassava + soybean system where cassava produced more than 100% of its pure stand yield (PLER more than 1.0), and soybean produced less than 50% of its pure stand yield (PLER less than 0.5), LER more than 1.0 was achieved (Cenpukdee and Fukai 1992a,b). This is considered to be an advantageous system in situations where the primary requirement is for a full yield of a main crop (cassava) and some yield of an associate crop (soybean). If the component crops A and B produce 100% of their pure stand yield, this gives LER of 2.0 (PLER 1.0 for each crop), and this indicates that it is a highly efficient productive system. However, differences in the relative economic value of the crops between regions may alter which system is most profitable, and the system with the largest net income may be different from the system with the highest LER. In this

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situation, a farmer can utilize a cassava-based intercropping system, although its productivity may be low. D. Economics of Intercropping Systems Although, in several intercropping studies, the yield of cassava as well as intercrop have been reported to be lower than the pure stand yield, the net income was always higher than the pure stand cassava crop. The gross/net income was higher in the following cassava intercropping systems with legumes/non-legumes than the pure stand of cassava. The gross income increased by 40–82% in a cassava + French bean system (Prabhakar et al. 1983; Mohankumar and Ravindran 1991), 25% in a cassava + urd bean system (Ashokan et al. 1985), 29% in a cassava + soybean or mungbean system (Sinthuprama 1979), 13–20% in a cassava + green gram, or black gram system (Muthukrishnan and Thamburaj 1979), 12–72% in a cassava + peanut system (Sinthuprama 1979; Ashokan et al. 1985; Mohankumar et al. 1987; Meera Bai et al. 1991; Mohankumar and Ravindran 1991; Tongglum et al. 2001), 28–41% in a cassava + peanut and black gram system (Meera Bai et al. 1991; Tongglum et al. 1992), 12–96% in a cassava + cowpea system (Prabhakar et al. 1983; Ashokan et al. 1985; Meera Bai et al. 1991; Mohankumar and Ravindran 1991), 26% in a cassava + peanut and cowpea system (Meera Bai et al. 1991), 15% in a cassava + pigeonpea system (Prabhakar and Nair 1979), and 33.3% in a cassava + soybean system (Tongglum et al. 2001) over the pure stand cassava crop. Gross income increased only marginally by 2–12% in cassava + maize or cassava + bean + maize systems over the pure stand cassava crop (Porto et al. 1979; Mohankumar et al. 1987). The increase in gross income in the cassava based legume + non-legume intercropping systems were 35% in cassava + mungbean, 13% in cassava + rice + mungbean, 45.7% in cassava + peanut + mungbean, 6.0% in cassava + maize + peanut - cowpea, 20.6% in cassava + rice + peanut - cowpea, 21.7% in cassava + peanut - mungbean - cowpea, and 16.0% in cassava + maize + rice - peanut - cowpea (Wargiono et al. 1995; Tongglum et al. 2001). Here, the legumes and non-legumes contributed 47 to 57% to total gross income (Wargiono et al. 1995). Some studies have shown that inclusion of maize (Sinthuprama 1979), soybean, black gram, or sunflower with cassava may not be profitable (Mohankumar et al. 1987; Tongglum et al. 1992). Intercropping cassava with vegetables such as tomato, onion, and cucumber, increased gross income by 23, 13–53, 13–57%, respectively, than the pure stand cassava crop (Muthukrishnan and Thamburaj 1979; Prabhakar et al. 1983; Mohankumar and Ravindran

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1991). Highest net income was achieved when cassava was intercropped with tobacco than with peanut, sorghum, chilli, or long bean (Chew 1979).

II. GROWTH AND PRODUCTIVITY OF CASSAVA Cassava is a perennial crop with indeterminate growth habit but is commonly cultivated as an annual crop between the latitudes 30° N and S, at altitudes from sea level up to about 2,000 m in equatorial regions, with annual precipitation ranging from 500 mm up to 6,000 to 8,000 mm (Irikura et al. 1979). It tolerates hot climate, but at temperatures below 20°C, the plant does not grow normally and the storage root yield decreases drastically (Rogers and Appan 1972; Cock and Rosas 1975; Kawano et al. 1978; Irikura et al. 1979). Depending on the growing conditions and the cultivar, crop duration may vary between 7–12 months (CTCRI 1998). In areas where a cool climate arrests plant growth and starch accumulation in the roots, cassava cultivars are being cultivated for a long duration, up to 2–3 years, although the eating quality declines with ageing due to increasing fiber content (Cours 1951; Obigbesan and Agboola 1973; Cock 1984, 1985; Lilley et al. 1988; Manrique 1990b,c; Pounti-Kaerlas 2001). After 4 seasons of cropping, 4 annual crops when combined produced 49.4 t/ha of dry storage root. Corresponding yields of two 2-year crops, one annual plus one 3-year crop, and one 4-year crop, were 44.7, 40.3, and 38.1 t/ha, respectively (Lilley et al. 1988). However, in most of the cultivars, marketable storage root yields are obtained in 10–12 months after planting (MAP) (Maini et al. 1970; CTCRI 1998). In the tropics and subtropics, cassava is cultivated under rainfed or irrigated conditions in soils of low fertility. Cassava cultivars vary widely in their storage root yield potential. An average fresh root yield of 25–35 t/ha in 6–7 months, and 21–48 t/ha in 10–12 months have been achieved in improved, high-yielding cultivars by advanced cultural practices (Magoon et al. 1970; Wholey and Booth 1979; Ramanujam 1991; CTCRI 1998). The world average storage root yields of cassava are about 9.8 t/ha, and the highest yields are obtained in Barbados (27.3 t/ha) and in India (24.0 t/ha). Current world production of cassava is 158,620 × 103 t from an estimated total planted area of 16,188 × 103 ha (Table 9.1). The succulent, starchy storage roots of cassava serve as staple food, animal feed, as a raw material for industrial purposes as a starch source, and for alcohol production (Balagopalan et al. 1988; FAO 1997a,b; PountiKaerlas 2001).

362 Table 9.1.

V. RAVI AND C. MOHANKUMAR Cassava area harvested, yield, and production, 2001 (www.FAO.org). Area harvested (× 103 ha)

Yield (t/ha)

Production (× 103 t)

World

17,020

10.5

178,863

Continents Africa Asia S. America NC America Oceania

10,894 3,496 2,433 181 15

8.7 14.3 13.3 5.9 11.6

95,239 49,914 32,469 1,068 178

Chief Countries Nigeria Congo Dem R Brazil Indonesia Thailand Mozambique Tanzania Ghana Angola Uganda Madagascar Ivory Coast India Benin Paraguay Viet Nam

3,135 1,902 1,741 1,280 1,150 926 761 600 530 390 350 330 270 260 257 250

10.8 8.1 13.8 12.6 15.9 5.8 7.4 14.2 6.2 13.5 6.4 5.8 25.9 10.8 15.0 8.2

33,854 15,436 24,088 16,158 18,283 5,362 5,650 8,512 3,300 5,265 2,228 1,900 7,000 2,800 3,854 2,050

Location

A. Stem Branching Cassava forms new leaves and stem at the same time as it fills the storage roots with starch. The crop has a range of forms, from a singlestemmed or unbranched to profusely branched habit giving a shrubby appearance (Rogers and Fleming 1973; Ramanujam 1991). Branching is a cultivar character and cultivars widely vary in their ability to form lateral branches. More lateral branches are formed under conditions of adequate illumination and soil fertility. Increase in N application more than 150 kg/ha increased shoot growth and increased dry matter partitioning to branches (Ramanujam 1979, 1980). The time of branching is a cultivar character and branching is delayed as the temperature increased or decreased from 24°C (Irikura et al. 1979; Manrique 1990b). Under conditions of low soil fertility, a genotype, that normally

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branches, may fail to develop branches (Cours 1951). Decrease in soil moisture also decreases branching (Connor and Cock 1981). Lian and Cock (1979b) obtained the lowest storage root yield in early and profusely branching cultivars rather than in late branching and nonbranching cultivars. Highest storage root yield can be achieved by using either a late branching type (6 months or later) with three branches at each point or an early branching type with two branches at each point (Lian and Cock 1979a). Reduction in light intensity or increase in shade more than 20% increased plant height and decreased the number of branches on the plant (Okoli and Wilson 1986). The effect was distinct at 50% shade. B. Leaf Area Leaf area (LAI, the ratio of total leaf area to land area) reflects the changes in leaf number and size. Under tropical rainfed conditions, the leaf area develops slowly until 3–4 weeks after planting. Cultivars significantly differ in their early vegetative growth. In some cultivars, that have early and profusely branching habit and dense canopy, 90% of the land area is covered with foliage by 45 days after planting (DAP), while other cultivars, regardless of their branching habit, may take 75–90 days to achieve the same foliage cover over land area (Ramanujam 1991). Canopy ground cover is faster in fertilized plants than in unfertilized plants (Pellet and El-Sharkawy 1993). Subsequently, leaf area, which increases rapidly until 6–7 months, declines sharply during the dry season, 7–12 months after planting (MAP) (Cours 1951; Ramanujam and Indira 1983; Ramanujam 1991; Pellet and El-Sharkawy 1993) because the leaf size and rate of leaf production decreases and as the older leaves senesce and abscise, the crop becomes dormant (Connor and Cock 1981; Connor et al. 1981; El-Sharkawy and Cock 1984, 1987; Porto 1983; Ramanujam 1991). When cassava is allowed to stay on land (beyond 12 months), after the onset of rains (subsequent monsoon), few storage root reserves are used to produce new leaves, and the leaf area increases a second time between 12–17 MAP to an extent somewhat lower than in the first year and then declines later (Cours 1951). Although the decline in the leaf area may be due to water deficit stress, there appears to be an inherent tendency for the leaf area of cassava to decline in a later period of growth (Cours 1951; CIAT 1973; Cock 1973). In subtropical regions, the growth of cassava alternates with summer and winter, and cooler temperatures in winter (22.5°C) affect the growth of cassava in a fashion similar to water stress in the tropics (Manrique 1990b). The rate of leaf formation and LAI decreases at temperatures less than 24°C (Irikura

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et al. 1979; Manrique 1990c). The cumulative number of leaves, regardless of their branching habit, continue to increase up to 6–8 MAP (Lian and Cock 1979b; Ramanujam and Indira 1983). Profusely branching cultivars have a higher mean LAI (2.5–4.2) than nonbranching cultivars (Ramanujam and Indira 1983). Thus, maximum canopy size (LAI varying between 2–10) for cassava occurs during an active growth period between 3–7 MAP regardless of their branching habit, which then declines between 7–12 MAP (Cours 1951; Williams 1972; Enyi 1972a,b,c, 1973; Cock 1973, 1976; CIAT 1972, 1978; Keating 1981; Manrique 1990c; Ramanujam 1991). The mean LAI of cassava cultivars was greater (6–8) in a subtropical environment than the LAI (2–4) in a tropical environment (Keating et al. 1982a; Fukai et al. 1984; Cock et al. 1979; Manrique 1990c; Ramanujam 1991). Increase in N application up to 250 kg N/ha increases LAI from 1.4 to 4 but optimum LAI (3.0) was achieved with the application of 150 kg N/ha (Ramanujam 1982a). Decrease in light intensity or increase in shade more than 40% significantly decreased LAI (Okoli and Wilson 1986). The LAI increases with increase in plant density. In 5 cassava cultivars, regardless of their branching habit, LAI at full canopy stand varied between 2.2–3.9 in a density of 12,340 plants/ha, between 3–6 in 17,770 plants/ha, and 3.7–6.7 in 27,770 plants/ha (Ramanujam 1982b, 1991). For 95% light interception, LAI of 2.5–3.5 was found to be optimum for cassava (Cock 1983). Low-yielding cultivars (27 t/ha) maintain either sub-optimal LAI (LAI less than 2) or supra-optimal LAI (LAI more than 4), whereas high-yielding (40t/ha) cultivars maintain LAI between 2.4–3 during an active growth period (2–6 MAP) (Cock et al. 1979; Ramanujam 1991). Under favorable growing conditions, an LAI more than 4 favors shoot growth at the expense of storage root growth. The orientation and distribution of leaves within the cassava leaf canopy varies markedly both between cultivars and with time of day. Vertical foliage and narrow lobed leaves allow more light transmission (light penetration into the lower layers of leaf canopy). However, cultivars with better light penetration had lower crop growth rate (CGR) at low LAI and higher CGR at high LAI. Thus, vertically oriented and narrow lobed leaves increase storage root yield in some cultivars but not in all (Hunt et al. 1977; Williams and Ghazali 1969; Williams 1972). Light interception is closely related to LAI and maximum light interception occurs at 28°C because of maximum leaf formation (Irikura et al. 1979). The light transmission also decreases with increase in plant density. The light transmission decreased from values between 60–75% in a density of 6,940 plants/ha to values between 20–25% in a density of 27,770 plants/ha (Ramanujam 1991). This means that light interception

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was greatest (80–75%) at highest plant density. Cultivars that have a thin canopy show less than 50% of light interception during their major part of the growth period, and hence yield low. However, in these cultivars, yield per unit land area increases at higher plant densities (Ramanujam 1991). A cultivar with profuse branching and dense canopy (LAI more than 9) shows lowest light transmission, which decreased from 22% to 14% as the plant density increased from 6,940 to 27,770/ha (Ramanujam 1991). A short stature, nonbranching cultivar, in which LAI increased from 2.5 to 3.2 as the plant density increased from 17,770 to 27,770 plants/ha, showed lowest light transmission (38%) at highest plant density as compared to branching cultivars, and this accounted for its higher storage root yield at higher plant density (Ramanujam 1991). In the forenoon hours, top layers of a fully developed cassava canopy intercept higher solar radiation than the lower layers. In the afternoon hours, light transmission to the lower layers of canopy increases due to the heliotropic response of cassava leaves (San Jose and Berrade 1983). Since cassava leaves require 1000 µEinstein/m2/s photosynthetically active radiation (PAR) for maximum photosynthetic rate (Palta 1982), any cultivar and plant population must ensure this amount of light transmission in the field. High light availability, soil moisture, soil fertility (particulary N content), and profuse branching habit increase the leaf production, leaf size, and leaf area (Irikura et al. 1979; Ramanujam 1982a,b; Cock 1983). Maximum light interception among cassava cultivars varies between 39.7–88.9% at LAI more than 2. Decrease in soil moisture decreases light interception by 58.2–70.1% (Ramanujam 1990). The photosynthetic rate of cassava cultivars varies between 13–26 µmol/m2/h (Mahon et al 1977; El-Sharkawy et al. 1984; Ravi and Saravanan 2000). The optimum temperature for maximum photosynthetic rate is between 25–35°C (Mahon et al. 1977; El-Sharkawy et al. 1984). Net photosynthesis and storage root yield was positively correlated (ElSharkawy and Cock 1990; El-Sharkawy et al. 1990; Pellet and Sharkawy 1993). Given the same LAI, higher light interception can be achieved in some cultivars than in others because of better leaf positioning as a result of leaf curvings and leaf angles (Pellet and Sharkawy 1997). In acid soils, application of NPK up to 100 kg/ha increased leaf area and light interception (Pellet and Sharkawy 1997). Cassava leaves have a longevity of 41–125 days under favorable growing conditions (Ramanujam 1977, 1979; Cock 1984), but leaves abscise within 10 days in 100% shade conditions (Cock and Rosas 1975; Rosas et al. 1976; Cock et al. 1979). However, cassava leaves tend to adapt to low light conditions. Exposure to 75–95% reduction in solar radiation reduces leaf life by up to 20 days (Cock et al. 1979). Under limited

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carbon assimilation caused by low solar radiation, assimilates are diverted to shoot growth. Shade also induces a large leaf area per unit weight (Fukai et al. 1984; Ramanujam and Jose 1984). Thus, shade has little effect on the overall LAI development but reduces storage root development more than shoot growth. Under conditions of low soil fertility, particularly when N is limiting, cassava tends to maintain the nutrient status of its leaves by reducing growth and leaf area development (Edwards et al. 1977; Cock and Howeler 1978). Under such conditions, cassava reduces its LAI mainly by decreasing leaf size and branching but maintains a high photosynthetic rate (CIAT 1978). Low air temperatures less than 15°C also cause leaf abscission (Fukai and Hammer 1987). C. Storage Roots Within 5 to 7 days after planting cassava, a rim of callus is formed at the base (distal end) of the stem. Adventitious roots arise from the callus and at the base of the axillary buds and the stipule scar (the nodes) (Cours 1951; Indira and Sinha 1970). Roots arising from the callus (callus roots) are destined to become storage roots. In addition, few roots arising from the nodes (nodal roots) are also capable of becoming storage roots (Indira and Sinha 1970). Starch deposition begins in adventitious roots during the 4th week of cassava growth (at 1 MAP), succeeding secondary thickening and production of xylem parenchyma cells (Cours 1951; Indira and Sinha 1970; Indira and Kurian 1977; Keating 1981). At this time, it is not possible to distinguish anatomically between roots that will bulk and those that will remain as fibrous roots. At about 6 weeks after planting, some of the roots begin to thicken rapidly, laying large quantities of xylem parenchyma that are packed with starch granules and these are destined to become storage roots. The number of storage roots per plant in a cultivar is thus determined early in the growing period and there is little change in the number of storage roots in most cultivars between 2–3 MAP (Cours 1951; Beck 1960; Orioli et al. 1967; Maini et al. 1970; Cock et al. 1979; Tan and Cock 1979; Keating et al. 1982a; Pellet and Sharkawy 1993). The number of storage roots had high positive correlation with the mean LAI, total dry matter, and storage root yield (Vine and Ahmad 1987; Pellet and Sharkey 1993). The number of storage roots varies among cultivars from 5 to 25 per plant (Maini et al. 1970; Connor et al. 1981; Ramanujam 1980; Keating et al. 1982a; Ramanujam and Indira 1983; Manrique 1990b; Pellet and Sharkawy 1993). Storage root number decreased little and the storage root formation was delayed at 22.5°C as

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compared to 27.0°C. Consequently, storage root length and diameter were larger at 27°C (Manrique 1990b). Adverse conditions such as low soil moisture and low light intensity have no effect or little effect on storage root number (Cours 1951; Beck 1960; Orioli et al. 1967; CIAT 1973). However, in one study, decrease in light intensity or increase in shade more than 20% for 12 weeks greatly reduced storage root number per plant (Okoli and Wilson 1986). Root elongation was 50% reduced when sunlight decreased by 32%, but even 78% shade had no effect on storage root initiation (Aresta and Fukai 1984). Soil fertility and the number of shoots per plant affect storage root number per plant. Cassava plants that received fertilizer at monthly intervals had a greater number of storage roots than those that received fertilizer at two months after planting (Orioli et al. 1967). Application of 75–100 kg N/ha increases storage root number per plant (Vijayan and Aiyer 1969; Mandal and Mohankumar 1972; Mohankumar et al. 1975b; Nair 1982). Application of 83 kg K/ha significantly increased storage root number per plant as well as individual storage root weight (Mohankumar et al. 1971; Nair and Aiyer 1986). Plants with more than one shoot produced more storage roots than plants with only one (Enyi 1972a,c). Growth regulators such as indoleacetic acid (IAA), naphthalene acetic acid (NAA), and 2chloroethyltrimethyl ammonium chloride (CCC) enhance the storage root number, whereas carbohydrates such as glucose and sucrose hasten storage root initiation (Indira and Sinha 1970) but have no impact on storage root yield (Indira and Maini 1973). The number of storage roots produced per hectare increased from 24,700 to 48,100 with the increase in plant population from 6,944 to 27,777 per hectare. The increase in plant population from 12,340 to 28,000 per hectare reduced the size of storage roots produced from 219–237g to 155–170g (Mohankumar et al. 1975; Villamayor et al. 1992). However, at high population, plants tend to have fewer storage roots per plant than those at low population (Enyi 1972a,c; CIAT 1974). In rainfed conditions, the storage root growth closely parallels the development of LAI (Ramanujam 1991). However, the rate of bulking of storage roots fluctuates widely (Ramanujam 1977, 1980). Storage root growth rate exceeds shoot growth rate around 3 MAP, and this indicates the beginning of the rapid storage root bulking (Ramanujam 1991; Pellet and Sharkawy 1997). When cassava is planted at the beginning of monsoon, in short duration cultivars (growth period 7–8 months), peak rate of storage root bulking occurs during 6 MAP, whereas in long duration cultivars (growth period 10–12 months), peak rate of storage root bulking occurs during 7 MAP. Between 6–10 MAP, the bulking rate of storage root decreases due to a decrease in soil moisture (due to low precipitation) and a decrease in LAI. If both

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the short and long duration cultivars are allowed to stay on the field for up to 12 months, a second peak rate in storage root bulking occurs around 11 MAP with the development of new canopy utilizing the second monsoon. However, the second peak in bulking rate occurs to an extent lower than the first peak (Ramanujam 1991). The high-yielding cultivar maintains a high rate of storage root bulking for the longest period, whereas the low-yielding cultivar has a low rate of storage root bulking, lasting for a short time (Lian and Cock 1979b). Maximum storage root growth rate occurs at LAI values between 2 and 3 (Cock et al. 1979; Irikura et al. 1979; CIAT 1976; Ramanujam 1991). The rate of bulking of storage root shows positive correlation with the CGR (Boerboom 1978). In acid soils, application of NPK up to 100 kg/ha enhanced DM accumulation in storage roots more than in unfertilized plants (Pellet and Sharkawy 1997). Application of K up to 83 kg/ha increased storage root yield (Mandal and Mohankumar 1969; Mohankumar et al. 1971; Nair and Aiyer 1986; Nair et al. 1980). Storage root bulking and yield was reduced at 22.5°C as compared to 27°C (Manrique 1990bc). Increase in shade more than 20% significantly reduced storage root bulking and storage root yield (Okoli and Wilson 1986). D. Dry Matter Production Dry matter production and the partitioning of DM (carbon assimilates) between shoot and storage root of cassava plant is influenced by several environmental factors such as photoperiod, temperature, light intensity, soil fertility and moisture status, and it differs between genotypes (Boerboom 1978; Tan and Cock 1979; Cock et al. 1979; Cock 1983; Ramanujam and Indira 1983; Manrique 1990c; Ramanujam 1991). Cassava cultivars vary widely in their growth rate. Total dry matter (TDM) produced by cassava varies between 15–47 t/ha in 10–12 months of growth period (Cours 1951; Enyi 1973; Cock et al. 1977; Holmes and Wilson 1977; Lian and Cock 1979b; Wholey and Booth 1979; Keating et al. 1982b; Ramanujam 1991). Some short duration cultivars (7–8 months) produced low TDM (14.7–18.8 t/ha) as compared to long duration cultivars (Ramanujam 1991). Regardless of branching habit, TDM of cassava cultivars continuously increases in a sigmoid pattern up to 12 months (Cours 1951; Williams 1972; Lian and Cock 1979b; Keating et al. 1982b; Ramanujam 1991). Under conditions of very long growth duration (24 months), total dry matter increases steadily from 3 MAP, reaches a peak at about 13 MAP, slows between 13–17 MAP, and then steadily increases up to 24 MAP (Cours 1951). Increase in N application up to 150 kg/ha increased TDM production and storage root yield (Mohankumar and

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Hrishi 1973; Ramanujam 1982b; Manrique 1990a). Increase in N application beyond 150 kg/ha also increased TDM but this was insignificant (Ramanujam 1982a). The combination of long photoperiods (more than 11h) and high temperatures (more than 14°C) high LAIs (more than 3) decrease the proportion of DM allocation to storage roots because under such conditions the shoot became the dominant sink for assimilates (Bolhuis 1966; Lowe et al. 1976; Mahon et al. 1976; Keating et al. 1982c; Manrique 1990c). Crop growth rate (CGR) of cassava varies between 100–150 g/m2/week (CIAT 1972; Cock 1973, 1983, 1984; Enyi 1973; Manrique 1990b). Crop growth rate increases with increase in LAI until the growth rate reaches a maximum and then either remains constant or declines (Cock 1973; Cock et al. 1979; Keating et al. 1982c). The carbohydrate requirement to form and sustain the existing LAI increases linearly with LAI and as the LAI increases above an optimum, less carbohydrate is available for storage root growth. In a tropical environment, optimum LAI needed for the maximum CGR varies between 3 and 4 (CIAT 1972; Cock et al. 1979; Cock 1983; Ramanujam 1991). In a tropical environment, LAI above 4 decreases CGR due to a short leaf life caused by mutual shading with a subsequent reduction in photosynthesis. Under such conditions, a large number of shaded leaves would become net consumers of assimilates (Cock et al. 1979). In a subtropical environment, CGR increases at LAI up to 6–11 depending on temperature or solar radiation, but LAIs 5–6 cause leaf abscission and a decline in storage root growth (Keating et al. 1982a,c). E. Dry Matter Partitioning In cassava, due to simultaneous development of leaf area and storage roots, the current supply of assimilates is partitioned between growth of shoot and storage roots. Under favorable growing conditions (more soil fertility than optimum, particularly N, and moisture), shoot growth dominates over the growth of storage roots, and assimilates are used to develop and sustain shoot growth while little DM accumulates in storage roots. An increase in N application up to 250 kg/ha increased TDM production and DM accumulation in leaves but had no significant effect on DM partitioned to storage roots. The dry storage roots yield increased up to 150 kg N/ha application and application of N more than 150 kg/ha did not significantly increase the dry storage roots yield (Ramanujam 1979, 1991). Between 0–200 kg N/ha, about 62–65% of TDM was partitioned to storage roots (Ramanujam 1991). The storage root yield significantly increased (42.2–88.3%) between 50–150 kg N/ha, as compared to unfertilized plants and further increase in the storage root yield was

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insignificant with the application of 150–250 kg N/ha (Cock 1973; Mohankumar and Hrishi 1973; Ramanujam 1991). Under optimal conditions of soil fertility and moisture, more assimilates tend to accumulate in the storage roots (Cours 1951; Hunt et al. 1977; CIAT 1978; Cock et al. 1979; Tan and Cock 1979; Manrique 1987). In a tropical environment, maximum storage root growth (rate of storage root dry matter increase) occurs at LAI between 3 and 4 and above this LAI, the storage root growth rate decreases (Cock et al. 1979; Irikura et al. 1979). At very high LAI values (more than 4), which result in high CGR, storage root growth rate was minimal (Irikura et al. 1979; Enyi 1972a,b,c; Enyi 1973). In a subtropical environment (mean temperature 27°C), maximum storage root production was attained at LAIs of about 6–8 (Manrique 1990c). These LAIs were two to three times larger than those LAIs considered optimal for an ideal cassava plant in the tropics (Cock et al. 1979). Apparently, LAIs greater than those required in the tropics are needed in subtropical environments for maximum storage root yields. The high storage root yield at high LAIs in a subtropical environment was presumably due to a relatively small amount of dry matter used to maintain high LAI. Thus, in the absence of a large sink capacity for LAI maintenance, the excess available DM was used for storage root growth (Manrique 1990c). There is high positive correlation between the TDM produced and DM accumulated in storage roots (Williams 1974; Boerboom 1978; Keating et al. 1982c; Ramanujam and Biradar 1987; Ramanujam 1991; Pellet and Sharkawy 1993) but TDM does not necessarily lead to a high storage root yield (Williams and Ghazali 1969; Cock 1976). During the initial 3 months of growth, cassava cultivars tend to accumulate more DM in leaves than in stem and storage roots. After 3 months, more DM accumulates in storage roots than in the rest of the plant parts and the storage roots continue to accumulate DM until the time of harvest (Wholey and Booth 1979; Ramanujam 1985, 1991; Manrique 1987). Profusely branching cultivars accumulate more DM in the shoot (Ramanujam and Indira 1983; Ramanujam 1985) than in the storage roots. Non-branching or partially branching cultivars accumulate more DM in storage roots than in the shoot (Ramanujam 1985). Proportion of DM partitioned to the storage roots steadily increases up to 4–6 MAP and then remains constant (Lian and Cock 1979b; Keating et al. 1982c; Ramanujam 1991). DM partitioning also remained constant at about 40% when cassava cultivars grew for a period of more than 16 months (Wholey and Booth 1979). High-yielding cultivars (30–40 t/ha) partitioned 50–80% of TDM to storage roots and the low-yielding cultivars partitioned less than 50% of TDM to storage roots (CIAT 1972;

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Enyi 1972a,b; Wholey and Booth 1979; Ramanujam 1991). Low solar radiation tends to limit the DM allocation to storage root growth, and delays storage root enlargement (Cock 1984; Fukai et al. 1984; Kasele et al. 1984; Ramanujam and Jose 1984; Ramanujam et al. 1984). Supplementary irrigation during drought increases TDM production, CGR, DM partitioning to storage roots, and storage root yield (Nayar et al. 1985). F. Plant Population One of the limiting factors for cassava storage root yield is a low LAI after 6 months due to decrease in rainfall (Sinha and Nair 1971; Cock 1973; Ramanujam 1991) often due to a decrease in soil moisture because of a decrease in rainfall. Increasing the plant population may increase LAI and light interception, which subsequently may increase DM production and yield. The storage root yield-plant population response curve is a function of cultivar morphology (branching, leaf size, leaf area) and is influenced by crop age, high soil moisture, and fertility, particularly N, which favor vegetative growth. However, cultivars vary widely in their response to an increase in plant population. Cultivars with an early and profusely branching habit with broad leaves and high LAI need wider spacing (1.0 × 1.0 m or more) and may be planted at low plant density, but cultivars with a tall and late branching habit may be planted at 90 × 90 cm spacing. Short, nonbranching cultivars need closer spacing (75 × 75 cm) and may be planted at high plant density. Planting at closer spacing may increase CGR, but generally decreases the carbohydrate supply available within each individual plant. At closer spacing, the carbohydrate supply to the storage root is limited and thus the growth of the storage root is source rather than sink limited. An increase in plant population, beyond the optimum number, may cause internode elongation due to decrease in light penetration inside the canopy, and increase plant height, which would consume more assimilates. This in turn reduces the carbohydrates available for storage roots (Cock et al. 1977; Hunt et al. 1977). In areas with low precipitation, the shoot growth will be reduced and hence cultivars may be planted at closer spacing at high plant density. Plant populations at which cassava cultivars are grown widely vary between 10,000 and 20,000 (Tardieu and Fauche 1961; Rodriguez et al. 1966; Gurnah 1973). In India, in areas of high precipitation (1,000–3,000 mm), cassava cultivars with branching habit are grown at a spacing of 90 × 90 cm (12,345 plants/ha) or at a spacing of 1.0 × 1.0 m (10,000 plants/ha) in a pure stand, and cultivars with nonbranching habit are planted at 75 × 75 cm (Mandal et al. 1973). In areas

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with less than 1,000 mm precipitation, cassava is planted at a closer spacing of 60 × 60 cm (27,777 plants/ha) or 75 × 75 cm (17,857 plants/ha) (Ranganathan 2000). Fresh storage root yield increases with crop age for all cultivars at any given plant population (Cock et al. 1977). Densely populated plants were less efficient in storage root production as compared to less densely populated ones. The optimum plant population for highest storage root yield varies widely among cassava cultivars. Increase in plant population from 12,000/ha to 30,000/ha decreased storage root number by about 26–55% and weight of individual storage roots by about 28–50% (Mohankumar and Mandal 1972; Mohankumar et al. 1975a; Cock et al. 1977). Shoot number per plant has a significant effect both on total TDM yield and on storage root yield. In single shoot plants, the TDM production increased with population up to 12,500 plants/ha but that of multiple shoot plants decreased from 47% to 37% as population increased above 6,000 plants/ha (Enyi 1972a,b). In cultivars with multiple shoots, storage root yield may be increased at low population (Chan 1970; Shanmugam and Srinivasan 1973) but the yield either decreased at high population or did not change at intermediate population (Enyi 1972c). In a cultivar with less-vigorous, short-stature, branching habit, and low leaf area, storage root yield increased up to 10,000 plants/ha and remained constant (55 t/ha) with further increase in plant population up to 40,000 plants/ha. In a less-vigorous cultivar with medium-height and very late branching habit, storage root yield increased up to 10,000 plants/ha, remained constant (55 t/ha) up to about 30,000 plants/ha, and then declined with further increase in plant population (Cock et al. 1977). In cultivars with medium-height, profusely branching habit and narrow leaves, or vigorous, tall, branching habit with broad leaves, storage root yield remained constant (40–45 t/ha) up to 10,000 plants/ha, after which the yield declined drastically. In a cultivar with medium height, broad leaves and variable branching habit, storage root yield increased up to 6,000 plants/ha (28 t/ha), after which the yield declined (Cock et al. 1977). In cultivars with less-vigorous, medium-height, very late branching habit, or non-vigorous, short-stature, branching habit with low leaf area, or medium-height, profusely branching habit with narrow leaves, at 4 MAP, light interception increased from 35–75% to 70–90% with increase in plant population from 5,000 to 40,000/ha. In a tall cultivar, light interception remained almost constant at about 85%, but in a cultivar with vigorous, tall, branching habit with broad leaves, light interception decreased from 80–70% with increase in plant population from 5,000 to 40,000/ha (Cock et al. 1977). The cultivar with non-

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vigorous, short-stature, branching habit with low leaf area tended to allocate about 70% of DM to storage roots in a population of 5,000–12,000 plants/ha, and about 60% DM to storage roots in a population of more than 12,000 plants/ha. In cultivars with medium-height, profusely branching habit and narrow leaves, or vigorous, tall, branching habit with broad leaves, or medium height, broad leaves and variable branching habit, the proportion of DM allotted to storage roots gradually decreased with an increase in population between 5,000 and 40,000 plants/ ha (Cock et al. 1977). A cultivar with multiple shoot decreased partitioning of DM to storage roots from 45% to 37% when the plant population was doubled from 6,000 to 12,000 plants/ha (Enyi 1972b). Storage root DM and yield decreased in a tall (3 m), profusely branching cultivar, as plant population increased from 8,000 to 20,000 plants/ha (Maduakor and Lal 1989). In tall (3 m), branching or nonbranching cultivars, maximum storage root yield was obtained at a population of 12,340 plants/ha, but a short, nonbranching cultivar, that yielded low at this population, yielded high at high plant density (17,770 plants/ha) (Ramanujam 1991). Thus, cultivars that are not very vigorous, shortbranching or medium-height, and very late branching, and show an increase in light interception with increase in plant population tend to yield high at higher plant population. Cultivars with vigorous, tall, and profusely branching habit, although tending to intercept high solar radiation, yield low because of increase in allocation of DM to shoot growth and loss of LAI due to increased leaf fall at higher plant population (Cock et al. 1977). Thus, in cassava, cultivar and the environment influence storage root yield. High storage root yield is associated with optimum leaf area for intercepting maximum solar radiation, vertical orientation of foliage to allow maximum light transmission, high assimilation and low respiration rates, high DM partitioning to storage roots, optimum plant population, and high sink activity. G. Starch Yield Cassava storage root contains 20–41% starch (expressed as a percentage of storage root weight) on a fresh weight basis (Maini et al. 1970; Obigbesan and Agboola 1973; Pushpadas and Aiyer 1976; Wholey and Booth 1979; Ramanujam 1980; Balagopalan et al. 1988; CTCRI 1998; Sriroth et al. 1998; Ravi 2001) or 50–86% on a dry weight basis (Maini 1970; Kurian et al. 1973; Ketiku and Oyenuga 1972; Rickard et al. 1991; Blanshard 1995). Starch yield varies between 5 and 17 t/ha when harvested 10–12 MAP (Nair 1969; Mandal et al. 1969, 1971a; Pushpadas and Aiyer

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1976; Boerboom 1978; Wholey and Booth 1979; Sriroth et al. 1998). Storage roots contain more than 80% starch on a dry weight basis at temperatures less than 24°C but starch content decreases at higher temperatures (Irikura et al. 1979). Starch content of storage root was less for the plants grown at 30,000 plants/ha than for those grown at 3000 plants/ha (Cours 1951; Enyi 1972c). Planting at too wide spacing (3.0 × 3.0 m) also decreased starch content and starch yield as compared to normal spacing (1.0 × 1.0 m) (Wholey and Booth 1979). Starch content of storage root increases with age of the crop but tends to fluctuate due to the fluctuations in precipitation and subsequent changes in the development of leaf area. When cassava grows under tropical rainfed conditions, starch content continues to increase from 3 MAP and tends to decrease during a dry season with a subsequent fall in LAI, which normally occurs between 7–10 MAP. If cassava is allowed to stay on the field until the next monsoon season, the starch content initially decreases little due to the development of leaves and then steadily increases after the establishment of canopy (Cours 1951; Maini et al. 1970; Wholey and Booth 1979). Cultivar differences exist not only in starch content of storage roots but also in time of maximum starch content (Maini et al. 1970; Ketigu and Oyenuga 1972; Obigbesan and Agboola 1973; Cock 1976). In some cultivars, the highest starch content (22–33% on a fresh weight basis) was found at 15–16 MAP (Maini et al. 1970; Obigbesan and Agboola 1973; Wholey and Booth 1979). In some other cultivars, maximum starch content was found between 6–10 MAP (Sinha and Indira 1971; Kurian et al. 1973; Kurian and Maini 1974; Ramanujam 1977). Thus, each cultivar has an optimum time of harvest for starch extraction and this is influenced by cultural practices or climatic conditions. Application of N (up to 150 kg/ha) and K (up to 84 kg/ha) increases starch content of cassava storage roots (Mandal et al. 1969; Vijayan and Aiyer 1969; Nair 1969; Maini et al. 1970; Pushpadas and Aiyer 1976; Nair 1976; Wholey and Booth 1979; Nair et al. 1980; CIAT 1981; Nair and Aiyer 1986).

III. GROWTH AND PRODUCTIVITY OF ASSOCIATE CROPS A. Cowpea Cowpea (Vigna unguiculata) is a widely adapted, drought tolerant legume grown on about 7 million ha in warm to hot regions of the world (Ehlers and Hall 1997). Cowpea (Vigna unguiculata) has three sub-

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species: sub-species unguiculata is the common grain cowpea; subspecies cylindrica is a fodder and grain type from India; sub-species sesquipedalis is the yard-long bean from India and its green pod is used as a vegetable (Wien and Summerfield 1984). Cowpeas are grown for nutritious grains (seeds) for human consumption as food, immature pods as vegetable, and vegetative parts as fodder. Mature cowpea grains contain about 17–33% protein, 60% carbohydrate, and 1.4–2.7% oil (Aykroyd and Doughty 1964; Chatterjee and Bhattacharyya 1986; Nielsen et al. 1993). Due to its efficient nitrogen fixing capacity, the crop is also used as green manure. Cowpea cultivars vary widely in their morphology, flowering time, and maturity. Plant architectural traits (determinacy, branch angle, and internode length) interact with flowering time to determine the basic plant size and shape (Ehlers 1984). Plant density, day length, temperature, soil moisture, and insect damage also influence plant development and architecture. Long day lengths may significantly delay flowering in cultivars that are erect and mature early in short day environments, and the cultivar may show a prostrate growth habit (Ehlers and Hall 1997). Cowpea cultivars may be semi-spreading, spreading (prostrate), tallerect, or dwarf-erect and compact type (Chatterjee and Bhattacharyya 1986; Ehlers and Hall 1997). Cowpea plants grow faster, and attain full ground cover in about 30 DAS. The canopy attains maximum light interception at a LAI of 3 by 35–40 days after emergence at densities ranging between 7–16 plants/m2 (IITA 1973; Littleton et al. 1979; Chaturvedi et al. 1980; Wien 1982; Mason et al. 1986b). The photosynthetic rate steadily declines between 6–13 weeks after emergence (WAE), but picking of pods at 7–8th WAE slows the decline of photosynthetic rate. Cowpeas are day-neutral (insensitive to photoperiod), or short day plants, but many cultivars are photoperiod sensitive (Ehlers and Hall 1996). Flowering is influenced by photoperiod and air temperature (Littleton et al. 1979; Wein and Summerfield 1980; Hadley et al. 1983; Dow El-Madina and Hall 1986; Ehlers and Hall 1996). Night temperatures exceeding 20°C and long days (14 h) slow down or inhibit floral bud development and cause significant reduction in grain yield (Warrag and Hall 1984; Nielsen and Hall 1985; Dow El-Madina and Hall 1986; Patel and Hall 1990). Early maturing cultivars of cowpea yield in 60–90 days after sowing (DAS), but late maturing cultivars yield in 100–130 DAS (Singh and Ntare 1985; Chatterjee and Bhattacharyya 1986). Grain yield of cowpea cultivars varies between 0.5 and 2 t/ha (Chatterjee and Bhattacharyya 1986) but dry grain yields above 7 t/ha have been achieved under experimental conditions (Sanden 1993). The optimum day/night temperature regime for highest grain yield is 27/22°C (Bagnall

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and King 1987). A day/night temperature regime of 21/16°C depresses grain growth, and a day/night temperature regime of 33/28°C depresses pod formation, resulting in 100 and 40% reduction in grain yield, respectively. Optimum plant population for maximum yield varies among cultivars. Shoot dry matter continuously increases from 5 weeks after seedling emergence (WAE) up to the 10th week, and thereafter increases little at a population of 100,000 plants/ha or decreases little at a population of 400,000 plants/ha at the 13th WAE. Shoot dry matter production was greater at high plant density than at low plant density (Kwapata et al. 1990). Cultivars produce the greatest grain yield at 100,000 to 200,000 plants/ha (Nangju et al. 1975; Kayode and Odulaja 1985; Kwapata and Hall 1990), or at 400,000 plants/ha (Kwapata and Hall 1990). Grain yield of some bush-type cowpea cultivars increases by 26–60% with an increasing plant population between 100,000–400,000 plants/ha (Kwapata and Hall 1990). High plant density (400,000 plants/ha) intercepts greater photosynthetically active radiation (PAR) than low plant density (100,000 plants/ha) (Kwapata et al. 1990). In high plant density, PAR interception continuously increases exponentially beginning at 2 WAE, reaches maximum (94%) at 7 WAE, and declines little (2–4%) at 10 WAE. In low plant density, PAR interception continuously and exponentially increases beginning at 2 WAE, reaches maximum 60–88% at 7–9 WAE, and remains the same up to 10 WAE. Cultivar differences in responsiveness to plant population were not associated with differences in plant morphology because grain yield in cowpea is not associated with the plant size or canopy characteristics of the different cultivars but with the efficiency of partitioning of photosynthate to grain during grain development and maturation. Changes in plant population had little effect on harvest indices for both the vegetable and grain cowpea cultivars (Kwapata 1989; Kwapata and Hall 1990). Shade has relatively little effect on cowpea seed yield. Shade (50% reduction in sunlight) throughout or from first flowering onwards reduced seed yield by 25% primarily due to the reduction in pod number (Summerfield et al. 1976). B. Peanut Peanut (also groundnut) (Arachis hypogaea) is an annual herb of indeterminate growth habit and is cultivated around the world in tropical, subtropical, and warm temperate climates. Peanut cultivars are divided into two subspecies each of which has been subdivided into two botanical varieties (Krapovickas 1969; Wynne and Gregory 1981; Stalker

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1997). Virginia type (subsp. hypogaea var. hypogaea) cultivars are bunch or runner type, long season plants, and so are not suitable for arid regions. Runner or spreading type cultivars (subsp. hypogaea var. hirsute) are alternately branched, prostrate, diageotropic, and have a relatively long growing season. Valencia type cultivars (subsp. fastigata var. fastigata) are red seeded peanuts. Spanish type cultivars (subsp. fastigata var. vulgaris) are erect (bunch) types, sequentially and densely branched, the branches are ascending, negatively geotropic, have a relatively short growing season and are suitable for dry-land conditions. Peanut seeds contain about 25–35% protein, 5–15% carbohydrate, and 36–56% oil (Woodroof 1966; Cobb and Johnson 1973; Ahmed and Young 1982; Ashley 1984; Chatterjee and Bhattacharyya 1986; Jadhao et al. 1993; Naveen et al. 1992; Nandania et al. 1992; Knauft and OziasAkins 1995). Peanuts are grown for seeds for extracting oil and for human consumption as food. In addition to seeds, the vine and foliage is an important fodder, and the meal remaining after oil extraction from the seeds, which contain 52% protein (Woodroof 1966), is used as animal feed, and as manure because it contains 6.5–7.5% N. Peanut plants grow faster and the canopy attains maximum light interception (95%) at a LAI of 3 in about 55–65 DAS (Duncan et al. 1978; Mason et al. 1986b; Singh et al. 1994). In a spreading type, LAI increased from 4 to 5.9 during 77–105 DAS, and after that it declined, apparently due to leaf senescence and abscission. Here, LAI 5 intercepts 95% solar radiation. Light interception remained relatively constant (95%) between 77–133 DAS. The photosynthetic rate remained constant between 63 and 105 DAS but drastically declined between 105 and 133 DAS to about 50% of that in 63 days (Jones et al. 1982). Cultivars intercepting 80% light between 60–100 DAS with a peak (90%) at 90 DAS have also been reported (Reddy et al. 1980). Row spacing and plant population significantly influence canopy development, LAI, and light interception (Gardner and Auma 1989; Singh et al. 1994). At a uniform plant population (95,000 plants/ha), canopy light interception, vegetative and reproductive growth, LAI, total dry matter, and pod and kernal yields increased to the maximum at nearly equidistant spacing (35 cm between rows × 30 cm between plants within rows) than wide-row spacings (70 cm between rows × 15 cm between plants within rows or 105 cm between rows × 10 cm between plants within rows). Plants in widerow spacings intercepted less solar radiation and used it less efficiently as compared to the equidistant spacing. The critical LAI was 6.0 for wide-row spacing (105 cm between rows × 10 cm between plants within rows), indicating that about 40% more leaf area is required to intercept 95% of solar radiation in wide-row spacing than in the equidistant

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spacing (Gardner and Auma 1989). In several cultivars with diverse growth habit, and all planted at a uniform plant population, canopy closure, LAI, light interception, CGR, and pod yields were greater in narrow (46 × 15 cm) and paired-rows (69–23 × 15 cm) than in conventional hedge rows (91 × 8 cm) (Jaaffar and Gardner 1988). An increase in population up to 400,000 plants/ha and an increase in row spacing up to 30 cm increased the rate of canopy development, LAI (more than 5), light interception (90%), total dry matter production, and the pod yield (4.2 t/ha) (Singh et al. 1994). Maximum pod yields (2.1–3.1 t/ha) at a population ranging between 64,000 and 74,400/ha have also been reported in bunch types of cultivars (Cahaner and Ashri 1974). In a branched, spreading type of cultivar, the pod and kernel yields were similar from 88,000 to 394,000 plants/ha (6.5 t/ha pods or 4.9 t/ha kernels), after which the yields declined to 5.7 t/ha pods or 4.3 t/ha kernels (Bell et al. 1987). In one study, pod yields of peanut planted at the spacing of 30 × 10 cm (333,000 plants/ha), and 45 × 10 cm and 30 × 15 cm (222,000 plants/ha) were similar (3.4 t/ha) (Jadhao et al. 1993). The world average pod yield was 1.3 t/ha, while the maximum pod yield up to 6.1 t/ha was obtained (FAO 2001). Peanut plants do not grow well in acid soils and soils that have high moisture but poor drainage. Because peanut plants require more calcium (Ca) for normal seed development, and it must be absorbed directly by the pod, Ca is the critical nutrient for peanut production (Sumner et al. 1988; Adams et al. 1993). The plant has a taproot system but many lateral roots develop about 3 days after germination. Although roots can grow 135 cm deep, they are generally concentrated at a depth of 5–35 cm below the soil surface (Intorzato and Tella 1960; Robertson et al. 1979). Meisner and Karnok (1992) reported that by 20 DAP, roots were extended to a depth of 40 cm, representing 32% of the total root lengths. By 50 DAP, roots were found extended to the 70 cm depth and represented 63% of the total root lengths. By 80 DAP, 95% of the total root lengths were found to be established. Photoperiod, temperature, and relative humidity (RH) determine pod set. Peanut plants are insensitive to photoperiod, but respond to photoperiod. Short-day conditions (9 h light/15 h dark) reduce plant height and total plant weight more than long-day conditions (9 h light/15 h dark period being interrupted by 3 h light). Plants under both short- and long-day conditions flower and produce pegs, but plants under short-day conditions flower later than plants grown under long days. However, plants grown under short-day conditions produce more pods, presumably due to a greater percentage of fertilization than is received by plants grown in long days (Wynne et al. 1973). Optimum temperature for veg-

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etative and reproductive growth varies among cultivars. Optimum air temperatures for vegetative growth range between 25 and 30°C and temperatures for reproductive growth may be similar or somewhat lower (20–25°C) (Ketring 1984). Day air temperature exceeding 30°C is detrimental for vegetative growth and pod yield of peanut plants (Cox 1979; Ketring 1984). Air temperatures ranging between 30 and 35°C significantly reduced leaf areas and dry weights of shoots (Ketring 1984). Usually, flowering begins 30–40 days after sowing, with a peak of flower production at 6 weeks later, and the number of flowers produced per day decreases as seeds mature (Hang et al. 1984; Gardner and Auma 1989; Stalker 1997). Cultivars attain maximum DM production (4.9–16 t/ha) at about 100–133 days after sowing (DAS) (Reddy et al. 1980; Willey et al. 1981; Hang et al. 1984). The erect types yield in 90–120 DAS, whereas the spreading types are usually late maturing (120–160 DAS). The pod yield of erect and spreading types varies between 0.8–7.1 t/ha. (Cahaner and Ashri 1974; Duncan et al. 1978; Hang et al. 1984; Naveen et al. 1992; Nandania et al. 1992). Artificial shade (75% reduction in full sunlight) during the peak flowering period reduces the number of flowers per plant, and inhibits peg formation. Shade during the pegging and podding phases reduce total peg, pod number, and pod dry weight. Shade during the maturing phase or after peak flowering reduces seed filling, which significantly decreases kernel size (Hudgens and McCloud 1975; Hang et al. 1984). On the average, 75% artificial shade decreases the growth rate of vegetative parts by 85%, the reproductive parts by 67%, and the total biomass by 66% compared to plants grown under full sunlight (Hang et al. 1984). Shade significantly reduces pod and seed yield 10.7–16.7% and 19.8–23%, respectively, only when the duration was for a 3–4-week period. Shade during the flowering (41–83 DAS) does not substantially reduce pod and seed yield, because the plants have adequate time to recover from the loss of active flowers and subsequently bear flowers and produce a normal number of pods (Hang et al. 1984). Shade during the podding phase (83–104 DAS) substantially reduces pod and seed yield 17.9 and 16.9%, respectively. Shade during the maturity phase (104–125 DAS) decreases seed yield 22%, primarily by decreasing seed filling in existing pods (Hang et al. 1984). Decrease in light intensity from 75 to 20% of full sunlight proportionately decreases the rate of photosynthesis and translocation of assimilates to the pods. Shade imposed during the podding phase (70–145 DAS) had more adverse effects on the translocation of assimilates than shade imposed during the flowering and late pod filling periods, which decreased pod yield (Sengupta and Jadhav 1988; Jadhav et al. 1993). Thus, low light intensity (shade) dur-

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ing pod development would substantially affect pod yield due to both a decrease in photosynthesis as well as reduced translocation of assimilates to the pods. C. Soybean Soybean (Glycine max) is a warm season legume and is mostly cultivated in temperate zones of the northern and southern hemispheres (Burton 1997). Soybeans are grown for seeds for extracting oil, that is used in a variety of food and industrial products. The remaining protein meal is primarily used as an animal feed or human food. Dry soybean seeds contain about 31.5–46.9% protein, 34% carbohydrate, and 15.7–24% oil (Rubel et al. 1972; Burton and Brim 1981; Kilen 1990; Hartwig and Kilen 1991; Khelkar et al. 1991; Khandait et al. 1991; Cober and Tanner 1995; Mansur and Orf 1995; Burton 1997; Kane et al. 1997). Soybean cultivars have an erect growth habit, and may have a single main stem with no branching or various degrees of branching. Cultivars may be determinate, indeterminate, or semi-determinate in their growth habit (Hartung et al. 1981). In semi-determinate types, the terminal bud ceases vegetative activity a little earlier than the indeterminate (ID) types. In determinate (D) types, the stem growth terminates abruptly at the onset of flowering (Hartwig 1973) or shortly after flowering (Bernard 1972), while in the ID types, stem growth and leaf production continue for several weeks after flowering has begun. During pod and seed set, vegetative dry weight increases about 3-fold in ID types (Hanway and Weber 1971) and about 2 units of LAI are formed (Weber et al. 1966). Thus, the potential for competition for photosynthate between vegetative and reproductive growth is greater in ID types than in D types, which may be detrimental to yield (Bernard 1972; Beaver et al. 1985). However, ID types begin to flower 2 weeks earlier, and the longer period of flowering and pod set may partially compensate for the competition between vegetative and reproductive growth in ID types (Egli and Leggett 1973; Shibles et al. 1975). When pod and seed development begin, the pods are the primary sink for photosynthate, with only limited competition from the vegetative portion of the plant regardless of the growth habit. This results in very little difference in seed yield between the D and ID types (Egli and Leggett 1973; Egli et al. 1980). Seed yield of both ID and D types were the same if they had the same maturity and length of reproductive period (Green et al. 1977). Soybean cultivars vary in height between 53 and 117 cm (Chang et al. 1982; Beaver et al. 1985; Foley et al. 1986; Cober and Tanner 1995; Mansur and Orf 1995; Steele and Grabau 1997). Soybean plants produce

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maximum LAI (4–9) at about 50–80 DAP and achieve 95% light interception at an LAI of 3.5–4.0 (Koller et al. 1970; Herbert and Litchfield 1984; Beaver et al. 1985; Board and Harville 1993; Rochette et al. 1995; Pengelly et al. 1999). Total dry matter, dry weight of stem and leaves of a soybean plant, increases in a sigmoid pattern. The total dry weight of a soybean plant was at its maximum at about 110 DAP and the dry weight of stem and leaves was at its maximum at about 80–89 DAP. The CGR was highest between 76–86 DAP. Seed dry matter began to increase 30 DAP and reached its maximum at 110 DAP (Koller et al. 1970; Egli and Leggett 1973). The HI of soybean cultivars varies between 25–65% and the D types partition more dry matter to the seeds than the ID types (Schapaugh and Wilcox 1980; Beaver et al. 1985). Branching is strongly influenced by plant population and more branching occurs at low plant density (Burton 1997). The D types produce more branch dry weight due to having a greater number of branches than the ID types (Beaver et al. 1985). Plant populations that produce maximum soybean seed yields depend on several factors, including row spacing, cultivar, and planting season. The optimum population for maximum soybean seed yield varies among cultivars and ranges between 180,000 and 800,000 plants/ha (Wilcox 1974; Cooper 1977; Costa et al. 1980; Herbert and Litchfield 1982, 1984; Willcott et al. 1984; Beaty et al. 1982; Parvez et al. 1989; Board et al. 1990; Khelkar et al. 1991; Khandait et al. 1991; Prasad et al. 1993; Sharma and Sharma 1993). Soybean seed yield is at its maximum at narrow row spacings (25–50 cm) rather than at spacings more than 50 cm (Shibles and Weber 1966; Cooper 1977; Costa et al. 1980; Beaty et al. 1982; Chang et al. 1982; Herbert and Litchfield 1982, 1984; Taylor et al. 1982; Willcott et al. 1984; Ethredge et al. 1989; Board et al. 1990; Porwal et al. 1991; Rajput et al. 1991; Bowers et al. 2000). Soybean planted in narrow rows (25–50 cm) had a higher LAI, intercepted more light, and yielded more than soybeans grown in wide rows (75 cm or above) (Shibles and Weber 1966; Taylor et al. 1982; Willcott et al. 1984; Board et al. 1994). At this range of plant populations and plant spacings, soybean seed yields vary between 1.4 and 5.7 t/ha (Beaty et al. 1982; Herbert and Litchfield 1984; Willcott et al. 1984; Khelkar et al. 1991; Khandait et al. 1991; Prasad et al. 1993; Sharma and Sharma 1993). The world average seed yield was 2.2 t/ha, while a maximum seed yield up to 3.5 t/ha was obtained (FAO 2001). Soybean has a tap root system with secondary roots developing from the taproot, and several fibrous, branch roots developing from the secondary roots (Carlson 1973). Growth and development of soybean roots occur in three phases. Downward tap and shallow horizontal lateral root

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growth accompany shoot growth; root development to the 76 cm depth accompanies flowering and pod formation, and deep penetration of several lateral roots occur during seed maturity (Mitchell and Russell 1973). Soil texture and moisture, cultural practices, and plant population influence the root growth and rooting depth of taproot and branch roots (Carlson 1973; Barber 1978; Robertson et al. 1980; Huck and Davis 1976). Soybean roots have been observed as deep as 1.5 to 2.0 m below the soil surface under normal field conditions (Kasper et al. 1984; Mayaki et al. 1976). Both tap root and branch root elongation account for root extension into deeper soil regions (Raper and Barber 1970; Taylor et al. 1978). In drought conditions, a low density of roots in the dry surface layer and a maximum root proliferation in the deeper, wetter soil layers occurs (Sivakumar et al. 1977; Boyer et al. 1980; Garay and Wilhelm 1983). Drought stress during later vegetative growth or early reproductive development also increases root growth rate (Hoogenboom et al. 1987). At physiological maturity, root growth may cease and some amount of roots may be lost due to decomposition (Brown 1984). At physiological maturity, 67% of soybean root dry matter was in the 0–5 cm layer and 80% in the 0–90 cm layer of the irrigated soybean as compared to 51–83% respectively for the nonirrigated soybean (Mayaki et al. 1976). The root density increases with depth until reaching a maximum concentration at 20–40 cm depth, with a constant decreasing concentration below (Arya et al. 1975). Thus, root dry matter varies less with depth than did root length density because large roots in the upper layer contribute greatly to dry matter but not to root length. The rooting pattern of soybean differs between single plant plots and row plots, suggesting an antagonism between the root system of plants in adjacent rows. In single plant plots, the primary branches tend to leave the taproot, and continue downward through the soil (up to 60 cm). In the row plots, the primary branches extend outward toward the center of rows for varying lengths (30–45 cm), then angle sharply downward at midrow. Once the lateral roots turn downward, they attain the same depth as the taproot. In both, second order roots penetrate vertically (Raper and Barber 1970). Cultivars are photoperiod sensitive, and flowering and pod maturity are generally influenced by seasonal temperature and photoperiod (Ecochard 1985; Summerfield and Roberts 1985; Tanasch and Gretzmacher 1991). Soybean cultivars need 14–15 h of photoperiod after emergence in order to make sufficient vegetative growth and produce a satisfactory yield (Hartwig 1954; Settimi and Board 1988). Determinate types need 42–58 days to first flowering under day lengths of 14–14.5 h, depending on temperature and other growing conditions (Hartwig

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1970; Huxley and Summerfield 1974; Huxley et al. 1976). Short day length (less than 14 h) induces premature flowering (Board and Hall 1984) and reduces vegetative growth (Boerma et al. 1982; Board and Hall 1984), causing reduction in seed yield. Thus, short photoperiod decreases plant height, reduces branch development, number of days to flowering, seed fill period, LAI, light interception, and decreases the length of vegetative and reproductive periods of development (Dunphy et al. 1979; Beaver and Johnson 1981; Parker et al. 1981; Boquet et al. 1983; Board and Hall 1984; Board 1985; Raymer and Bernard 1988; Settimi and Board 1988; Weaver et al. 1991). The short day requirement for appearance of flowers and for high flower production differs. Termination of short day treatment at or before first flowering followed by long day treatment either inhibited or reduced flower production. Therefore, to sustain a high level of flower production during the flowering period, a continuous exposure to floral stimulus (short day length 14–15 h) is necessary for maximum flower production (Settimi and Board 1988). Because a large proportion of the seed yield from determinate soybean comes from the branches (Ramseur et al. 1984; Board 1985), short day induced reduction in branch development decreases seed yield. Under short-day conditions, a minimum of 45 days from emergence to early bloom is required to permit the vegetative growth necessary to produce moderate seed yields (Hartwig 1970). In short-day conditions, adequate vegetative growth is only probably attainable in day-neutral cultivars that produce adequate vegetative growth under all photoperiod conditions or in a cultivar with delayed flowering under short-day conditions. Day-neutral or photoperiod insensitive cultivars flowered in 25–37 days under photoperiods ranging between 12–24 h (Criswell and Hume 1972; Polson 1972). Long day length (16 h) inhibits flower production (Settimi and Board 1988), and thus may affect soybean seed yields. The number of days from planting until first flower and pod formation increases with long photoperiod (24 h) compared to 12 h photoperiod (Criswell and Hume 1972). The early-maturing soybean cultivars are less sensitive to photoperiod than late-maturing cultivars (Johnson et al. 1960; Criswell and Hume 1972). Cultivars insensitive to photoperiod have also been reported (Criswell and Hume 1972; Polson 1972). Cultivars attain physiological maturity in 130–150 days after emergence or earlier (87–112 days) (Gbikpi and Crookston 1981; Cober and Tanner 1995; Mansur and Orf 1995). Cool temperatures delay flowering in soybean (Major et al. 1975). Cool temperatures also affect fertilization and pod formation, while drought and high temperatures cause flower shedding (Van Shaik and Probst 1958; Hume and Jackson 1981). Seed

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yield of soybean increases as the day/night temperature increases between 18/12°C and 26/20°C, but yield decreases at higher temperatures (Huxley et al. 1976; Sionit et al. 1987; Dornbos and Mullen 1991). An increase in night temperature from 10°C to 24°C increases seed yield (Seddigh and Jollif 1984). Seed yield of soybean was reduced more than 15% when 75% artificial shade occurred just prior to flowering, after flowering, during the pod enlargement phase, and during the seed-filling period (Prine 1976). Imposition of 63% of artificial shade during the reproductive period has also been reported to reduce seed yield by about 23–54.8% (Egli and Zhen-Wen 1991; Egli 1993; Jiang and Egli 1995; Egli 1997). Soybeans acclimate to the light environment (Beuerlein and Pendleton 1971; Bowes et al. 1972). Soybeans grown in a low-light environment saturated at low-light intensity and photosynthesized at low rates. Conversely, leaves from plants grown at a high-light intensity saturated at the high-light intensity and had the highest rate of photosynthesis (Burn and Cooper 1967; Dreger et al. 1969; Keck et al. 1970; Beuerlein and Pendleton 1971; Bowes et al. 1972). D. Pigeonpea Pigeonpea (also red gram) (Cajanus cajan) is an erect, shrubby, perennial grain legume but is cultivated as an annual crop in tropical and subtropical regions of the world. In East Africa, pigeonpea is intercropped in the first year but is then allowed to perennate as a sole crop in subsequent years. In India, pigeonpea is more commonly grown as an annual, particularly the early maturing cultivars. Though found in a wide range of agro-climatic conditions, its deep rooting and drought tolerant characters make it a suitable crop in areas of low and uncertain rainfall (about 600 mm) and on the lighter soils. Pigeonpea seeds contain about 21.8% protein (Hulse 1975; Pushpamma 1975), that is consumed as human food. Cultivars may be early maturing (120–150 days), medium (intermediate) maturing (160–200 days), or late maturing (200–280 days) (Ramanujam 1981; Roy Sharma et al. 1981; Chatterjee and Bhattacharyya 1986). However, if allowed to stay on the land, the crop may produce seeds for 3–4 years. Cultivars may be either dwarf type, which may grow up to 1.2 m in height, or tall type, which grow up to 3 m in height. The plant has a bushy growth habit due to its ascending branches. It is a short-day plant with a 13 h critical day length (Roy Sharma et al. 1981) but day-neutral cultivars have also been reported (Turnbull et al. 1981). In one study, most of the cultivars flowered in a natural day length (14.8 h), but flowering was delayed up to 25 days by exposure to

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extended daylength (16 h) (Wallis et al. 1981). Reduction in photoperiod (8 h) or increase in temperature more than 24/16°C also delayed flowering (Turnbull et al. 1981). Pigeonpea grows slowly in the early stage, and shows a less dense canopy area. In early-maturing cultivars, at 30 days after sowing (DAS), light interception remains less than 10%, and at 60 DAS, it hardly reaches 50%. Peak light interception (84%) by pigeonpea occurs at about 100 DAS (Willey et al. 1981). There is an initial lag phase in DM accumulation in pigeonpea between 30 and 85 days (Wallis et al. 1975; Sheldrake and Narayanan 1979) presumably due to relatively slow leaf area development and initial high investment in root development. The early-maturing cultivars, at optimum plant population (44,000 plants/ha) attained maximum DM (3.5 t/ha) in about 120 days, whereas, at a density of about 66,000 plants/ha, the same cultivar attained maximum DM (4.8 t/ha) at about 126 DAS (Sheldrake and Narayanan 1979). Medium-maturing cultivar attained maximum DM (5.7 t/ha) at 140 DAS (Sheldrake and Narayanan 1979; Willey et al. 1981). Thus, the early-maturing cultivar must be grown at a much higher plant population to achieve maximum DM production per unit area. Such early-maturing cultivars also have higher HI (34%) as compared with medium-maturing cultivars (Sheldrake and Narayanan 1979; Willey et al. 1981). In late-maturing cultivars, stem and leaf dry matter, LAI, and CGR increased exponentially from 70 DAS. Maximum DM (3.6–4.2 t/ha) was produced at 238 days. Maximum LAI (13.4–15.5) developed at 140 DAS. The maximum CGR occurred between 196 and 224 DAS (Wallis et al. 1975). Maximum light interception (95%) was achieved by an LAI of 6–7 (Rachie and Roberts 1974; Wallis et al. 1975; Hughes et al. 1981). Compared to other legumes, medium-maturing pigeonpea cultivars develop massive stems and abundant foliage and these plant parts may contribute 80% of total plant dry weight at maturity (Sivakumar and Virmani 1980), and hence they have a low HI of about 14–25% (Ariyanayagam 1975; Sheldrake and Narayanan 1979; Roy Sharma et al. 1981). The optimum plant population for maximum seed yield varies among cultivars. Populations between 52,700 and 333,000 plants/ha at 90–120 cm row spacing resulted in the highest seed yields ranging between 1.1 and 5.8 t/ha (Padmalatha and Rao 1993; Rao et al. 1981; Singh and Kush 1981; Sarvaiya et al. 1993; Singh et al. 1994). The seed yield of cultivars varies between 0.7 and 5.8 t/ha (Rao et al. 1981; Roy Sharma et al. 1981; Singh and Kush 1981; Chatterjee and Bhattacharyya 1986). When planted during a cool, dry weather season with short photoperiod, about 75% of plant height may be reduced and yield increased by 35–50% as compared to a warm and rainy season crop (Roy Sharma et al. 1981).

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Imposing 35% of artificial shade decreased the photosynthetic rate and reduced the assimilate supply to pods, leading to a drastic reduction in pod number and seed yield per plant (36% reduction) as compared to plants grown under full sunlight (Pandey 1981). E. Common bean The common bean (Phaseolus vulgaris) (also French bean, dry bean, field bean, snap bean) is a herbaceous annual with determinate or indeterminate growth habit. It is grown under extremely variable conditions from 52°N to 32°S latitude, and from near sea level to elevations of more than 3,000 m (Graham and Ranalli 1997). On germination, the plant is initially taprooted, but adventitious roots emerge soon thereafter and dominate the taproot, which remains 10–15 cm in length (Duke 1981). Determinate cultivars may be bush or dwarf type (Type I). Indeterminate cultivars may have an upright habit, with an erect stem and branches (Type II), or bush habit with weak and prostrate stem and numerous branches and variable ability to climb (Type III), or climbing habit with a weak, long and twisted stem and reduced branching (Type IV) (Graham and Ranalli 1997). Plant height varies in different growth habits. It may be 44 cm in Type I, 92 cm in Type II, 103 cm in Type III, and 160 cm in Type IV (Laing et al. 1984). Maximum canopy photosynthesis occurred at LAI of about 4.5 and it did not change up to LAI of 7.5 (Sale 1975). Maximum light (95%) was intercepted at LAI of about 4 (Aguilar et al. 1977). Time to flowering varies with cultivar, temperature, and photoperiod. Cultivars that flowered well at a 2,700 m elevation and 13°C mean temperature did not flower or were extremely slow to flower when grown under the same natural daylengths at a 1,000 m elevation and 24°C mean temperature; however, flowering was induced with a shortened (9 h) photoperiod (Wallace 1985; White et al. 1987). Day-neutral, erect, indeterminate types of cultivars have also been reported (White and Laing 1989). Flowering is usually initiated 28–42 days after planting. Determinate cultivars produce flowers over a very short period of 5–6 days, whereas indeterminate cultivars produce additional nodes after initial flowering, with flower formation thereby extended to 15–30 days. However, two-thirds of all the flowers produced may abscise, and in high temperature or under water deficit stress, young fruits and developing seeds may abort. Seed-filling periods may extend from as few as 23 days in the case of the determinate cultivars to nearly 50 days in determinate and climbing varieties. Physiological maturity (the stage beyond which no further increase in seed dry matter takes place) may occur 60–65 days after planting among early

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cultivars used in areas where the growing season is very short, or extend to 200 days after planting among climbing cultivars used in cooler upland elevations (Graham and Ranalli 1997). Optimum plant populations are 60,000 plants/ha for Type III cultivars and about 480,000 plants/ha for Type I cultivars (CIAT 1976; Graham and Rosas 1978). For Type IV cultivars, the optimum population is about 120,000 plants/ha. Seed yields can range from less than 0.5 t/ha to as much as 5.0 t/ha under experimental conditions (Graham 1978; Graham and Ranalli 1997). Artificial shade (reduction in light intensity from 390 µE/m2/s to µ55 E/m2/s) reduced leaf number, leaf area, and leaf thickness (Crookston et al. 1975). It also reduced the number of stomata/unit area by 36%, and thereby increased total leaf resistance to CO2 uptake by 76%, reduced photosynthetic enzyme (RuBPcase, ribulose biphosphate carboxylase/oxygenase) activity about 70%, which in turn reduced the photosynthetic rate by 38%. Under shaded conditions, leaf thickness and the spongy and polisade leaf cell size decreased. The chloroplasts grown in normal light were filled with large starch grains and contained well developed grana, whereas those from leaves grown under shaded conditions were smaller in size and did not have starch granules. F. Mungbean Mungbean (Vigna radiata) (also green gram, golden gram) is a warm season annual, with trifoliate leaves like the other legumes. It is grown widely for use as a human food (as dry bean or fresh sprout), but can also be used as a green manure crop and as forage for livestocks. Seeds contain 19–25% protein and 49–60% carbohydrate. Plants are adapted to the same climate areas as soybean and cowpea. Cultivars may be dwarf erect, determinate and non-branched, or indeterminate and semiprostrate or tendrilous and profusely branched. Plant height varies between 52 and 72 cm. Short-duration cultivars mature in 60–89 DAS, whereas long-duration cultivars mature in 90–120 DAS (Chatterjee and Bhattacharyya 1986). The maturity of mungbeans depends upon environmental conditions and cultivars. The pod harvest is generally made twice between 55 and 75 DAS depending upon cultivar and growing conditions. Alternatively, plants may be harvested when around 90% of pods turn black. Mungbeans are planted at the spacing of 15–25 cm between rows × 10 cm between plants within a row, with a population of 500,000 plants/ha or at the spacing of 50–75 cm between rows × 5–10 cm between plants within a row, with a population of 375,000–400,000 plants/ha (Poehlman 1974; USDA 1975; Robinson 1975; Kuo et al. 1978; Rawson and Craven 1979; Jain and Mehra 1980; Lekwanich 1984; Cupka

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1987; Oplinger et al. 1990). In 25 cm row spacing, plants intercepted the greatest amount (82–99%) of solar radiation, and produced the highest dry matter (7.8 t/ha) and grain yield (3.4 t/ha). The grain yield of mungbean cultivars varied between 0.5 and 1.9 t/ha (Chatterjee and Bhattacharyya 1986; Bhardwaj et al. 1996, 1997). Mungbeans are short-day plants. Flowering is both photoperiod and temperature sensitive. However, there are variations from completely photoperiod insensitive types to strongly photoperiod sensitive types. G. Maize Maize (Zea mays) is a tall, robust annual crop widely grown in the tropical (tropical maize) and temperate (temperate maize) regions of the world. Maize kernels (grains) are used as human food and its stover as animal feed. Maize grains contain 4–14% oil (Earley et al. 1966; Lambert et al. 1998). A maize plant usually has a single dominant stem, but may produce a few basal branches in temperate maize. In tropical maize, tillers rarely develop and do not contribute to grain yield. Its leaves are distichous with overlapping sheaths and long broad laminae positioned. Leaf inclination widely varies among cultivars and leaf position varies from horizontal to vertical. The adventitious roots develop from the lowest nodes of the stem where the nodes are close together and about 2.5 cm below the soil surface. Some roots grow horizontally for 0.5–1.0 m and then turn sharply downward. Others grow almost vertically to a depth of up to 2.5 m. These roots branch profusely. At the time of rapid elongation of the stem, the 2–3 nodes above ground produce whorls of prop or brace roots. On entering the soil, they branch and behave like ordinary roots (Purseglove 1972). Maize is a monoecious and protandrous plant. It produces its staminate flowers in a terminal inflorescence (tassel) and its pistillate flowers on lateral shoots (ears). Male flowering (pollen shed) usually occurs one or two days before the appearance of the style (silking). A tassel continues to shed excessive pollen from 2 to 14 days with 5–8 days of peak shedding. Because of the separation of ear and tassel, and the protandry of flowering, maize is primarily a cross-pollinated plant. Cultivars may be either early maturing (65–75 days), medium maturing (90–115 days), or late maturing (200–360 days) depending on genetic potential and length of growing season as determined by temperature, and moisture availability (Purseglove 1972; Thakur 1979; Fischer and Palmer 1984). Maize is a short-day plant (Kiesselbach 1950), and the total number of leaves, determined at the time of floral initiation, depends on the cultivar and photoperiod, although temperature may have a little influence

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(Hesketh et al. 1969; Stevenson and Goodman 1972; Tollenaar et al. 1979). The threshold photoperiod may vary between 10 and 13.5 h/day (Hunter et al. 1974). Maize leaves have a C4 photosynthetic pathway with high photosynthetic rates that do not saturate even in full sunlight (Hatch and Slack 1970; Hesketh and Musgrave 1962). The crop growth rate of maize cultivars varies between 28 and 49 g/m2/day (Stewart 1970; Goldsworthy et al. 1974; Goldsworthy and Colegrove 1974). Crop growth rates were highest at an LAI of about 7.5, whereas total dry matter production was highest at LAIs 6 and 7 at the low and high elevation sites, respectively. However, under water deficit stress conditions, CGR was highest at an LAI of 3 (Fischer and Palmer 1984). The optimum LAI for maximum grain yield is considerably less than that for maximum CGR or maximum dry matter production. In favorable conditions, maximum grain yield occurs at LAI 4–5, whereas under water deficit stress conditions, maximum grain yield occurs at an LAI of 2.5 (Fischer and Palmer 1984). When LAI was greater than 5, the additional dry matter produced accumulated mainly in the stem (Goldsworthy et al. 1974). Cultivars with a small leaf area per plant often gave the maximum grain yield at a relatively high plant population (Major et al. 1972; Daynard et al. 1977; Fischer et al. 1982). In temperate maize, at flowering, a larger proportion of the assimilate from upper leaves moves to the tassel, upper stem, and ear; lower leaves supply the lower stem, roots, and also the ear. The leaf subtending the ear supplies about one-quarter of its assimilate to the ear, which determines the grain yield (Eastin 1969; Edmeades et al. 1979; Edmeades and Daynard 1979). In tropical maize, the leaf area above the ear is often larger (leaf area/cm of height) so that less light reaches the ear leaf and those below it. At larger plant populations, this may account for more barren plants in tropical than temperate maize (CIMMYT 1976/77; Fischer and Palmer 1984). Cultivars may grow up to 3 m in height, and are cultivated under rainfed or irrigated conditions. The plant population is a critical factor, determining the leaf area, light interception, canopy photosynthesis, dry matter production, and grain yield. The optimum population for maximum grain yield varies between 5,000 and 100,000 plants/ha (Fery and Janick 1971; Alessi and Power 1975; Prior and Russell 1975; Francis et al. 1978; Bullock et al. 1988; DeLoughery and Crookston 1979; Tetio-Kagho and Gardner 1988; Tollenaar and Bruulsema 1988; Hashemi-Dezfouli and Herbert 1992; Dong and Hu 1993; Otegui and Ruiz 1993; Cox 1996). At populations ranging between 30,000 and 100,000 plants/ha, maize grain yield varies between 1.1 and 11 t/ha (Alessi and Power 1975; Bullock et al. 1988; DeLoughery and Crookston 1979; Tetio-Kagho and Gardner 1988). Reduction in row spacing from 100 to 50 cm did not alter the grain yield (2.9 t/ha)

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(Alessi and Power 1975), whereas equidistant spacing (38 × 38 cm) increased the grain yield (Bullock et al. 1988). The world average maize grain yield was 4.4 t/ha, while maximum grain yield up to 9.8 t/ha was obtained (FAO 2001). In a population ranging between 63,000 and 100,000 plants/ha, which resulted in the highest grain yield, maize developed the highest LAI of 4–5 between 70 and 80 days after sowing and attained full canopy closure and maximum light interception (95%) by this time (Alessi and Power 1975; Tetio-Kagho and Gardner 1988; Tollenaar and Bruulsema 1988; Maddonni and Otegui 1996). Although maize is grown in about 50 million hectares in the tropics, about twothirds of the world’s maize is produced in temperate climate zones (Fischer and Palmer 1984). The grain yield of maize cultivars, in pure stand, varies between 2.5 and 19 t/ha, whereas stover yield varies between 7.5 and 10 t/ha (Cuany et al. 1970; Frey 1971; Alessi and Power 1975; De Loughery and Crookston 1979; Thakur 1979; Francis et al. 1983; Bullock et al. 1988; Varshney 1991; Hashemi-Dezfouli and Herbert 1992; Paradkar and Sharma 1993; Sharma et al. 1998; Maheshkumar et al. 1992). Although the rates of dry matter production by the temperate and tropical maize cultivars are similar, in tropical maize cultivars, a relatively little proportion of the total dry matter is allocated to the grains as compared to the temperate maize cultivars. The harvest index (HI) of the tropical cultivars varies between 0.3 and 0.4, whereas the HI for temperate cultivars varies between 0.5 and 0.6 (Daynard et al. 1969). Thus, tropical maize cultivars are less efficient than temperate cultivars, even when tropical maize is grown in a subtropical environment (Fischer and Palmer 1984) and this accounts for low grain yields of tropical maize cultivars (Goldsworthy 1974; Goldsworthy and Colegrove 1974; Goldsworthy et al. 1974; Yamaguchi 1974). Therefore, larger grain yields are obtained in temperate regions than in the tropics. Decrease in light intensity from 100% to 30% of solar radiation significantly decreases grain and stover yields by 59 and 35%, respectively (Earley et al. 1966). The amount of radiation intercepted by a maize plant during flowering is the main factor that determines grain number (Tollenaar 1977). Shading before initiation of the inflorescence had no significant effect on grain yield. But shading the crop by 54% for 22 days close to the flowering stage significantly reduced grain yields in both tropical and temperate maize cultivars (Fischer and Palmer 1984). Shade (50%), particularly during reproductive growth (flowering and grain filling), causes severe reduction in grain yield mainly through a decrease in kernel number per ear (Earley et al. 1967; Kiniry and Ritchie 1985; Reed et al. 1988). Shade also delays silking (extension of the tasselingto-silking interval), which may cause a failure to achieve complete pol-

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lination and increase ear barrenness (Stinson and Moss 1960; Buren et al. 1974; Karlen and Camp 1985; Hashemi-Dezfouli and Herbert 1992). Thus, the period around flowering (about 10 to 15 days before and after) is a critical period for ear development when shade should be avoided. Imposing 50% artificial shade above the canopy, 44 days after emergence, decreased the grain yield in the range of 23–66% at a population ranging between 30,000 and 120,000 plants/ha, suggesting that the effect of shade is an aggravation when there is a high plant population (Hashemi-Dezfouli and Herbert 1992). In maize, about 30–40% of solar radiation is intercepted by the tassels at a population of 26,000–63,000 plants/ha (Tetio-Kagho and Gardner 1988). Detasseling has been shown to increase maize grain yield by 9.5–21.0% (Grogan 1956; Duncan et al. 1967; Hunter et al. 1969; Poey et al. 1977). This may be partly due to the increase in the amount of light that reaches the lower leaves (Duncan et al. 1967; Hunter et al. 1969; Lambert and Johnson 1978) and partly due to the removal of the apical dominance of the tassel (Muleba 1980; Paterniani 1981). Selection for shorter plants in tropical maize reduced the proportion of the total dry matter allocated to the stem from 60 to 49% and increased the dry weight in the reproductive parts of the ear by 2–3.2%. Shortening of plant height from 2.8 to 1.8 m through selection increased grain yield by 66%, and optimum population from 48,000 to 65,000 plants/ha (Fischer and Palmer 1984). Fewer and narrow leaved tropical maize cultivars with 17% lower leaf area per plant produced 7.2% more grain yield and had high HI (0.42) at a high plant population as compared to normal plants (CIMMYT 1975). Thus, selection for shorter plants, fewer and narrower leaves, and a smaller tassel increased tolerance to high plant population that resulted in fewer barren plants at a high plant population (Fischer and Palmer 1984). H. Rice Rice (Oryza sativa) is grown all over the tropical and subtropical regions of the world. There are three botanical varieties of rice: O. sativa var. indica, grown all over the tropical regions; O. sativa var. japonica, grown in Spain, Italy, Japan, and the United States; and O. sativa var. javanica, grown in Indonesia, Madagascar, and the United States. Indica variety yields lower than japonica, and lodges due to heavy manuring. Japonica variety yields higher than indica, has short stature, and is responsive to heavy manuring. Javanica yields are intermediate, do not lodge, and are non/low-photosensitive. Short-duration cultivars mature in 100–125 days after transplanting (DAT). Medium-duration cultivars mature in 126–150 DAT. Long-duration cultivars mature in 151–170

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DAT. Lowland rice cultivars are grown in irrigated conditions with about 5 cm submergence under water. Upland rice cultivars are grown in areas where neither irrigation nor any water-retaining structure is available. It grows and matures like dry-land crops. Rice, being a tropical and subtropical crop, requires an optimum temperature of about 30°C for the day and 20°C for the night (Sreenivasan 1985). Rice may be directly sown in the field, often under upland conditions, or seedlings may be raised in nurseries; 25- to 45-day-old seedlings are transplanted to the field (Rao 1985b). The optimum spacing depends on several factors such as the plant type, season, and the fertility level. The optimum spacing for cultivars varies between 15 and 25 cm between rows, and between 10 and 25 cm between the hills within the row (Rao 1985b). Maximum light utilization was observed when rice was planted in a rectangular geometry with a spacing of 15 × 20 cm (Narkhede et al. 1971). The number of seedlings per hill varies among cultivars and about 2–6 seedlings are planted per hill (Rao 1985b; Pandey et al. 1987). The growth of a rice plant can be divided into four phases (Thakur 1979). The first phase is the active vegetative phase. This is the period from transplanting to the maximum tiller production. Plant height, tiller number, and straw weight increase during this phase. The second phase is the late vegetative phase often found in cultivars that are sensitive to photoperiod and which are maturing late. This is the period from maximum tiller production to the time of initiation of panicle. During this period, some of the tillers die back. There is some increase in plant height and straw weight. The third phase is the reproductive phase. This is the period from panicle initiation to the flowering. During this period, panicle primordia develop, and plant height and straw weight increase. The fourth phase is the ripening phase. This is the period from the flowering to the physiological maturity. During this period, the panicle weight increases rapidly, and straw weight decreases. Plant height varies among cultivars between 75 and 140 cm (Thakur 1979). Rice roots are fibrous. The root growth can vary dramatically between soils; it is influenced by soil profile characteristics, soil moisture, air temperature, and growth stage. Rice roots grow rapidly during vegetative growth with maximum root length occurring at the panicle initiation phase. Root length either plateaus or declines during reproductive growth. During early stages of rice growth, about 80–100% of the total root length occurred in the upper 40 cm of the soil. About 80–95% of the total root length was observed in the top 20 cm of the soil at the maximum tillering stage, and this declined at harvest to about 50% (Beyrouty et al. 1988). At the panicle stage, almost 80% of the root length was restricted to the upper 20 cm of the soil, and less than 3% of the total roots occurred below 30 cm.

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At harvest, 48% of the roots were found between 20 and 40 cm (Beyrouty et al. 1988). The roots may be shallow and compact, deep and compact, deep and spreading, or shallow and spreading (Kamath 1973). Maximum LAI occurs at flowering or 15 days after flowering, and it varies between 5 and 8 (Mandal and Chatterjee 1973). Rice is considered a short-day plant, and it requires an 8 h photoperiod and a 16 h dark period for normal flowering. However, rice flowering is influenced by temperature and photoperiod, and the optimum photoperiod varies with the age, treatment, duration, season, temperature, and humidity (Misra and Khan 1973; Khan and Misra 1974). Photoperiod insensitive cultivars also exist. The early-maturing, low-photoperiod sensitive indica cultivars are more temperature sensitive, and the javanicas are both photo and thermo insensitive, whereas the japonicas are similar to the early indica cultivars (Misro and Rao 1967; Murty 1985). Maximum grain yields were achieved in cultivars with LAI between 5.7 and 6.2 (Rao et al. 1974). The dry matter production during panicle initiation to flowering is associated with grain yield (Muthuswamy et al. 1973; Sircar and Das 1974). About 90% of the dry matter produced after flowering is utilized to produce grain yield in dwarf cultivars, whereas in the tall cultivars less than 70% of the dry matter contributed to the grain yield (Sircar and Das 1974). Carbon assimilation during the grain filling period plus assimilates reserves stored in the straw support the grain dry matter increase (Cock and Yoshida 1972; Weng et al. 1982). Plant population significantly affects tillering (Counce et al. 1992; Schnier et al. 1990), and tillering capacity of a cultivar influences the dry matter production, panicle density, and grain yield. Rice compensates when there is a lower plant population by producing a greater number of tillers/plant, larger panicles, and greater floret survival to grain maturity. Laterproduced tillers are more abundant at lower plant densities, with a trend toward the size of panicles decreasing. Increase in plant population decreases the proportion of secondary and tertiary tillers (Hoshikawa 1989). An increase in plant population between 1,220,000 and 4,580,000 plants/ha increased the tiller density (Miller et al. 1991). But, the total dry biomass/unit area at harvest was not significantly different at populations ranging between 560,000 and 1,690,000 plants/ha (Wu et al. 1998). The number of total and productive tillers and grain yield/hill were greater at a lower population (440,000 plants/ha) than at 1,000,000 plants/ha. However, the number of total and productive tillers/m2 and grain yield/ha were higher in higher population (1,000,000 plants/ha) than at lower population (440,000 plants/ha) (Reddy and Reddy 1992). Greater ability of tillering, higher spikelet density, and a longer maturation period resulted in high grain yield (Wu et al. 1998). Rice grain

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yield varies among cultivars between 1 and 10 t/ha (Thakur 1979). Inhibition of photosynthesis during the grain filling period due to shading can reduce the grain dry matter (Tanaka and Matsushima 1963; Nagato and Chaudhry 1970; Kobata and Moriwaki 1990). Shade during the vegetative stage reduces tillering and induces uneven flowering, whereas shading during the reproductive stages decreases dry matter production, harvest index, and grain number per panicle (CRRI 1972). Artificial shading of ears and the leaves reduced the grain yield by 48 and 52%, respectively (Basak and Chakrabarty 1963). Solar energy after the heading stage (panicle formation) is more important, because about 60–70% of the carbohydrate in the grain is derived from photosynthates after heading (Ramanathan and Moorthy 1973; Sakai and Saxena 1973). Imposition of shade (50% reduction in full sunlight) during 40 DAP to flowering was more detrimental to grain yield than shade imposed during flowering to harvest or 40 DAP to harvest (Dey et al. 1989).

IV. INTERCROPPING CASSAVA Intercropping with cassava is a widespread practice in the humid and sub-humid tropics. Cassava may also be relay planted into an early crop of short duration. In this pattern, cassava may be planted rather late in the rainy season and the crop invariably extends into the following rainy season. A three-tier system is used in Southern Cameroon, where both an early (peanut) and a late crop (plantains) are associated with cassava (Mutsaers et al. 1981). It has been estimated that about 40% of cassava is intercropped in Latin America (Leihner 1983). In Africa, up to 50% of the cassava grown is intercropped (Leihner 1983). In Uganda 49% of the cassava grown is intercropped, whereas in Nigeria a lower portion of cassava (27%) is grown in intercropping systems (Okigbo and Greenland 1976). The percentage of intercropped cassava has not been documented in Asia. Generally, farmers plant cassava during the onset of monsoon, and between 3 and 4 MAP the crop slowly develops the canopy to cover the entire field. During this early growth period, the crop does not efficiently use solar radiation and water, due to its slow initial development. Canopy spread and light penetration studies in cassava fields revealed that there is 100% light penetration through the canopy between two rows of cassava up to the 45th day after planting and thereafter the percentage of light penetration is reduced to 50, 36, and 25% at 75, 90, and 120 days after planting, respectively (Ashokan et al. 1986). Thus, dur-

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ing the early growth period, a greater proportion of insolation may be wasted between cassava rows. Consequently, high soil temperature and low soil moisture may occur and this could in turn affect the economic yield of cassava. Thus, a short-duration (75 days) crop may be interplanted during the early period of cassava growth to make more efficient use of resources. Because of cassava being cultivated as an annual crop, when grown as a pure stand, a minimum period of at least 10 months lapses before the return of investment to the cultivators. Therefore, technologies such as intercropping would result in supplemental income from the cassava field after shorter intervals, thus improving the economic condition of the farmer. One important factor is that, in many crop combinations involving cassava, cassava is usually considered by farmers as the main crop. In such a case, the farmer’s requirement is for a full yield of cassava or nearly so. Thus, for a crop to grow as an intercrop, it must not drastically reduce the storage root yield of cassava. A. Cassava + Legumes Several studies on cassava intercropping systems with short-duration grain legumes such as cowpea and pigeonpea, and oil seed legumes such as peanut and soybean, indicated reduction (often significant) in storage root yield of cassava due to competition for resources needed for growth: water, nutrients, and light. Thus, the storage root yield of cassava often remains highest when grown as a pure stand over the cassava + legume systems. 1. Cassava + Cowpea. Cowpea is adapted to the same agro-climatic conditions as cassava. In a cassava + cowpea system, storage root yields of cassava cultivars varied between 11 and 27 t/ha, whereas grain yields of cowpea cultivars varied between 0.2 and 1.8 t/ha (Prabhakar et al. 1982, 1983; Montero et al. 1984; Okeke 1984; Ashokan et al. 1985; Anilkumar and Sasidhar 1985; Mason et al. 1986a; Olasantan 1988; Sheela and Mohamed Kunju 1988; Evangelio et al. 1995; Nguyen Huu Hy et al. 1995; Okoli 1996). In these studies, in pure stands, storage root yield of cassava cultivars varied between 18.9 and 36 t/ha, whereas grain yield of cowpea cultivars varied between 0.4 and 2.7 t/ha. Thus, in a cassava + cowpea system, cassava produced 50–96% storage root yield of pure stand (Prabhakar et al. 1982, 1983; Okeke 1984; Anilkumar and Sasidhar 1985; Mason et al. 1986a; Sheela and Mohamed Kunju 1988), whereas cowpea cultivars produced 55–64% grain yield of pure stand (Okeke 1984; Mason et al. 1986a). Although, in some studies, the

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yield per hectare of cassava was substantially reduced when intercropped with cowpea, the size of storage roots was not affected (Prabhakar et al. 1982, 1983; Anilkumar and Sasidhar 1985). The fresh weight of individual storage roots decreased from 210 g in pure stand cassava to 205 in intercropped cassava, or sometimes even increased from 279 g in pure stand cassava to 332 g in intercropped cassava (Prabhakar et al. 1982, 1983). However, the number of storage roots produced per plant was significantly reduced from 5.2–13.8 in pure stand cassava to 3.8–11.1 in intercropped cassava (Prabhakar et al. 1982, 1983; Anilkumar and Sasidhar 1985; Mason et al. 1986a,b; Okoli 1996). This suggests that the reduction in storage root number is the major limiting factor for cassava yield in a cassava + cowpea system. Similarly, the grain yield of cowpea intercropped with cassava was reduced mainly because of the reduction in the number of pods per plant rather than the reduction in the number of grains per pod and grain weight (Mason et al. 1986a,b). The number of pods per plant was reduced from 11.0 in pure stand cowpea to 7.1 in cowpea intercropped with cassava. Cassava and grain cowpea cultivars with different morphologies interact differently when grown in association. In the association of grain cowpea and cassava cultivars, the performance of different plant types depends not only upon competitive ability but also on yield potential of the different components (Montero et al. 1984). In one study (Montero et al. 1984), the reduction in storage root yields of two cassava cultivars was greater when they were intercropped with erect and prostrate types of grain cowpea cultivars than with semi-erect and climbing grain cowpea cultivars. These two cassava cultivars were adversely affected by competition by prostrate and erect cowpeas because the component crops were planted simultaneously and also because of the greater vigor of prostrate cowpea and the high plant population of erect cowpea. When intercropped with cassava, grain yields of prostrate and erect cowpea types were greater, as compared to the semi-erect and climbing cowpea types. The semi-erect type of cowpea was poorly competing with all cassava cultivars, and this was reflected in the low grain yields of semi-erect cowpea and the relatively high storage root yields of cassava in all cassava + semi-erect cowpea combinations. A cassava cultivar that allowed greater light penetration during 308–382 DAP, facilitated high grain yield of climbing cowpea when this type of cowpea was planted 253 days after planting cassava. The grain yield of climbing cowpea was lower when grown in combination with cassava cultivars, which do not allow greater light penetration. A cassava cultivar that had low leaf area and low yield potential produced lower storage root yields than all cassava cultivars in all cassava + cowpea

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combinations (Montero et al. 1984). The grain yields of erect and prostrate types of cowpea were lower when planted at 253 days after planting cassava than when planted simultaneously with cassava. Thus, in the cassava + cowpea system, the combination of aggressive plant types of component crops was more productive than the association of less aggressive types. The height of cassava and photosynthetic active radiation (PAR) greatly influences the yield of grain cowpea when planted 253 days after planting cassava; and grain cowpea yield is directly proportional to the amount of light not intercepted by the cassava canopy (Montero et al. 1984). Cassava plants intercropped with grain cowpea had a reduced growth rate. In a cassava + grain cowpea system, the number of leaves, leaf dry weight and leaf area index (LAI), plant height, stem girth, dry matter accumulation by storage root, and storage root number per cassava plant remains lower than the pure stand of cassava. When cassava was grown with cowpea, storage root yield of cassava decreased by 29–30% mainly due to the 48% reduction in population density of cassava (Porto 1990; Mason et al. 1986a,b; Anilkumar and Sasidhar 1987; Sheela and Mohamed Kunju 1988). On the other hand, cowpea grain yield decreased by 25–40% depending upon the plant density of cowpea. When cowpea and cassava were planted at the same time, cassava storage root yield decreased by 13.6%, whereas cowpea grain yield decreased by 35.5% (Mason et al. 1986a). In this study, the LAI of pure stand cassava remained greater than the intercrop up to 80–150 DAP, and after that the difference became insignificant. The crop growth rate (CGR) of pure stand cassava remained higher than the intercropped cassava between 80 and 212 days. However, at a later period of growth, the difference in CGR between pure stand and intercropped cassava became insignificant (Mason et al. 1986b). Thus, the difference in total and storage root dry matter between the pure stand and intercropped cassava becomes insignificant after the harvest of cowpea. However, for both the intercropped and pure stand cassava, the pattern of dry matter accumulation in storage roots closely follows the pattern of whole plant dry matter accumulation. This suggests that intercropping cassava with cowpea does not significantly influence partitioning of dry matter to the storage roots of cassava. On the other hand, throughout the initial 3-month growth period, the LAI, total dry matter, and pod dry matter remains greater in pure stand of cowpea than the intercrop (Mason et al. 1986b). Thus, in a cassava + cowpea system, cassava storage root yield per unit area is inhibited by 4–50%, whereas grain yield per unit area of cowpea is inhibited by 36–45%, as compared to their pure stand yield. This indicates that the two crops are mutually competing with each other. However, LERs (1.2–2.0) (IITA 1977; Mba

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and Ezumah 1985; Ezumah 1986; Mason et al. 1986a; Olasantan 1988; Okoli 1996) for the cassava + grain cowpea system indicate that this crop combination is highly productive. In a cassava + cowpea system, the LER was highest (1.8) when both crops were planted at the same time. Planting cassava 3 months before or after cowpea decreased LER to 1.5 and 1.4, respectively (Wargiono et al. 2001). This indicates that for highest productivity, both crops should be planted at the same time. Cassava and fodder cowpea is a good food + fodder combination, as raising fodder cowpea with cassava did not affect the storage root yield per unit area of cassava (Sheela et al. 1996). In different spatial arrangements and nutrient management, cassava storage root yields varied between 20.6 and 38.7 t/ha, and fodder cowpea yields varied between 6.2 and 13.8 t/ha. Fodder cowpea yields per unit area were reduced by 34.3–57.0% compared to pure stand yields. An increase in spacing between paired cassava rows from 90 cm to 150 cm improved cowpea fodder yield due to an increase in the plant population of cowpea but decreased the intercropped cassava yield compared to pure stand yield because of a reduction in the plant population of cassava to 50% of pure stand. 2. Cassava + Peanut. In cassava + peanut systems, storage root yields of cassava cultivars varied between 11 and 41 t/ha, whereas pod yield of peanut cultivars varied between 0.4 and 2.5 t/ha (Muthukrishnan and Thamburaj 1979; Mohankumar and Hrishi 1979; Sinthuprama 1979; Ashokan et al. 1985; Anilkumar and Sasidhar 1985; Mason et al. 1986a; Ghosh 1987; Osiru and Hahn 1988; Sheela and Mohamed Kunju 1988; Tan 1990; Villamayor et al. 1992; Osiru and Ezumah 1994; Evangelio et al. 1995; Tian Yinong et al. 1995; Wargiono et al. 1992, 1995; Tongglum et al. 1992, 2001; Nguyen Huu Hy et al. 1995, 2001). In these studies, in pure stands, storage root yield of cassava cultivars varied between 13.9 and 35.9 t/ha, whereas seed yield of peanut was 2.1 t/ha. Thus, cassava produces 53–90% of pure stand storage root yield in a cassava + peanut system (Muthukrishnan and Thamburaj 1979; Mohankumar and Hrishi 1979; Sinthuprama 1979; Ashokan et al. 1985; Anilkumar and Sasidhar 1985; Mason et al. 1986a; Ghosh 1987; Osiru and Hahn 1988; Sheela and Mohamed Kunju 1988; Tan 1990; Tongglum et al. 2001), whereas peanut produces 62% of pure stand seed yield (Mason et al. 1986a). An increase in the plant population of peanut (Sinthuprama 1979) caused a reduction in storage root yield of intercropped cassava over the pure stand, although the reduction was insignificant. Peanut of short duration and short stature can be har-

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vested before the full development of the cassava canopy. Tan (1990) found that the storage root yield of cassava was reduced 13.7% when peanut was planted in a double row system with higher plant density. Although, in some studies, the yield per hectare of cassava was substantially reduced when intercropped with peanut, the size of storage root was not affected. The dry weight of the individual storage root was not affected in intercropped cassava (149g) as compared to pure stand cassava (Mason et al. 1986a). However, the storage root number per plant was significantly reduced from 7.8–13.8 in pure stand cassava to 5.0–11.1 in intercropped cassava (Mason et al. 1986a,b; Anilkumar and Sasidhar 1987; Ghosh 1987; Sheela and Mohamed Kunju 1988). Thus, the reduction in storage root number is one of the major limiting factors for cassava yield in a cassava + peanut system. Similarly, the seed yield of peanut intercropped with cassava was reduced mainly because of the reduction in the number of pods per plant rather than the reduction in the number of seeds per pod and seed weight (Mason et al. 1986a,b). The number of pods per plant was reduced from 9.8 in pure stand peanut to 6.2 in peanut intercropped with cassava. In a cassava + peanut system, plant height, number of leaves, LAI, total dry biomass, and stem girth per cassava plant remains lower than the pure stand cassava (Mason et al. 1986b; Ghosh 1987; Anilkumar and Sasidhar 1987; Sheela and Mohamed Kunju 1988). Intercropping cassava with peanut reduced the plant height of cassava. Here, the plant height of cassava varied between 44 and 78 cm in pure stand, and between 35.8 and 73 cm in intercropping (Osiru and Ezumah 1994). Thus, in a cassava + peanut system, cassava may intercept more radiation than peanut. When peanut is intercropped with cassava at the same time, cassava storage root yield decreased mainly due to the decrease in storage root number in cassava, and peanut yield decreased due to the reduced LAI, total and pod dry matter, and number of pods per peanut plant (Mason et al. 1986a). In a cassava + peanut system, lower LAIs in cassava during the initial growth period caused reduction in dry matter of cassava than the intercropped cassava (Mason et al. 1986b). In both intercropped and pure stand cassava, the dry matter accumulation in storage roots closely followed the dry matter accumulation pattern of the whole plant (Mason et al. 1986b). On the other hand, cassava decreases the LAI of intercropped peanut below that of pure stand peanut, which apparently reduced total and pod dry matter in peanut. In a cassava + peanut system, water availability was shown to influence storage root yield of cassava. In one study, cassava intercropped with peanut produced 91% and 70% storage root yield of pure stand in irrigated and rainfed conditions, respectively

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(Prabhakar and Nair 1992). Thus, in a cassava + peanut system, storage root production by cassava was inhibited by 10–47% by peanut cultivars, whereas seed yield of peanut was inhibited by 38.4%. The reduction in the yields of both crops in combination, as compared to their pure stand yield, indicates that the two crops are mutually competing with each other. However, LERs for a cassava + peanut system (1.0–1.9) (Sinthuprama 1979; Ashokan et al. 1985; Mason et al. 1986a; Osiru and Hahn 1988; Tongglum et al. 1992) indicate that a cassava + peanut combination is an efficient productive system. 3. Cassava + Soybean. In cassava + soybean systems, storage root yield of cassava cultivars varied between 6.3 and 27.8 t/ha, whereas seed yield of soybean cultivars varied between 0.2 and 2 t/ha (Mohankumar and Hrishi 1979; Sinthuprama 1979; Prabhakar et al. 1982; Ashokan et al. 1985; Tsay et al. 1987, 1988a, 1989; Cenpukdee and Fukai 1992a; Villamayor et al. 1992; Evangelio et al. 1995; Nguyen Huu Hy et al. 1995, 2001; Tongglum et al. 2001). In these studies, in pure stands, storage root yield of cassava cultivars varied between 10.7 and 14.4 t/ha, whereas seed yield of soybean cultivars varied between 1.7 and 2.3 t/ha. Thus, in cassava + soybean systems, cassava produces 81–88% of pure stand storage root yield (Mohankumar and Hrishi 1979; Sinthuprama 1979; Prabhakar et al. 1982; Ashokan et al. 1985; Tsay et al. 1987, 1988a, 1989; Tongglum et al. 2001), whereas soybean produces 25–66.5% of pure stand seed yield (Tsay et al. 1988a; Cenpukdee and Fukai 1992a). Early maturing (85 days) and non-spreading, short stature soybean is suitable for intercropping because it does not significantly affect the growth and storage root yield of cassava (Tsay et al. 1986, 1987, 1988a,b; Cenpukdee and Fukai 1992ab). In a cassava + soybean system, where soybean was planted 14 days later than cassava, the LAI, total biomass, and seed yield of both early- and late-maturing soybean cultivars decreased due to intercropping with cassava (Tsay et al. 1988a). Both early-maturing and late-maturing (100–120 days) soybean cultivars produced an average seed yield of 2.3 t/ha in pure stand and 1.5 t/ha in intercropping. The differences in seed yield between early- and late-maturing soybean cultivars were not significant in both pure stand and intercropping. Earlymaturing soybean, at a plant population of 22 plants/m2, which was lower than that of pure stand (33 plants/m2), reduced cassava growth during the early period presumably due to competition for N. However, after the harvest of early-maturing soybean, cassava recovered quickly to produce high leaf area, effectively intercepted solar radiation, and produced high total biomass. Because of reduced branching, dry matter partitioning to storage roots increased during the later period of cassava

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growth. This resulted in a high harvest index in intercropped cassava similar to pure stand cassava. For these reasons, cassava storage root yield was not significantly affected when intercropped with earlymaturing soybean. On the other hand, growth of cassava was restricted when intercropped with late-maturing soybean (100–120 days maturity) at a soybean population of 14.8 plants/m2, which was lower than that of pure stand (22 plants/m2). After the harvest of late-maturing soybean, recovery of cassava was poor, and with a short growing season remaining (96 days), intercropped cassava produced 50–60% storage root yield of pure stand cassava. Here, cassava produced storage root yield of 11.5 t/ha in pure stand. Intercropping cassava with an early-maturing and late-maturing soybean cultivar resulted in 8.5 t/ha and 5.7 t/ha of storage root yield, respectively. The average number of storage roots produced per plant was 7.0 in pure stand, and in intercropping with an early-maturing soybean cultivar, and it was reduced to 5.0 in intercropping with a long-duration soybean cultivar. A late-maturing soybean cultivar also suppressed cassava branching, and LAI was reduced to 2.0 rather than 4.0 in pure stand cassava, causing reduction in light interception (Tsay et al. 1988a). Because cassava produces branches mainly during early periods of growth and branching in cassava is related to the light intensity (Hunt et al. 1977), shading from the intercropped tall and late-maturing soybean partly contributes to the suppression of branches in cassava plants, apart from their competition for N (Tsay et al. 1988a). Because the differences in storage root yield between cassava cultivars in intercropping are similar to those obtained in pure stand, cultivar performance in pure stand is important in determining storage root yield potential of cassava in intercropping (Cenpukdee and Fukai 1992a,b). When soybean was planted 35 days after cassava planting (DACP), with a soybean population (67,000 plants/ha) lower than that of pure stand (250,000 plants/ha), the plant height of soybean varied between 37 and 41 cm and of cassava between 70 and 120 cm at 75 DACP. Plant canopy width varied between 43 and 60 cm in soybean and between 82 and 143 cm in cassava. Plant height less than 50 cm was achieved in both pure stand and intercropped soybean at the time of harvest (100 DACP). By this time, a tall cassava cultivar achieved 150 cm of height and a short stature cassava cultivar achieved 100 cm of height in intercropping (Cenpukdee and Fukai 1992a,b). Thus, plant height and canopy width of intercropped soybean always remained lower than that of cassava, and did not interfere with growth of both tall and short stature casava. Thus, the development of canopy and radiation interception by cassava was not affected by intercropping with soybean. Because of the reduction in radiation available to the short, regular, late-maturing soybean, soybean

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growth and seed yield was greatly reduced by tall cassava cultivars. On the other hand, short or compact cassava cultivars with a small canopy affected the growth of soybean less severely, and in some cases, storage root yield increased more than pure stand yield in the associated soybean because of little increase in harvest index. Storage root yield of cassava varied between 15.1 and 34.9 t/ha and seed yield of soybean was 1.7 t/ha in pure stand. Storage root yield of cassava varied between 11.2 and 39.2 t/ha and seed yield of soybean varied between 310 and 600 kg/ha in intercropping. The highest soybean seed yield was achieved by using a short stature cassava cultivar (1.2 m). Thus, in a cassava + soybean system, storage root production by cassava was inhibited by 12–19% by soybean cultivars, whereas seed yield of soybean cultivars was inhibited by 30–88%. The reduction in the yields of both crops in combination, as compared to their pure stand yield, indicates that the two crops are mutually competing with each other. However, LER for a cassava + soybean system varied between 1.1 and 1.7 (Kawano and Thung 1982; Tsay et al. 1988a,b; Cenpukdee and Fukai 1992a,b), indicating that this crop combination is an efficient productive system. Here, PLER for cassava varied between 0.9 and 1.3, whereas PLER for soybean varied between 0.2 and 0.4. Using short stature cassava cultivar (0.6–1.2 m) resulted in high PLER (1.2) in cassava and in soybean (0.3). Taller cassava cultivars (1.4 m height) decreased PLER of both cassava (0.8–1.0) and soybean (0.05–0.07). Thus, taller and late-maturing soybean cultivars with high yield potential may compete more strongly with intercropped cassava and are not suitable for intercropping with cassava. 4. Cassava + Pigeonpea. In cassava + pigeonpea systems, storage root yield of cassava varied between 0 and 24.4 t/ha, whereas seed yield of pigeonpea cultivars varied between 0.2 and 1.6 t/ha (Prabhakar and Nair 1979; Cenpukdee and Fukai 1992a,b,c; Villamayor et al. 1992; Evangelio et al. 1995). In pure stands, storage root yield of cassava cultivars varied between 2.9 and 36.4 t/ha, whereas seed yield of pigeonpea cultivars varied between 1.4 and 3.0 t/ha. Thus, in cassava + pigeonpea systems, cassava produces 71.6% (Prabhakar and Nair 1979) or less than 25% (Cenpukdee and Fukai 1992a,b; Fukai et al. 1984) of pure stand storage root yield, whereas pigeonpea produces 7.7–99.6% of pure stand seed yield (Cenpukdee and Fukai 1992a,b,c). When intercropped with cassava, pigeonpea substantially reduces the number of leaves, the number of storage roots produced per plant, and the storage root size of cassava (Prabhakar and Nair 1979). Here, the number of storage roots produced per plant decreased from 7.6 in pure stand to 6.2 in intercropping. The weight of a single storage root decreased from 262g

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in pure stand to 227g in intercropping. A long period of severe competition between the two crops causes severe yield loss in both (Fukai et al. 1984; Cenpukdee and Fukai, 1992a,b,c). When pigeonpea and cassava cultivars were planted at the same time, cassava emerged 9 days later than pigeonpea, and under conditions of high pigeonpea population density (267,000 plants/ha), pigeonpea completely dominated cassava at a cassava population of 14,800 plants/ha, resulting in little or almost no cassava storage root yield. The canopy width of cassava did not increase once the cassava inter-row was occupied by pigeonpea. Here, the canopy width of pigeonpea remained much larger (101–142 cm) than that of cassava (42–52 cm) at 78 days after cassava planting (DACP). The canopy width of pure stand cassava remained higher (122–212 cm) than that of intercropped cassava (57–113 cm) at 184 DACP, even after the harvest of pigeonpea at 103 DACP. Although intercropped cassava cultivars grew taller (94–105 cm) than pure stand cassava (82–99 cm) until 78 DACP, they remained shorter than pigeonpea (130–138 cm). The increase in the height of cassava plants was due to the reduction in light intensity available to cassava plants because of greater light interception by pigeonpea plants. However, after the harvest of pigeon pea, intercropped cassava plants became shorter (94–122 cm) than pure stand cassava (116–163 cm) at 127 DACP. Pigeonpea little affected the radiation interception by taller cassava cultivars but severely affected it in a short stature cassava cultivar. Intercropped cassava also suffered due to belowground competition from a vigorous pigeonpea root system. The radiation intercepted by the cassava canopy after pigeonpea harvest was not efficiently converted to biomass, presumably because of the low rate of photosynthesis and the reduction in the N content of leaves. Total dry matter production as well as storage root bulking was significantly reduced in intercropped cassava as compared to pure stand cassava. Subsequent recovery of cassava after the harvest of pigeonpea was slow, and cassava produced storage root yield less than 25% of the yield of pure stand. Here, storage root yield of cassava varied between 10 and 16.6 t/ha in pure stand and between 0.14 and 0.5 t/ha in intercropping (Cenpukdee and Fukai 1992a). When the competitive ability of pigeonpea was reduced by decreasing its plant population to 67,000 plants/ha and delaying the planting of pigeonpea by 35 DACP, only the short stature cassava cultivar was severely affected by pigeonpea, and its recovery was poor after pigeonpea harvest at 185 DACP. Cassava cultivars, which were tall and medium in height (1.7–2.2 m), grew much taller than pigeonpea (1.6–1.7 m), had greater canopy width (141–202 cm) than pigeonpea (147–189 cm) at 125 DACP, and produced storage root yields up to 70% of pure stand yield. Here, pigeonpea had little

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effect on the light interception by cassava cultivars with tall and medium height but severely affected leaf area development of a short stature cultivar and hence its light interception. Pigeonpea had little or no effect on the TDM and bulking of storage root in tall cassava cultivars with a large canopy, but significantly reduced it in a short stature cultivar with a small canopy. The strorage root yield of cassava varied between 15 and 34.9 t/ha in pure stand, and between 0.71 and 33 t/ha in intercropping. However, tall cassava cultivars almost completely suppressed pigeonpea’s growth, TDM production, and seed yield due to the reduction in radiation interception by pigeonpea, and the too long competition between the two crops. The TDM of pigeonpea was 6.3 t/ha in pure stand and it varied between 1.0 and 2.3 t/ha in intercropping. The seed yield of pigeonpea was 3 t/ha in pure stand, and it was significantly reduced in intercropping. Pigeonpea seed yields varied between 0 and 180 kg/ha in intercropping with tall stature cassava cultivars. Pigeonpea seed yield was higher (1.2 t/ha) with a short stature cassava cultivar than with tall cultivars (Cenpukdee and Fukai 1992b). At a high pigeonpea population (267,000 plants/ha) and simultaneous planting of cassava and pigeonpea, the LER for a cassava + pigeonpea system varied between 0.70 and 1.3. Here, the PLER for cassava varied between 0 and 0.2, and for pigeonpea it varied between 0.6 and 1.1. Delayed pigeonpea planting by 35 DACP with a high pigeonpea population resulted in LER ranging between 1.0 and 1.1. Here, PLER for cassava was lower (0.2) than that for pigeonpea (0.7) with a short stature (1.2 m) cassava cultivar. With a taller cassava cultivar (1.5 m), PLER for cassava was higher (0.8) than that for pigeonpea (0.3). Reduction in the pigeonpea population (67,000 plants/ha) and delayed pigeonpea planting by 35 DACP resulted in LER ranging between 0.7 and 1.3. This also increased PLER for cassava to values between 0.5 and 1.1 but decreased it for pigeonpea to values between 0 and 0.6 (Cenpukdee and Fukai 1992a,c). Delayed planting of pigeonpea by 37 DACP with tall cultivars of cassava (135–146 cm height) with canopy width ranging between 138 and 161 cm and a low pigeonpea population increased LER up to 1.4 (Cenpukdee and Fukai 1992b). Here, as the height of cassava cultivars increased from 60 to 146 cm, PLER for cassava increased from 0.4 to 0.7 but PLER for pigeonpea decreased from 0.3 to 0.2. Thus, delayed planting, a lower pigeonpea population, and taller cassava cultivars increased productivity of cassava but decreased it in pigeonpea. Using a short stature cassava cultivar decreased productivity of cassava cultivar but increased it in pigeonpea. Thus, a cassava + pigeonpea system is not an efficient one (Cenpukdee and Fukai 1992a,b,c). Tall cultivars of pigeonpea are not suitable for intercropping with cassava because of the long growth duration and tall

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stature of both the crops (Prabhakar and Nair 1979; Fukai et al. 1984; Cenpukdee and Fukai 1992a,b). On the other hand, short (less than 2 m in height) and compact cassava cultivars are not suitable for intercropping with pigeonpea because the former’s growth would be severely affected. Therefore, when cassava is intercropped with an aggressive crop such as pigeonpea, highly competitive cassava cultivars with a height not less than that of the pigeonpea plants and with high yield potential should be used. Use of quick maturing, short stature pigeonpea cultivar, a lower cassava population (less than 14,800 plants/ha) and pigeonpea population (67,000 plants/ha) or wider plant spacing (more than 1.5 m), and delayed planting of pigeonpea by 35 days may reduce the competition between the two component crops (Cenpukdee and Fukai 1992a,b,c), and increase the efficiency of this intercropping system. 5. Cassava + Mungbean. In cassava + mungbean systems, storage root yield of cassava varied between 18.5 and 35.8 t/ha, whereas grain yield of mungbean cultivars varied between 0.1 and 1.8 t/ha (Villamayor et al. 1992; Wargiono et al. 1995; Evangelio et al. 1995; Nguyen Huu Hy et al. 1995; Din Ngoc Lan and Nguyen The Dang 2000; Le Sy Loi 2000; Tongglum et al. 1992, 2001). In pure stands, storage root yield of cassava varies between 13.8 and 36.5 t/ha, whereas grain yield of mungbean was 0.3 t/ha. Thus, in a cassava + mungbean system, cassava produces 82.5–98.6% of pure stand cassava yield, whereas mungbean produces 35.5–58.9% of pure stand grain yield (Wargiono et al. 1995; Nguyen Huu Hy et al. 1995; Din Ngoc Lan and Nguyen The Dang 2000; Tongglum et al. 1992, 2001). Sometimes, cassava storage root yield increased by 2.4–11.6% in a cassava + mungbean system (Evangelio et al. 1995; Wargiono et al. 1995; Tongglum et al. 2001), probably due to the beneficial effect (release of N) extended by the legume, and reduced weed growth. The LERs for a cassava + mungbean system varied between 1.6 and 19 (Tongglum et al. 1992), indicating that this is a highly efficient productive system. 6. Cassava + Vegetable Legumes. French bean (Phaseolus vulgaris) (Thomas et al. 1982; Prabakar et al. 1983; Prabhakar and Nair 1988) and vegetable cowpea (Ghosh et al. 1987) are considered to be suitable intercrops with cassava. Cassava produces 66.9–84.8% of pure stand storage root yield in a cassava + vegetable cowpea system (Muthukrishnan and Thamburaj 1979; Ghosh et al. 1987). In one study, when a vigorous type of dwarf bean (Lablab niger) was intercropped with cassava, the storage root bulking was affected with a yield reduction of 28.5% over

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the pure stand cassava yield (Muthukrishnan and Thamburaj 1979). Storage root yield reduction of intercropped cassava was almost negligible with an early-maturing (80 days) French bean cultivar, while it varied between 20–40% with a late-maturing (90 days) cultivar (Thung and Cock 1979). On the other hand, yield of the early-maturing French bean cultivar was more affected by cassava than the late-maturing one. B. Cassava + Non Legumes 1. Cassava + Okra. The LER for cassava + okra varies between 1.22 and 1.33 (Ikeorgu et al. 1984), indicating that this crop combination is an efficient productive system. 2. Cassava + Maize. Cassava intercropped with maize is common in the lowland humid tropics when both are sown at the same time at the beginning of the rainy season. In the cassava + maize systems, storage root yields of cassava cultivars varied between 7.8 and 37 t/ha, whereas grain yield of maize cultivars varied between 1.1 and 5.7 t/ha (Mohankumar and Hrishi 1979; Moreno and Hart 1979; Porto et al. 1979; Sinthuprama 1979; Olasantan 1988; Ikeorgu et al. 1989; Tan 1990; Widodo et al. 1993; Ikeorgu and Odurukwe 1994; Osiru and Ezumah 1994; Evangelio et al. 1995; Nguyen Huu Hy et al. 1995). In pure stands, storage root yield of cassava cultivars varied between 16.8 and 39.6 t/ha, whereas grain yield of maize cultivars varied between 0.6 and 4.2 t/ha. Thus, in the cassava + maize systems, cassava cultivars produce 50–98.8% storage root yield of pure stand, whereas maize cultivars produce 47.6–86.8% grain yield of pure stand (Mohankumar and Hrishi 1979; Moreno and Hart 1979; Sinthuprama 1979; Olasantan 1988; Tan 1990). In some studies, the storage root yield of cassava decreased with maize yield exceeding 3.5 t/ha (Kang and Wilson 1981; Ezumah and Lawson 1983; Ikeorgu and Odurukwe 1994), whereas maize yield increased by 26–83.3% more than that of the pure stand maize crop (Porto et al. 1979; Ikeorgu et al. 1989), presumably because maize dominated cassava. In the cassava + maize system, maize decreased the storage root yield of cassava by 28% even though the maize population was only 50% of the pure stand crop (Ikeorgu et al. 1989). The reduction in storage root yield of intercropped cassava was because of the reduction in the number of leaves, leaf dry weight and LAI, crop growth rate, total dry matter production, dry matter accumulation in storage root, and the number of storage roots produced per plant compared to the pure stand (Zandstra 1979; Porto 1990). In a cassava + maize mixture, an important

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factor of competition is presumably light. Here, the dominant maize crop intercepts most of the light and induces cassava plants to grow taller. In one study, cassava plant height varied between 44 and 78 cm in pure stand, whereas in a mixture with maize, cassava plant height varied between 60.5 and 100 cm at 8 weeks after planting (Osiru and Ezumah 1994). However, the effects of maize on the performance of the associated cassava varied substantially with maize growth habits (Osiru and Ezumah 1994). The tall, spreading maize substantially reduced cassava yield at a population higher than 50,000 plants/ha, whereas short spreading maize did not significantly reduce cassava yield even at a high population of 80,000 plants/ha, indicating that the plant height and population of the component crops are important factors influencing compatibility. A maize cultivar with erect leaves allows much light to reach the associated cassava. Maize cultivars with a high harvest index will have lower vegetative vigor and may be less competitive. Thus, maize cultivars with the same yield potential may have a different effect on associated cassava according to their canopy structure or vegetative vigor (Mutsaers et al. 1993). Maize cultivars that produce high yield in pure stand also give the highest yield when intercropped with cassava (Ezumah 1990; Osiru and Ezumah 1994). In the cassava + maize systems, LER varied between 1.2 and 2.1 (Moreno and Hart 1979; Kang and Wilson 1981; Ezumah and Lawson 1983; Ikeorgu et al. 1984, 1989; Osiru and Hahn 1988; Ezumah 1988; Olasantan 1988). This indicates that this crop combination is an efficient productive system. In a yam + maize + cassava mixture, yields of all the three component crops were highest in pure stand. Here, intercropping significantly decreased yield of cassava by 46%. Cassava storage root yield was 26.4 t/ha in pure stand; it decreased to 14.2 t/ha in intercropping. Yam tuber yield was 9 t/ha in pure stand; it decreased to 4 t/ha in an intercrop mixture. However, maize grain yield (2.6 t/ha) did not differ significantly between pure stand and an intercrop mixture (Odurukwe and Ikeorgu 1994). 2. Cassava + Rice. In a cassava + rice system, in upland conditions, storage root yield of cassava and grain yield of rice are influenced by cassava cultivar and population. In one study, in both pure stand and cassava intercropped with rice, storage root yield significantly increased as the cassava population increased from 6,666 plants/ha to 16,666 plants/ha. Here, the highest storage root yield was obtained at the highest cassava population (16,666 plants/ha), and the lowest storage root yield at the lowest population (6,666 plants/ha) (Dahniya et al. 1994).

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This trend in increase in yield was observed in cassava cultivars regardless of their yield potential. There was no significant difference in yield between pure stand and intercropped cassava in different cassava populations. In a pure stand, in the cassava cultivar with high yield potential, storage root yield increased from 14 t/ha at the lowest population to 23.6 t/ha at the highest population. In the intercropped system, storage root yield of this cultivar increased from 13.5 t/ha at the lowest population to 17.4 t/ha at the highest population. Here, the increase in storage root yield of this cultivar was insignificant as the cassava population increased above 13,333 plants/ha. In a cassava cultivar with low yield potential, the storage root yield increased from 3 t/ha to 5.2 t/ha in pure stand, and from 2.6 t/ha to 5.7t/ha in cassava intercropped with rice, as the cassava population increased from 6,666 plants to 16,666 plants/ha. There was no significant difference in the number of storage roots produced per plant between pure stand and intercropped cassava. This was because rice was sown 1 month after planting cassava, and by this time initiation of storage roots had started before effective competition was encountered with rice. Here, the number of storage roots produced per plant remained nearly constant in a cultivar with low yield potential in both pure stand (2.3–2.8) and intercropped cassava (2.1–2.8) as the cassava population increased from 6,666 plants/ha to 16,666 plants/ha. But, in a cassava cultivar with high yield potential, the number of storage roots produced per plant decreased from 4.9 to 3.7 in pure stand, and from 5.9 to 3.5 in intercropped cassava, as the cassava population increased from 6,666 plants/ha to 16,666 plants/ha. In both pure stand and intercropped cassava, the weight of individual storage root significantly decreased as the cassava population increased from 6,666 plants/ha to 16,666 plants/ha. The weight of the individual storage root significantly decreased in cassava intercropped with rice compared to that in pure stand. In pure stand, the weight of a single storage root (170g and 440g in low- and high-yielding cultivars, respectively) produced in the lowest cassava population decreased to 160g and 340g in low- and high-yielding cultivars, respectively, as the cassava population increased to 16,666 plants/ha. In intercropped cassava, the weight of a single storage root (180g or 350g) produced in the lowest cassava population decreased to 120g or 270g as the cassava population increased. Cassava cultivars with either high- or low-yielding potential did not have any significant effect on rice grain yield. Rice grain yield was highest (3.6 t/ha) in pure stand. This was, however, not significantly different from rice intercropped with both high- and low-yielding cassava cultivars at a cassava population of 6,666 plants/ha. However, rice grain yield decreased from 3.2 t/ha to 1.5 t/ha as the cassava population increased from 6,666

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plants/ha to 16,666 plants/ha. Here, the population of rice was kept constant (rice seed rate 80 kg/ha, about 3,200,000 plants/ha). The number of panicles per square meter of pure stand rice (48.8) was substantially reduced from that obtained (76.5) with rice intercropped with cassava up to a cassava population of 10,000 plants/ha. However, an increase in the cassava population from 6,666 plants/ha to 16,666 plants/ha decreased the number of grains per panicle and 1,000-grains weight as compared to pure stand rice. The number of grains per panicle decreased from 80.2 to 40.8, and the 1,000-grains weight decreased from 23.6 to 20.2 as the cassava population increased from 6,666 plants/ha to 16,666 plants/ha. The 1,000-grains weight of pure stand rice (25.1g) was not significantly different from that of rice intercropped with cassava. There was no significant difference in plant height between pure stand and intercropped rice as the cassava population increased. In other studies, storage root yield of cassava increased from 3.3 to 8.6 t/ha with an increase in its population from 3,333 to 13,333 plants/ha, but rice grain yield decreased from 1.5 to 0.7 t/ha (Jalloh 1995, 1998). However, an increase in the cassava population between 10,000 and 13,333 plants/ha did not significantly increase the storage root yield of intercropped cassava (Dahniya et al. 1994; Jalloh 1995, 1998). Increasing the cassava plant population from 3,333 to 6,666 plants/ha caused a 12% reduction in the grain yield of rice, while increasing the cassava plant population from 10,000 to 13,333 plants/ha caused a 20–25% reduction in rice grain yield (Jalloh 1998). Thus, in a cassava + rice system, cassava produced 83–100% of pure stand storage root yield, whereas rice produced 25–88% of pure stand grain yield (Zandstra 1978; Porto et al. 1979; Dahniya et al. 1994; Jalloh 1995). Because cassava was planted one month before rice, cassava remained taller than rice throughout their period of association and shading of rice by cassava, particularly at the reproductive stage, reduced the grain yield of intercropped rice (Dahniya et al. 1994; Jalloh 1995, 1998). Shading during the vegetative stage minimally affects the rice grain yield, whereas shading during the reproductive stage has a greater effect than during grain ripening (Yoshida and Paraw 1987). In cassava intercropped with rice, total dry matter and storage root dry matter of cassava decreased by 49% and 20% respectively compared to the pure stand cassava crop (Zandstra 1978). The LER varied between 1.6 and 1.9 as the cassava population increased up to 10,000 plants/ha, and it decreased to 1.1 at a cassava population of 16,666 plants/ha. The LER (1.5–1.9) achieved in a cassava + rice system (Dahniya et al. 1994; Wargiono et al. 2001) shows that this crop combination is an efficient productive system up to a cassava population of 10,000 plants/ha.

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C. Cassava + Legumes and Non-Legumes Cassava and French bean may be intercropped with little or no reduction in yield of either crop, but when maize is included in the system, the yields of both bean and cassava are reduced to half their pure stand yield, whereas that of maize is not affected (Moreno and Hart 1979). In an intercropping system where cassava, maize, and French bean are planted at the same time, bean does not allow weed invasion during the initial 2 months, the maize successfully excludes the weeds between 3 and 4 months, and 5 and 8 months, and when the cropping period ends, the cassava canopy develops enough to exclude weed invasion (Hart 1975a,b). This offers a beneficial saving in labor because weed control is a major part of cassava management. When cassava was intercropped with French bean, cassava yield was not reduced but the bean yielded 80% of the pure stand bean. Adding maize to cassava and French bean reduced bean yield to 70% of the pure stand bean (Holle 1976). Cassava intercropped with maize and French bean or lima bean (Phaseolus lunatus) produces 70% of pure stand storage root yield (Dos Santos 1978). On the other hand, maize yield is decreased by 60% when intercropped with cassava and French bean or lima bean compared to pure stand maize yield. Among the different cropping systems, the cassava + maize + lima bean cropping system produces the highest carbohydrate and protein. When intercropped with rice + maize or rice + Fench bean, cassava produced 87.8% of pure stand storage root yield (Porto et al. 1979). The other crops, in general, also suffer in their production when grown in association, while rice is specifically affected with losses up to 95% in a cassava + rice + French bean + maize system. In this intercropping system involving four crops, cassava produced 50.7% storage root yield of pure stand. In a maize + rice + cassava system, the total dry matter and the storage root dry matter of cassava decreased by 54.2% and 27.8%, respectively, compared to the pure stand cassava (Zandstra 1979). In cassava + rice – mungbean system, cassava produced 27.8 t/ha, which was 1.0 t/ha less than the yield of pure stand cassava. Here, rice produced 0.91 t/ha, which was 34% less than the yield of pure stand rice, and mungbean produced 0.12 t/ha, which was 61% less than the yield of pure stand mungbean (Wargiono et al. 1995).

D. Cassava + Perennials In Kerala, India, there has been a steady decline in area under cassava because more profitable plantation crops, including rubber, have moved into this area. In this situation, use of multi-tier cropping with crops hav-

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ing their canopies at different levels is a realistic approach to sustain cassava production in this region. 1. Growth and Productivity. A multi-tier cropping system consists of different canopy levels. Perennial crops such as coconut, banana, Eucalyptus, and Leucaena constitute the top-level canopy, while cassava occupies the second-level canopy. Seasonal crops such as peanut or vegetable cowpea constitute the ground-level canopy (Ghosh 1987). In a study on a multi-tier cropping system, coconut was planted at 10.0 × 6.0 m spacing (10 m between rows and 6 m between trees within a row; 166 plants/ha), and banana, Leucaena leucocephala, and Eucalyptus at 5.0 × 2.5 m spacing (5 m between rows and 2.5 m between trees within a row; 800 plants/ha). Cassava was planted at 90 × 90 cm spacing both in pure stand (9,700 plants/ha) and when intercropped with perennials (12,345 plants/ha). Legumes (4,300 cowpea plants/ha; 8,600 peanut or French bean plants/ha) were planted at 30 × 20 cm spacing (30 cm between rows and 20 cm between plants within a row), both as pure stand and when intercropped with cassava and perennials. There were two rows of legumes between two rows of cassava in intercropping systems (Ghosh 1987). The shoot growth (plant height and stem girth) of banana in a cassava + banana combination was adversely affected during the initial 12 months. However, at 30 months, the shoot growth of banana was not adversely affected by cassava. The shoot growth of banana in a banana + cassava + peanut combination was similar to the pure stand banana crop. In pure stand banana plots, lateral roots of banana plants extended up to 1.8 m, whereas in cassava + banana plots, lateral roots of banana plants extended up to 2.0 m. Thus, in cassava + banana plots, except the central row, most of the cassava plants confronted the roots of banana. Cassava delayed the flowering and fruiting of banana and adversely affected banana yield. Over a period of 33 months, the highest total banana yield (6.2 t/ha) was recorded in pure stand, and total banana yield decreased to 1.8 t/ha due to intercropping with cassava. Inclusion of cowpea or peanut along with cassava decreased total banana yield to 1.7 and 1.3 t/ha, respectively. Growth of cassava in association with banana was more vigorous than other perennial combinations. Compared to pure stand, the total biomass of cassava increased by 11.5% in the cassava + banana system. Cassava in combination with banana produced more leaves and LAI due to more uniform branching in the cassava plants than in the pure stand cassava and, therefore, light interception by cassava plants remained highest in the cassava + banana rather than in pure stand and other perennials. Over the period of 33

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months, light intensity under banana plants remained constant (86.5% of solar radiation), which indicated that light intensity was not a limiting factor in the cassava + banana system. Over the period of 33 months, storage root yield of cassava was higher (27.2 t/ha) when intercropped with banana than was the pure stand cassava yield (25.1 t/ha), but the difference was not significant. Inclusion of peanut and cowpea with the banana + cassava mixture did not affect cassava yield (22.9 t/ha). The average NPK uptake by cassava was significantly higher in the cassava + banana combination than in other perennials combinations. The average NPK uptake by cassava was 195.9, 13.2, and 106.5 kg/ha, respectively, in pure stand, and this increased to 216.5, 15.2, and 127.7 kg/ha, respectively, in the cassava + banana combination. Here, cassava more efficiently utilized the applied nutrients. Inclusion of peanut or cowpea reduced the average NPK uptake by cassava to 187.5, 9.3, and 98.9 kg/ha, respectively. The nutrients uptake by peanut and cowpea was highest in association with cassava + banana as compared to other perennial combinations. Here, the NPK uptake by peanut was 53.7, 3.1, and 47.8 kg/ha, respectively, and NPK uptake by cowpea was 54.5, 2.2, and 37.1 kg/ha, respectively. This indicates that peanut and cowpea competed with cassava and banana plants for nutrients. The pod yield of peanut (0.8 t/ha) and fresh pod yield of cowpea (4.7 t/ha) was greatest in the cassava + banana system rather than in other cassava + perennial combinations. Increases in cassava LAI, biomass, and storage root yield in the cassava + banana system indicate that cassava competed with banana for resources and decreased banana yield. In the cassava + Leucaena mixture, shoot growth (plant height and stem girth) of Leucaena was adversely affected during the initial 12 months. However, at 30 months, the shoot growth of Leucaena was not affected by cassava. The shoot growth of Leucaena in the cassava + Leucaena + cowpea combination was similar to that in the pure stand Leucaena. At 32 months, lateral root growth of Leucaena was adversely affected by the cassava intercrop. In the pure stand, lateral roots of Leucaena plants extended up to 3.5 m, whereas in cassava + Leucaena plots, lateral roots of Leucaena plants extended up to 2.0 m. Thus, in cassava + Leucaena plots, except the central row, most of the cassava plants confronted the roots of Leucaena plants. Cassava adversely affected the forage yield of Leucaena. In the cassava + Leucaena system, over a period of 33 months, cassava reduced the total forage yield of Leucaena to 4.8 t/ha compared to the pure stand Leucaena crop (6.5 t/ha), but total forage yield increased to 7.5 with the inclusion of peanut with cassava + Leucaena. During the first-year crop, Leucaena did not significantly affect the LAI of cassava. However, from the 2nd year onward there was

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significant reduction in LAI of cassava under Leucaena (15–44%). Inclusion of peanut or cowpea along with cassava + Leucaena did not appreciably increase the LAI of cassava. Over a period of 32 months, light intensity under Leucaena trees remained 70.7%, indicating light intensity was not a limiting factor. Cassava yield substantially decreased to 13.2 t/ha in the cassava + Leucaena combination as compared to pure stand (24.4 t/ha). The nutrient uptake by cassava in the cassava + Leucaena combination was lower than that in pure stand cassava. Here the average NPK uptake by cassava was 124, 9.2, and 70.0 kg/ha, respectively. Inclusion of peanut and cowpea along with cassava + Leucaena reduced the uptake of nutrients by cassava. Here, average NPK uptake by cassava was 109.9, 4.8, and 44.0 kg/ha, respectively. This also resulted in an average yield of cassava of 16.2 t/ha. Thus, in the cassava + Leucaena system both the crops competed with each other for resources and the reduction in LAI, and the nutrient uptake in cassava probably reduced biomass production and storage root yield. In the cassava + Leucaena combination, NPK uptake by peanut was 42.3, 1.9, and 17.2 kg/ha, respectively, and NPK uptake by cowpea was 29.1, 1.5, and 32.2 kg/ha, respectively. Here, the pod yield of peanut was 0.5 t/ha and the fresh pod yield of cowpea was 2.7 t/ha. In the cassava + Eucalyptus combination, the plant height and stem girth of Eucalyptus plants continuously increased up to 30 months. The plant height and stem girth of Eucalyptus plants were also found to be greater in the cassava + Eucalyptus + peanut and cassava + Eucalyptus + cowpea combinations. While about 53.1% of Eucalyptus plants in the pure stand attained a girth greater than 30 cm by 33 months, 63.1% plants in the Eucalyptus + cassava combination, 76.2% of plants in the cassava + Eucalyptus + peanut combination, and 71.9% of plants in the cassava + Eucalyptus + cowpea combination attained similar stem girth during the same period. The increase in stem height and girth of Eucalyptus plants in three intercropping combinations was because Eucalyptus probably competed with the intercrops and utilized nutrients applied to the intercrops, besides efficiently utilizing the soil moisture. At 32 months, the lateral root growth of Eucalyptus was adversely affected by cassava intercrop. In pure stand Eucalyptus plots, lateral roots of Eucalyptus plants extended up to 4.9 m, whereas in cassava + Eucalyptus plots, lateral roots of Eucalyptus plants extended up to 2.7 m. Thus, in cassava + Eucalyptus plots, all the cassava plants confronted the roots of Eucalyptus plants. Over a period of 33 months, total wood yield of Eucalyptus was little affected (28.1 t/ha) in a cassava + Eucalyptus combination as compared to pure stand (30.1 t/ha). However, total wood yield of Eucalyptus increased to 40.4 t/ha in the cassava + Eucalyptus + peanut

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combination, and to 43.5 t/ha in the cassava + Eucalyptus + cowpea combination. The increase in Eucalyptus wood yield when grown along with cassava and peanut or cowpea was attributed to the better utilization of soil moisture and nutrients by Eucalyptus trees. Cassava growth decreased in association with Eucalyptus + peanut, and was unaffected by cowpea. Total cassava biomass decreased 46.2% in cassava + Eucalyptus as compared to pure stand. During the first-year crop, Eucalyptus did not significantly affect the LAI of cassava. However, from the 2nd year onward there was a significant reduction in LAI of cassava under Eucalyptus (11–38%). Inclusion of cowpea along with cassava + Eucalyptus had no effect on the LAI of cassava. Over the period of 33 months, under Eucalyptus trees, the light intensity decreased from 85% to 47.4%. Such a reduction in light intensity may have caused reduction in photosynthesis of the cassava canopy. The nutrient uptake by cassava was lowest in the cassava + Eucalyptus combination compared to that in other cassava + perennial combinations. Here, the average NPK uptake by cassava was 97.6, 6.7, and 43.8 kg/ha. Inclusion of peanut or cowpea along with cassava + Eucalyptus reduced the NPK uptake by cassava to 81.7, 3.7, and 34.8 kg/ha, respectively. The decrease in LAI, canopy photosynthesis, and nutrient uptake in cassava under Eucalyptus trees probably reduced cassava biomass production and storage root yield. Storage root yield of cassava decreased to 11.2 t/ha when intercropped with Eucalyptus. Inclusion of peanut and cowpea with cassava + Eucalyptus reduced cassava yield to 10.8 t/ha. The nutrient uptake by peanut and cowpea was lowest in association with cassava + Eucalyptus, indicating that Eucalyptus competed with intercrops for nutrients. Here, the NPK uptake by peanut was 20.6, 1.0, and 10.28 kg/ha, respectively, and the NPK uptake by cowpea was 29.2, 1.1, and 29.0 kg/ha, respectively. The pod yield of peanut (0.4 t/ha) and the fresh pod yield of cowpea (1.9 t/ha) was lowest under Eucalyptus trees rather than under other perennials. The decrease in light intensity under Eucalyptus trees and the decrease in nutrient uptake by the legumes probably reduced the yield of peanut and cowpea when intercropped with cassava. In cassava + coconut intercropping, up to three years, cassava had no effect on the spread and length of the lateral roots of coconut. Coconut did not affect the LAI of cassava over the period of 32 months. Inclusion of peanut or cowpea along with cassava + coconut had no effect on the LAI of cassava. The nutrient (NPK) uptake, particularly N and K, by cassava was lower in the coconut + cassava combination than pure stand cassava. Inclusion of peanut or cowpea reduced the uptake of nutrients by cassava. The nutrient uptake by peanut and cowpea was higher in the coconut + cassava combination than in cassava + Leucaena. Under coconut trees, over the period of 32 months, the light intensity decreased

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from 94.5% to 81.8%, indicating light was not a limiting factor under coconut trees up to a period of 3 years. However, the total cassava biomass decreased 14.8%, whereas storage root yield decreased by 25.4% when intercropped with coconut as compared to pure stand. The decrease in nutrient uptake by cassava, particularly N and K, probably reduced storage root yield in cassava under coconut trees (Ghosh 1987). Under a coconut garden with 30-year-old trees and 86% shade (solar radiation 953 µEinstein/m2/s under full sun and 131 µEinstein/m2/s under the coconut garden), cassava plants increased their height (Ramanujam et al. 1984). The plant height of 12 cassava cultivars varied between 1.4 and 2.3 m under full sunlight and between 2.2 and 2.9 m under 86% shade. The increase in height was mainly due to internodal elongation. Shade also reduced branching of those cassava cultivars, that profusely branched under full sunlight. In 86% shade, the mean LAI of 12 cassava cultivars was 2.2 under full sunlight, and 2.4 under shade. Due to longer leaf life, the number of leaves retained at any time of cassava growth under shade is significantly higher. This results in higher LAI in cassava grown under shade than under full sunlight. The number of stomata, thickness of palisade and spongy parenchyma, and starch deposition in the vascular region were also drastically reduced in cassava leaves under shade as compared to the leaves under full sunlight (Ramanujam and Jose 1984; Ramanujam et al. 1984). A decrease in stomatal conductance to CO2 and increases in stomatal resistance to water vapor diffusion have also been reported under light intensity less than 1,000 µEinstein/m2/s in leaves of cassava plants grown under normal light intensity with a normal number of stomata (Palta 1982). Thus, under the shade conditions of a coconut garden, reduction in the number of stomata and palisade and spongy parenchyma increases mesophyll resistance to CO2 uptake, which in turn affects the efficiency of cassava leaves in terms of CO2 assimilation. Initiation of storage roots, which occurs beginning the 3rd week after planting under full sunlight, was delayed under shade. The time taken for initiation of storage roots for 12 cultivars varied between 26 and 30 days under full sunlight, and 45 and 54 days under 86% shade. The number of storage roots per plant was drastically reduced under shade. In 86% shade, crop growth rate (CGR) and storage root yield were drastically reduced. In 12 cassava cultivars, the CGR varied between 3.4 and 6.5 g/m2/day under open sunlight, and 1.0 and 2.9 under shade. The dry matter (DM) accumulation in shoots of 12 cassava cultivars grown under full sunlight and shade was on par with each other, while a significant difference was noticed for dry matter accumulated in storage roots. Under shade, DM accumulation in roots was drastically reduced and more DM accumulated in shoots than in roots. The storage root yield was 65–94% reduced

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among 12 cultivars under shade. The storage root yield varied between 1.8 and 2.6 kg/plant under full sunlight and between 160 and 800 g/plant under shade (Ramanujam et al. 1984). Thus, under the shade conditions of a coconut garden, assimilates of the cassava plant were mostly utilized for shoot growth, affecting storage root growth significantly. Storage root formation and photosynthesis limit the productivity of cassava under a coconut garden (Ramanujam et al. 1984). Under the shade conditions of a coconut garden, an increase in plant spacing from 60 × 60 cm to 120 × 120 cm increased plant height, while it decreased LAI in cassava plants. This means that the reduction in cassava plant density by increasing plant spacing, under shade conditions resulted in more dry matter production and accumulation per plant. The light transmission (light penetration to the lower layers of the cassava canopy) increased from 49% at closer spacing to 54–68% at wider spacing. This in turn increased storage root yield from 118 g/plant at closer spacing to 563 g/plant at wider spacing (Ramanujam et al. 1984). However, planting cassava in normal spacing (90 × 90 cm) under a pre-bearing coconut garden reduced the storage root yield of cassava by 53% compared to the pure stand (Ravindran and Nair 1999). In a 25-year-old coconut garden with trees planted at 7.5 × 7.5 m spacing, cassava planted at a spacing of 90 × 90 cm (8,000 plants/ha) yielded maximum storage root (Nayar and Sadanandan 1991). In various cassava + perennials intercropping systems, the highest net return was produced by the banana + cassava + cowpea or French bean system, closely followed by the banana + cassava system. Inclusion of legumes with cassava and Leucaena or Eucalyptus increased the net return (Ghosh 1987). Cassava seems to have a retarding effect on the growth of rubber trees (Lim 1969). Rubber growth can decrease when intercropped with cassava, resulting in a delay in opening for tapping and a consequent loss of returns to the farmer. Nevertheless, with adequate fertilizers and planting of the cassava intercrop at least 1.5 m from the rubber row, the effect on rubber can be reduced to a minimum (Pushparajah and Tan 1970). 2. Nutrient Management and Soil Fertility. Ghosh (1987) presents fertilizer requirements per hectare for cassava-based intercropping systems with perennials and legumes. For cassava, 100 kg N and 83 kg K in two equal split doses at planting and after 2 months (after harvest of the intercrop), and 43 kg P at the time of planting were applied. For banana, 180 kg N, 77.4 kg P, and 298.8 kg K in two equal split doses were applied 2 and 4 months after planting. For Leucaena, 43 kg P was applied at the time of planting. For Eucalyptus, 80 kg N, 4.3 kg P, and 12.5 kg K at the 7th month during the third year were applied per

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hectare. For coconut, 50 kg N, 13.8 kg P, and 99.6 kg K at the 3rd month; 170 kg N, 47.3 kg P, and 332 kg K at the 12th month; 340 kg N, 92.5 kg P, and 664 kg K at the 2nd year; and 500 kg N, 137.6 kg P, and 996 kg K at the 3rd year were applied. For peanut, 10 kg N, 8.6 kg P, and 16.6 kg K were applied. For French bean, 20 kg N, 12.9 kg P, and 33.2 kg K were applied. For cowpea, 10 kg N, 6.5 kg P, and 8.3 kg K were applied. All the legumes were fertilized at one month after planting. In all the cassava + perennial combinations, after the harvest of the first-year cassava crop, organic carbon increased, except in the case of coconut. There was a slight improvement in the available N of the soil where cassava was intercropped with Eucalyptus and coconut as compared to the pure stand of respective perennials. Available P decreased in the cassava + Eucalyptus combination, whereas it increased in the other cassava + perennials combinations. There was less available K in banana + cassava and cassava + Leucaena combinations and more in cassava + Eucalyptus and coconut + cassava combinations. During the second year, the organic carbon content tended to be low when perennials were grown alone compared to cassava + perennial combinations, except in the case of Leucaena, which remained the same. The available NPK status of the soil remained high in all the cassava and perennial combinations as compared to the respective pure stands of perennials. Over the period of two years, the soil fertility tended to decline in pure stand Eucalyptus and cassava + Eucalyptus combinations as compared to other perennials, which may have accounted for the low yield of cassava. Cassava in association with the perennials such as banana, coconut, and Leucaena maintained or slightly improved the soil fertility and the fertility status was almost similar to that found in a pure stand of cassava (Ghosh 1987). This indicates that soil fertility was not a limiting factor for cassava yield in three perennial combinations. When cassava was planted under a pre-bearing coconut garden, there was a slight reduction in N and P, whereas organic carbon and K increased. This indicates that cassava intercropping under coconut in no way affects the fertility status of a coconut garden (Ravindran and Nair 1999).

V. RELAY SEQUENTIAL CROPPING CASSAVA A. Lowlands In Kerala, India, where there is no waterlogging, two crops of rice followed by a fallow period or two crops of rice followed by a pulse crop are common practices. As the cultivation of rice is labor intensive and more than 70% of the cost of cultivation is attributed to wages, the net

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returns per unit area per unit time are discouraging. Mohankumar and Nair (1990) studied the various root and tuber cropping sequence systems for lowland conditions of Kerala where two crops of rice are produced each year. The study revealed that the aroid Amorphophallus + forage cowpea followed by vegetable cowpea gave the highest net income, one that was significantly superior to all other cropping sequences. The next best cropping sequence was vegetable cowpea followed by cassava, with a net income on par with cassava - peanut and rice - cassava sequences. The yields of short (7 months) duration cassava in lowland conditions were 47.6, 49.6, 33, and 30.6 t/ha in rice - cassava, cassava - peanut, cassava - vegetable cowpea - sweetpotato, and rice cassava - vegetable cowpea sequences, respectively. The grain yield of rice, pod yield of peanut, vegetable cowpea, and storage root yield of sweetpotato were 2.2, 0.9, 4.1, and 7.4 t/ha, respectively. This was presumably due to the availability of adequate soil moisture throughout the growth period. In the crop sequence vegetable cowpea-cassava, vegetable cowpea was grown as a duel-purpose crop. Within 60 days, two pickings of green pods (succulent seed stage) were achieved and the crop was uprooted and used as a green manure for the succeeding crop of cassava. Cassava yield could be maintained by adopting this practice and money could be saved in the cost of weed control. Thus, in lowland conditions where two crops of rice are harvested annually, maximum net returns per unit area and unit time are achieved with Amorphophallus + cowpea (green manure) followed by vegetable cowpea, and the next being the vegetable cowpea followed by cassava sequence. B. Uplands In Peru, growers commonly plant rice alone or with maize at the beginning of the rainy season. After a few weeks, cassava and plantain are relay planted among the rice seedlings. They interfere very little with the rice as they grow. After rice harvest, cassava and plantain grow rapidly and quickly develop a canopy. These crops are then harvested 6–12 months later (Wade and Sanchez 1984). In Kerala, India, in upland rainfed conditions, the usual practice is to grow one crop of rice during the rainy season. After the harvest of this crop, the land is left fallow due to lack of water for growing a second crop of rice. In an attempt to find a suitable cropping sequence for this situation, Mohankumar et al. (1985) studied various root and tuber crops in a cropping sequence. They found that the highest yield (64.4 t/ha) and net profit was obtained when cassava was grown as a pure stand during the first year. Cultivation of cassava after rice decreased the storage root

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yield of cassava to 41.7 t/ha and net income by 40.3% compared to pure stand cassava. Here, usually, cassava will be planted during April–May with the onset of rain and will be harvested in the next year by February–March, with a fallow period for 2 months. In this context, when a short-duration cassava cultivar is grown and harvested within a period of 7 months, the land will remain fallow for a period of 5 months. Mohankumar et al. (1999) studied various root and tuber double crop sequences in upland conditions. Here, average storage root yield of a short-duration cassava was significantly reduced to 24.6, 23.7, 25.6, and 27.3 t/ha when cassava was planted after the harvest of preceding shortduration crops such as maize, peanut, grain cowpea, or vegetable cowpea, respectively, compared to the yield in pure stand (38.6 t/ha). The differences in cassava yield in different cropping sequences were not significant. Thus, planting cassava during May and maintaining the land fallow after the harvest of cassava between December–April resulted in the highest cassava yields compared to cassava planted after the harvest of the short-duration crops. The reduction in storage root yield of lateplanted cassava was due to the lack of soil moisture during the bulking of storage root when cassava was planted after preceding crops or after fallow. When cassava was planted in May, up to the harvest of the crop in November, it was not subjected to drought, as the crop received rain during two monsoons for growth and development. Delaying the planting season of cassava from May to July or August caused a significant reduction in storage root yield because of a reduction in duration. The total dry matter production by cassava was highest (28.5 t/ha) in the cropping sequence vegetable cowpea - cassava, and 17.2, 18.3, 28.2, and 27.5 t/ha in the cropping sequences such as short duration cassava vegetable cowpea - sweetpotato, rice - short duration cassava - vegetable cowpea, cassava - peanut, and rice - cassava, respectively. In various cropping sequences, an increase in N application from 50 to 100 kg/ha and an increase in K application from 41.5 kg/ha to 83 kg/ha with the quantity of P remaining the same (21.5 t/ha) did not significantly affect cassava yield. Here, the highest P and K (44.1 and 340.1 kg/ha, respectively) were removed by the rice - cassava sequence, whereas the highest quantity of N was removed by the cassava - peanut sequence (276 kg/ha). The total N, P, and K uptake were 215.4, 44.1, and 340.1 kg/ha in the rice - cassava sequence; 276, 41.8, and 277.5 kg/ha in the cassava - peanut sequence; 174.6, 34.5, and 184.1 kg/ha in the short duration cassava - vegetable cowpea - sweetpotato sequence; and 214.2, 35.3, and 203.8 kg/ha in the rice - short duration cassava - vegetable cowpea sequence. A study of the economics of cassava-based sequential cropping systems revealed that short-duration cassava planted

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in May and harvested in December (in pure stand) followed by fallow gave higher returns than growing a seasonal crop in May before planting cassava (Mohankumar et al. 1999; Mohankumar and Nair 1996).

VI. MULTI-CROPPING MANAGEMENT A. Plant Type Plant type includes plant architecture, vigor, and maturity. In cassava, the characteristics of branching and vigor (leafiness) both influence the quantity of light intercepted during the early growth period and cassava’s competitive abilities. Although, cassava has a slow leaf area development during early stages of growth, there are some vigorous leafy culivars that establish their canopy early, and consequently, may not be suitable for intercropping. Cultivars with an erect growth habit (late branching), and medium vigor will provide less shade to an intercrop than those with early branching and high initial vigor. Thus, cassava cultivars with high initial vigor and early branching cause a greater reduction in the yield of French bean than do cultivars with medium vigor and late branching (Leihner 1983). The latter have erect growth habit and are more suitable for intercropping since they impose little competition on the intercrop initially and also can have high yield potential. In a grain legume and cassava association, early flowering and maturity of the legume cultivar is an important character. With early maturity, the period of competition with cassava is reduced and excessive shading of the legume during pod filling is avoided. In the length of time that both crops are together in the field, the interaction between them increases in an exponential manner and yields are mutually affected. For instance, in an association of cassava with the early-maturing legumes (French bean and cowpea), cassava storage root yield decreases when the legume maturity is greater than 100 days. For simultaneous planting, the associate crop should have a growth period of less than 100 days. For planting toward the end of the cassava growth period, the associate crop should not exceed 120 days to maturity when simultaneous harvesting of cassava and the intercrop is desired (Leihner 1983). When planted simultaneously, climbing types of legumes greatly reduce cassava yield as compared to either an erect or prostrate habit. When cassava was intercropped with erect, semi-erect, or prostrate cowpea types, the storage root yield decreased by 6–24%, whereas a cowpea cultivar with climbing growth habit reduced cassava storage root

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yield by 32% compared to a pure stand of cassava (Hegewald and Leihner 1980). However, climbing types of legumes such as the common bean (Phaseolus vulgaris), lima bean (Phaseolus lunatus), and velvet bean (Mucuna deeringiana) also may be selected for association with cassava toward the end of its growth period (Leihner 1983). Vigorous legume cultivars must be chosen for this purpose because these crops must compete with an already established cassava crop. Cassava, even when associated with the most vigorous climbing legumes, does not normally suffer a reduction in yield, because at this later phase cassava development is already completed (CIAT 1978; Leihner 1983). In a cassava + maize mixture, plant height, earlyness to maturity, and plant architecture of maize genotypes are factors contributing to the reduction of cassava yield. Similarly, cassava plant height, branching pattern, and vigor or leafiness are some important factors that determine its ability to compete with other crops. Cassava cultivars substantially differ in their response to intercropping with maize (Osiru and Ezumah 1994). Maize cultivars with low LAI and early (90 days) maturity cause less reduction in cassava yield (15–17 t/ha) as compared to the pure stand cassava yield (19 t/ha), but give lower grain yield (2 t/ha). Highyielding, hybrid maize cultivars with longer growth duration (120 days) cause greater reduction in cassava yield (13–5 t/ha) as compared to the pure stand yield, but give higher grain yield (3–4 t/ha). Although cassava yields are higher with early-maturing maize cultivars, the total productivity of the cassava and late-maturing maize cultivars mixture is higher when cassava is intercropped with high-yielding maize genotypes (Osiru and Ezumah 1994). Alternatively, maize cultivars that mature before 100 days and yield 3–4 t grain per hectare are ideal for intercropping with cassava. B. Planting Schedule The relative time of planting, that is, planting of the intercrop before, at the same time, or after cassava is an important factor that influences the productivity of the intercrops. Cassava does not impose much competition at the beginning of its growth period and at the same time does not tolerate much competition by the associated crop if the intercrop is planted much earlier than cassava. Therefore, cassava storage root yield may be drastically reduced if the intercrop is planted much earlier than cassava, imposing competition for light and other factors. On the other hand, if cassava is planted earlier than the intercrop, growth and yield of the intercrop can be affected by shading and competition for other growth resources. In many studies, the greatest yields in intercropping situations were obtained when both cassava and the intercrop (French

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bean or legumes or maize) were planted at the same time or with a difference in planting time of less than 1 week (Thung and Cock 1979). The yield of French bean was highest when it was planted 4 weeks before cassava and lowest when planted 6 weeks after cassava. When soybean was planted 1 month after cassava, soybean yield was severely affected. Here, the vigorous, early-branching cassava suppressed soybean seed yield more than the less vigorous late-branching cassava. When soybean was planted 1 month before cassava, soybean yield in the intercrop was the same as in pure stand. When cassava and soybean were planted at the same time, soybean yield was little reduced (Thung and Cock 1979). Tsay et al. (1986) investigated the appropriate time of planting of soybean with cassava. When early-maturing (90 days maturity), mediummaturing (120 days maturity), and late-maturing (150 days maturity) cultivars of soybean were intercropped with cassava at 5 weeks after cassava planting, both cassava and soybean plant height was not significantly affected as compared to pure stand. When early-maturing soybean cultivar was planted at 1 week or 14 weeks after cassava planting, soybean plant height was not significantly affected in both the cases as compared to pure stand. However, in both these plantings, as compared to pure stand, cassava plant height was significantly reduced. When earlymaturing soybean cultivar was planted at 9 weeks after cassava planting, both cassava and soybean plant height was not significantly affected (Tsay et al. 1986) as compared to pure stand. Compared to pure stand, total dry matter production per unit area of early-maturing soybean cultivar was significantly reduced by intercropping when soybean was sown at 9 and 14 weeks after planting cassava. Compared to pure stand, total dry matter production per unit area of early-maturing, mediummaturing, and late-maturing cultivars of soybean was not significantly reduced by cassava when soybean was sown at 5 weeks after planting cassava. Here, the late-maturing cultivar produced the highest total dry matter per unit area (Tsay et al. 1986). Compared to pure stand, the LAI of early-maturing soybean cultivar was insignificantly reduced by cassava when soybean was sown at 1, 5, and 9 weeks after planting cassava, but it was significantly reduced when soybean was sown at 14 weeks after planting cassava. When soybean was sown at 5 weeks after cassava planting, intercropping insignificantly reduced the LAI of medium- and late-maturing soybean cultivars. Compared to pure stand, seed yield per unit area of early-maturing soybean cultivar was insignificantly reduced by cassava when soybean was sown at 1 and 5 weeks after planting cassava, but it was significantly reduced when soybean was sown at 9 and 14 weeks after planting cassava. The lowest seed yield of soybean achieved in the case of 9 and 14 weeks after planting cassava

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relative to the pure stand yield was mainly due to a reduction in the number of pods per plant as a result of shading from associated cassava. The soybean pod number per plant and the 100-seed weight were reduced when plants were continuously shaded (Kuo et al. 1978). Compared to pure stand, seed yield per unit area of early-, medium-, and latematuring soybean cultivars was not significantly reduced by cassava when soybean was sown at 5 weeks after planting cassava (Tsay et al. 1986). Although the medium- and late-maturing soybean cultivars were expected to produce higher total dry matter and higher seed yields per unit area than the early-maturing soybean cultivar both in pure stand and in intercrop, all three cultivars produced similar seed yields both in pure stand and in intercrop (nearly 2 t/ha). This was associated with a decrease in the efficiency of light energy conversion of medium- and late-maturing soybean cultivars rather than a decrease in light interception. While the growth of early-, medium-, and late-maturing cultivars of soybean sown at 5 weeks after cassava planting were only minimally affected and their seed yields were close to the pure stand yield, the growth of cassava was affected differently, with the least effect caused by the early-maturing soybean cultivar. The medium- and latematuring soybean cultivars were taller and occupied cassava inter-row spaces for longer periods. This resulted in a long delay in the development of the cassava canopy and consequently affected cassava yield. Thus, tall soybean cultivars with long growing seasons are unsuitable for intercropping with cassava. It is therefore possible to achieve high soybean yields when semi-dwarf, early-maturing soybean cultivars are intercropped with a less vigorous cassava genotype or with cassava grown in sub-optimal conditions. The yield of soybean sown at a later period of cassava growth (5 months after planting cassava) will be more affected by rapid growth and subsequent ground cover of cassava. Because shoot growth often dominates storage root growth in cassava, the intercrop should influence shoot growth of cassava without reducing storage root yield. A long growing season (10 months) gives cassava an opportunity to recover from the effect of intercropped soybean (Tsay et al. 1986). The storage root yield as well as starch content of cassava was not affected when a bushy French bean was intercropped at the 7–9th month after planting cassava. On the other hand, compared to pure stand yield (1.2–2.3 t/ha), French bean yields were reduced to 0.65, 0.85, and 0.64 t/ha when planted at 7, 8, and 9 months after cassava planting, respectively (CIAT 1981). Here, the differences in the yields of French bean intercropped under the 7–9th month crop of cassava were not significant. However, in a double intercropping system, under the agroclimatic conditions of Kerala, India, it was not possible to raise a second

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intercrop of short-duration legumes such as black gram (Vigna mungo), horse gram (Dolichos uniflorus), and mungbean immediately after the harvest of first intercrop with cassava (Meera Bai et al. 1991). This was because, at the time of harvest of the first intercrop, cassava developed enough canopy to cover the entire field at 3 MAP, and the sunlight penetration into the ground was less than 10% of solar radiation falling on the top of the cassava canopy. Another reason for the non-establishment of the second intercrop is that the cassava growth period (7–10 months) coincided with the dry period, resulting in low moisture in the soil. When cassava and pigeonpea were planted simultaneously, pigeonpea emerged 5 days after sowing, and cassava emerged 2 weeks after planting. Thus, in a cassava + pigeonpea system, when both component crops are simultaneously planted, cassava emerges 9 days later than pigeonpea (Cenpukdee and Fukai 1992a). In one study (Cenpukdee and Fukai 1992c), in pure stand, the final plant height of cassava was 170 cm and 120 cm in a tall and a short stature cultivar, respectively, at 200 days after planting (DAP). The highest canopy width was 150 cm and 100 cm in a tall and a short stature cassava cultivar, respectively, at 150 DAP. Pigeonpea height was 150 cm in pure stand at 100 DAS. Simultaneous planting of cassava and pigeonpea resulted in pigeonpea being taller and dominant over cassava. Here, simultaneous planting of cassava and pigeonpea with both lower (67,000 plants/ha) and higher (267,000 plants/ha) pigeonpea population, the height of pigeonpea (150 cm) remained higher than the tall cassava cultivar up to 100 DACP. But, the height of a short stature cassava cultivar remained lower than that of pigeonpea, until the time of pigeonpea harvest (160 days). Simultaneous planting of cassava and pigeonpea, with high pigeonpea population, resulted in a canopy width of 150 cm in pigeonpea at 100 DAS, but depressed the canopy width to less than 50 cm in a tall and short stature cassava cultivar. Canopy width of both tall and short stature cassava cultivars recovered after the harvest of pigeonpea at 160 DAS but attained only 50 cm in a tall cultivar and less than 50 cm in a short stature cultivar. With lower pigeonpea population, canopy width of pigeonpea was reduced to 100 cm at 100 DAS. Here, canopy width, which remained less than 50 cm at 100 DAS, improved to more than 100 cm in a tall cassava cultivar, and to 50 cm in a short stature cassava cultivar after the harvest of pigeonpea. As a result, regardless of pigeonpea population, simultaneous planting of both the component crops facilitates more light interception by pigeonpea than the associated cassava. Delayed planting of pigeonpea by 35 DACP did not affect the height of both tall and short stature cassava cultivars at both higher and lower pigeonpea population. But, pigeonpea plant height was less (100 cm) in delayed

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planting than in simultaneous planting (150 cm). Delayed planting of pigeonpea by 35 DACP at both a higher and a lower pigeonpea population minimally affected the canopy width of a tall cassava cultivar compared to a short stature cultivar. Here, pigeonpea canopy width was more affected (50 cm or less than that) than with a short stature cassava cultivar (100 cm or less than that) at 100 DAS. Thus, delayed planting of pigeonpea by 35 DACP helps the taller cassava cultivar obtain higher light interception than pigeonpea, at both a lower and a higher pigeonpea population. The delayed planting of pigeonpea helps the short stature cassava cultivar obtain higher light interception only at a lower pigeonpea population but not at a higher pigeonpea population. Simultaneous planting reduced LAI of a tall cultivar more than delayed planting of pigeonpea. But, in both simultaneous and delayed planting, the reduction in LAI was significant as compared to pure stand. In a short statured cassava cultivar, both simultaneous and delayed planting of pigeonpea adversely affected LAI, resulting in total leaf shedding at the time of harvest. The LAI of pigeonpea was affected less by simultaneous planting than by delayed planting of pigeonpea. The variation in light interception by cassava cultivars due to the differences in time of planting and pigeonpea population resulted in a significant reduction in the TDM production and storage root yield of cassava as compared to pure stand crop. The effect was more pronounced in a short stature cassava cultivar than in a tall cultivar and at a higher population of pigeonpea than at a lower population. Simultaneous planting of cassava and pigeonpea resulted in higher seed yield of pigeonpea (1.1–1.6 t/ha) than planting pigeonpea 35 DACP (0.3–0.9 t/ha). The effect was more pronounced in a short stature cassava cultivar (1.3–1.5 t/ha) than in a tall cultivar (1.1–1.2 t/ha). However, in both simultaneous and delayed pigeonpea planting, pigeonpea seed yield was significantly reduced compared to pure stand yield (1.4–1.7 t/ha). When planting of pigeonpea was delayed by 35 DACP, cassava storage root yield was higher (7.3 t/ha) than pure stand yield (6.5 t/ha) only in a tall stature cassava cultivar at a lower pigeonpea population, and the reduction in yield of this cultivar was not significant at a higher pigeonpea population (5.3 t/ha). However, with tall and short stature cassava cultivars, pigeonpea seed yield was significantly reduced (0.3–0.9 t/ha) as compared to pure stand yield (1.3–1.5 t/ha). The effect of pigeonpea population was insignificant for both sowing times and both cassava cultivars. Thus, in a cassava + pigeonpea system, the possiblity of increasing the efficiency of the system through adjusting the planting time appears to be limited. Mungbean and cassava or soybean and cassava may be planted simultaneously, whereas peanut may be planted 20 days earlier than cassava

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for achieving the highest yields of component crops (Sinthuprama 1979). Here, planting cassava and mungbean simultaneously resulted in a 27.4 t/ha storage root yield in cassava and a 1.1 t/ha grain yield in mungbean. Planting cassava and soybean simultaneously resulted in 24.0 t/ha storage root yield in cassava and 0.6 t/ha seed yield in soybean. Planting soybean 20 days after planting cassava increased soybean yield to 0.8 t/ha but decreased cassava yield to 12.6 t/ha. Planting peanut 20 days after planting cassava resulted in 24.6 t/ha storage root yield in cassava and 1.3 t/ha peanut yield. Planting cassava 1 month after maize (delayed planting) caused a significant reduction in cassava storage root yield only when cassava was planted in a single row (250 cm between cassava rows × 50 cm between plants within the row) as compared to simultaneous planting. The average cassava yield was 35 t/ha in simultaneous planting and 31.5 t/ha in delayed planting. The reduction in cassava storage root yield was not significant, as compared to simultaneous planting, when cassava was planted in a double row arrangement (100 cm between 2 subsequent cassava rows × 550 cm between 2 subsequent cassava paired-rows × 50 cm between cassava plants within the row). Here, cassava yield was 32.7 t/ha in simultaneous planting, and 34 t/ha in delayed planting. On the other hand, delayed planting resulted in a high maize grain yield compared to that in simultaneous planting, but the difference in maize yield was insignificant. Here, maize grain yield was 3.2 t/ha in delayed planting, and 3.0 t/ha in simultaneous planting. In both simultaneous planting and delayed planting, a second crop of maize or peanut resulted in an average maize grain yield of 2.5 t/ha, and peanut yield of 1.8 t/ha (Guritno and Sugito 1990). Cassava can be planted 1 or 2 months after planting intercrops such as maize + rice (followed by mungbean or soybean) or maize + peanut or soybean, without reduction in cassava yield. However, a 3-month delay in planting cassava after planting intercrops in a cassava + maize + peanut or soybean system significantly decreased cassava yields, particularly in the dry season. On the other hand, yields of the intercrops were not affected. In a wet season, a 3-month delay in planting cassava after planting maize + peanut decreased the yield of cassava from 27.4 to 25.1 t/ha. In a dry season, a 3-month delay in planting cassava after planting maize + soybean decreased the yield of cassava from 27.3 to 16.5 t/ha. In the intercropping systems, yields of peanut, soybean, and maize were 0.4, 0.5, and 2.8 t/ha, respectively (Wargiono et al. 1995). A three-month delay in planting cassava after planting intercrops in a maize + rice (followed by soybean) system significantly decreased the yields of cassava but had no effect on the yields of intercrops. Here, the

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yields of cassava substantially decreased from 39.8 to 21.8 t/ha. The yields of maize, rice, and soybean were 2.6, 2.0, and 0.31 t/ha, respectively (Wargiono et al. 1995). A three-month delay in planting cassava after planting intercrops in a maize + rice (followed by mungbean) system significantly decreased the yields of cassava but had no effect on the yields of intercrops. A three-month delay in planting cassava after planting maize + rice followed by mungbean significantly decreased the yields of cassava from 18.5 to 4.7 t/ha. Here, the yields of maize, rice, and mungbean were 1.1, 2.2, and 0.42 t/ha, respectively (Wargiono et al. 1995). In a yam + maize + cassava mixture, delaying the introduction of cassava by 28 or 56 days after planting yam and maize significantly increased yam tuber and maize grain yields but reduced cassava storage root yield significantly (Odurukwe and Ikeorgu 1994). In this crop combination, cassava storage root yield was highest (22.0 t/ha) when planted with yam and maize at the same time. Each 28-day delay in the introduction of cassava into the yam + maize system resulted in a 29% decrease in cassava yield. Delaying introduction of cassava by 28 days significantly increased yam tuber yield by 17.5%. Further delay did not affect the yam yield. Delay in the introduction of cassava into the yam + maize system significantly increased maize grain yield. Delaying for the initial 28 days increased maize grain yield by 14%, as compared to simultaneous planting. A further 28-day delay increased maize grain yield by 27.5%. Here, cassava depressed tuber yield of yam by 56% and maize grain yield by 23% if planted at the same time. Therefore, in a yam + maize + cassava mixture, a farmer who needs the highest yields of yam and maize may delay planting cassava by 28 days with a loss of 29% cassava yield. In a cassava + rice system, the time of introducing rice into cassava significantly affected cassava storage root yield and its components. In one study, the storage root yield of cassava increased from 2.3 t/ha to 11 t/ha as the time of introducing rice into cassava was delayed from 0 weeks to 6 weeks after planting (WAP) cassava (Jalloh et al. 1994). Cassava yield was 14.4 t/ha in pure stand crop. Here, the storage root yield of cassava was reduced 84, 61.8, 36.8, and 23.6%, as compared to pure stand yield when rice was introduced into cassava at 0, 2, 4, and 6 WAP cassava, respectively. Similarly, the number of storage roots produced per plant and the weight of a single storage root increased as the time of introducing rice into cassava was delayed from 0 weeks to 6 WAP cassava. The number of storage roots produced per plant increased from 1.4 to 3.8 as the time of introducing rice into cassava was delayed from 0 weeks to 6 weeks after planting cassava. The weight of a single storage root increased from 160g to 290g as the time of introducing rice into

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cassava was delayed from 0 weeks to 6 weeks after planting cassava. In pure stand cassava, the number of storage roots produced per plant was 4.5 and the weight of a single storage root was 330g. Cassava plants grew taller, branched at a higher height, and had thinner stems with earlier introduction of rice, that is, when rice was introduced into cassava within 2 WAP cassava. This was because of the strong competitive ability of rice compared to that of the relatively slow growing cassava. However, after the harvest of rice, cassava recovered rapidly and the effect was not perceptible at the time of cassava harvest at 12 MAP. Rice grain yield decreased insignificantly as the time of the sowing of rice was delayed from 0 WAP to 6 WAP in both pure stand and intercropped rice. However, rice grain yield was greater in pure stand than in intercropped rice. Here, LER increased from 1.0 to 1.5 as the time of introducing rice into cassava was delayed from 0 weeks to 6 WAP cassava. Thus, the result of this study suggests that in cassava + rice mixtures, for obtaining higher cassava yields, it should be planted 4–6 weeks before rice. In Indonesia, with the onset of monsoon, maize is sown on hills in rows with spacing of 200 cm between rows × 50 cm between plants within rows, at a population of 20,000 plants/ha (2 seeds/hill). Two weeks later, rice is sown on hills (5 seeds/hill) between the maize rows with spacing of 40 cm between rows × 10 cm between plants within rows. If early maturing (90 days) maize cultivar is used, maize and rice are sown at the same time. One and a half month after sowing maize, cassava is planted between the rice hills in every other row, with spacing of 4 m between cassava rows × 50 cm between plants within a row. After harvesting the rice, the straw is cut close to the ground and pushed aside into the cassava rows. Peanut is sown (1 seed/hill) beside each hill of rice stubble with spacing of 50 cm between rows × 10 cm between plants within a row. The rice straw is then spread out on the field surface as mulch to suppress weed growth, conserve both soil moisture and organic matter, and prevent soil erosion. After the peanut harvest, cowpea seeds are sown on hills (2 seeds/hill) with spacing of 40 cm between rows × 20 cm between plants within a row and harvested before the harvest of cassava (Soedomo and Soegiyanto 1983). Thus, maize planted in October of the previous year is harvested in January of the next year (4 MAS), cassava planted in November of the previous year is harvested in September of the next year (11 MAP), rice planted in November of the previous year is harvested in March of the next year (5 MAS), peanut planted in April is harvested in June (3 MAS), and cowpea planted in July is harvested in September (3 MAP) before cassava.

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C. Plant Density and Spatial Arrangement Plant density and planting pattern or spatial arrangement of crops in the field is of great importance in intercropping systems because it may affect the efficiency with which solar radiation, space, soil nutrients, and other resources are utilized. In South East Asian countries such as China, Thailand, Vietnam, Indonesia, Malaysia, and the Philippines, in a pure stand, cassava is planted with spacing of 80–100 cm (between rows) × 80–120 cm (between plants within a row) with a population ranging between 10,000 and 15,625 plants/ha (Howeler 2001; Tongglum et al. 1987; Wargiono et al. 1995, 1998, 2001; Li Jun et al. 2001). Here, to accommodate leguminous intercrops (mungbean, peanut, soybean), cassava is planted at a wide spacing of 200 cm (between cassava rows) × 50 cm (between cassava plants within a row). In Africa, cassava is planted, mostly with intercrops, at a density varying between 10,000 and 15,000 plants/ha depending on cultivar and branching habit (Hahn et al. 1979). In Latin America, in traditional intercropping systems, cassava is often planted at lower densities than in pure stand. In this region, planting densities vary between 3,000 and 25,000 plants/ha (the average is 11,300 plants/ha) for cassava as a pure stand, and between 4,000 and 18,000 plants/ha for intercropped cassava (the average is 8,300 plants/ha) (Leihner 1983). In India, in single row spacing at 90 × 90 cm (90 cm between rows × 90 cm between plants within a row), cassava is planted at a density of 12,435 plants/ha both as pure stand, and with an intercrop (Mohankumar and Hrishi 1979; Anilkumar and Sasidhar 1985, 1987; Bridgit et al. 1985; Prabhakar and Nair 1988, 1992; Sheela and Mohamed Kunju 1988; Meera Bai et al. 1991). At wider spacing, cassava is planted in lower densities. At 1.0 m × 1.0 m spacing, cassava is planted at a density of 10,000 plants/ha both as a pure stand, and with an intercrop (Prabhakar et al. 1982). In the paired row method, at 45/135 × 90 cm spacing (45 cm between two subsequent cassava rows making up a pair, 135 cm between two such pairs and 90 cm between plants within the row), cassava is planted at a density of 12,345 plants/ha both in a pure stand, and with an intercrop (Mohankumar and Hrishi 1979; Anilkumar and Sasidhar 1985, 1987; Prabhakar et al. 1982; Prabhakar and Nair 1992). In CIAT conditions, the variation in the spatial arrangement of cassava from square (100 × 100 cm) to rectangular (200 cm × 50 cm, wide row) did not affect cassava yield, given the same plant density (10,000 plants/ha) in pure stand (CIAT 1977, 1980). Here, the average cassava yield was 23 t/ha in the square method and 24.5 t/ha in the rectangular method. Cassava planted in single rows at 100 × 80 cm spacing (100 cm

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between cassava rows × 80 cm between plants within the row), and paired rows with 60/200 × 60 cm spacing (60 cm between 2 subsequent cassava rows × 200 cm between 2 such paired rows × 60 cm between plants within the row), at the same plant density (12,500 plants/ha), had a similar growth rate, dry matter accumulation, and partitioning in pure stand (Porto 1990). A plant population lower than that normally planted in pure stand, along with the competition imposed by the intercrop, may partially reduce the yield of cassava in intercropping systems as compared to the pure stand yield. However, planting cassava at pure stand density may minimize the reduction in storage root yield per unit area of intercropped cassava. On the other hand, the yield of an intercrop may decrease due to the lower plant density of the intercrop, and also due to the mutual competition between the component crops. An intermediate or moderate cassava plant population may minimize the reduction in yield of the intercrop (Fonseca 1981). The plant height and canopy width are important factors that determine the optimum population for component crops in an intercropping system. In pure stand, the highest cassava yield can be achieved from leafy and early branching cultivars planted at relatively low densities (5,500–6,900 plants/ha). These low densities can also produce the highest yields in intercropping. On the other hand, cultivars with less foliage and late branching may produce the highest yield at intermediate plant densities (6,900–9,300 plants/ha), and at this plant density, acceptable yields of cassava can be obtained in intercropping (Thung and Cock 1979). Therefore, the optimum pure stand cassava plant population can be planted in an appropriate arrangement in an intercropping system without causing excessive yield reduction of the component crops (Mohankumar and Hrishi 1979; Leihner 1983; Anilkumar and Sasidhar 1985, 1987; Bridgit et al. 1985; Anilkumar and Sasidhar 1987; Prabhakar and Nair 1988, 1992; Sheela and Mohamed Kunju 1988; Meera Bai et al. 1991). Higher intercrop densities are likely to compete more with cassava, and reduce its yield as compared to lower densities. The optimum plant spacing and population for legumes and non-legumes (maize and rice) for pure stand have been discussed earlier. In a cassava + French bean system, the bean yield was greater when intercropped with a less vigorous type of cassava and the bean yield increased with an increase in its plant density up to 40 plants/m2. However, the bean yield decreased with an increase in cassava plant density beyond 5,500 plants/ha (Thung and Cock 1979). In India, in the normal method where cassava is planted at 90 × 90 cm spacing (90 cm between cassava rows and 90 cm between cassava plants within a row with 12,345 plants/ha), the intercrop (legume) is planted in between cassava rows with 20–30 cm (between

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legume rows) × 15–20 cm (between plants within a row) at a density of 66% of pure stand density (Mohankumar and Hrishi 1979; Anilkumar and Sasidhar 1985; Bridgit et al. 1985; Anilkumar and Sasidhar 1987; Prabhakar and Nair 1988, 1992; Sheela and Mohamed Kunju 1988; Meera Bai et al. 1991). When there is wider plant spacing, the intercrop is planted in lower densities. At 1.0 m × 1.0 m spacing (1.0 m between cassava rows and 1.0 m between plants within a row with 10,000 plants/ha), the intercrop (legume) is planted at a density of 54% of a pure stand density (Prabhakar et al. 1982). In the paired-row method, that is, 45/135 × 90 cm spacing (45 cm between two subsequent cassava rows making up a pair, 135 cm between two such pairs and 90 cm between plants within the row with 12,345 cassava plants/ha), the intercrop (legume) is planted in 3–5 rows (20×30 cm between rows × 15–20 cm between plants within the row) at a density of 61% of a pure stand density (Mohankumar and Hrishi 1979; Anilkumar and Sasidhar 1987; Prabhakar et al. 1982). However, experiments conducted in CIAT conditions show that the grain legume plant density that gives the best results as pure stand can also be used in intercropping systems by planting cassava at a lower plant density as compared to its pure stand density (Thung and Cock 1979; CIAT 1980; Hegewald and Leihner 1980; Fonseca 1981). Here, cassava yield was not substantially affected (the average yield was 25 t/ha) with an increase in cowpea plant density between 50,000 and 200,000 plants/ha or peanut plant densities between 100,000 and 600,000 plants/ha (CIAT 1980). Therefore, grain legume plant populations that yield highest in pure stand can also be used in intercropping systems with cassava. In CIAT conditions, the plant populations for legumes are 250,000 for French bean (bush type), mungbean, and peanut; 160,000 for French bean (climbing type); and 110,000 for cowpea per hectare and they are recommended for intercropping with cassava (Leihner 1983). Planting cassava in paired rows with wider spacing between cassava rows has no significant influence on the storage root yield per unit area of cassava but, on the other hand, it often significantly increases the yield of intercrops. The paired-row method facilitates the operation of mechanical devices, furrowing, and ridging, especially in soils with poor drainage (Mattos et al. 1980). The paired-row method also increases illumination of the leaves in the canopy as well as the period of photosynthesis per leaf, and minimizes leaf shedding (Porto 1990). Prabhakar and Nair (1992) intercropped cassava with peanut using different spatial arrangements at the same cassava plant density (12,345 plants/ha). Cassava was planted with narrow (single) row spacing (90 × 90 cm) and 2 rows of peanut were planted at 30 cm spacing in between

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2 rows of cassava, or cassava was planted in wide rows at 180 cm (between 2 subsequent cassava rows) × 45 cm (between plants within the row) spacing and 4 or 5 rows of peanut were planted in between 2 rows of cassava. Here, cassava yield was higher in pure stand than in intercropping in both rainfed and irrigated conditions. In pure stand, cassava yield was higher in narrow row spacing than wide row spacing, but the difference was insignificant. Here, cassava yield was higher (31.6 t/ha) in narrow row spacing than in wide row spacing (28.4 t/ha) in rainfed conditions. Irrigation increased cassava yield to 41.1 t/ha and 38.8 t/ha in narrow and wide row spacing, respectively. In both rainfed and irrigated conditions, peanut yield increased with an increase in its density but decreased cassava yield. In rainfed conditions, cassava yield decreased from 31.6 t/ha in pure stand to 24.5 t/ha in intercropping in narrow row spacing and the difference was insignificant. Similarly, cassava yield significantly decreased from 28.4 t/ha in pure stand to 19.3 t/ha in intercropping in wide row spacing. Irrigation minimized the decrease in cassava yield in intercropping. In irrigated conditions, cassava yield decreased from 41.1 t/ha in pure stand to 37.7 t/ha in intercropping in narrow row spacing. Similarly, cassava yield decreased from 38.8 t/ha in pure stand to 35.8 t/ha in intercropping in wide row spacing. The difference in intercropped cassava yield between wide row spacing and normal row spacing was not significant. In rainfed conditions, cassava yield decreased from 24.5 t/ha in narrow row spacing to 19.3 t/ha in wide row spacing. Similarly, in irrigated conditions, cassava yield decreased from 37.7 t/ha in narrow row spacing to 35.8 t/ha in wide row spacing. In both rainfed and irrigated conditions, peanut yield did not differ significantly between narrow row and wide row spacing. In rainfed conditions, in both narrow row and wide row spacing, peanut yield was 1.0 t/ha. In irrigated conditions, peanut yield was 1.4 t/ha in narrow row spacing and 1.5 t/ha in wide row spacing. An increase in the peanut population from 2 to 5 rows in between cassava rows increased peanut yield in both rainfed (1.0 to 1.1 t/ha) and irrigated conditions (1.4 to 1.6 t/ha). Intercropping with peanut or cowpea significantly decreased cassava yields in both single row spacing (90 × 90 cm) and paired row spacing (45/135 × 90 cm, 45 cm between two subsequent cassava rows, 135 cm between two such pairs and 90 cm between plants within the row with 12,345 cassava plants/ha) as compared to pure stand yield (Anilkumar and Sasidhar 1985). In pure stand, cassava yield was significantly higher in paired row spacing than in single row spacing. Here, cassava yield was 20.4 t/ha in paired row spacing and 18.0 t/ha in single row spacing. But the difference in intercropped cassava yield between the single and

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paired row spacings was not significant. When cowpea was planted between 2 cassava rows (30 cm between cowpea rows × 20 cm between plants within the row), cassava storage root yield decreased to 11.7 t/ha in single row spacing and to 10.3 t/ha in paired row spacing. When peanut was planted between 2 cassava rows (30 cm between peanut rows × 20 cm between plants within the row), cassava storage root yield decreased to 12.8 t/ha in single row spacing and to 13.4 t/ha in paired row spacing. In a cassava + fodder cowpea system, in pure stand, cassava storage root yield was 46.0 t/ha, in single row spacing at 75 × 75 cm (17,778 plants/ha), 46.2 t/ha in paired row spacing at 60/90 × 75 cm (60 cm between 2 cassava rows × 90 cm between 2 subsequent cassava rows × 75 cm between plants within the row, 17,778 plants/ha), and 31.6 t/ha at 75/150 × 75 cm (75 cm between 2 cassava rows × 150 cm between 2 subsequent cassava rows × 75 cm between plants within the row, 13,330 plants/ha). Obviously, the reduction in cassava plant population in 75/150 × 75 cm spacing reduced cassava yield but resulted in the highest green fodder yield. Intercropping with fodder cowpea significantly increased cassava yield in single row spacing, and paired row spacing at 60/90 × 75 cm as compared to pure stand yield. Intercropped cassava storage root yield was 50.3 t/ha, 56.5 t/ha, and 33.1 t/ha in 75 × 75 cm spacing, and in paired row spacing at 60/90 × 75 cm and 75/150 × 75 cm, respectively. On the other hand, green fodder yield of cowpea was 13.7 t/ha in pure stand. Green fodder yield of cowpea significantly decreased to 3.2 t/ha, 2.9 t/ha, and 6.7 t/ha in single row spacing at 75 × 75 cm spacing, and in paired row spacing at 75/150 × 75 cm, and 60/90 × 75 cm, respectively, in intercropping (Anilkumar et al. 1991). Inclusion of peanut or cowpea as intercrop increased the storage root yield of cassava in both single row (90 cm × 90 cm) and paired row spacing (45 cm/135 cm × 90 cm, 45 cm between 2 subsequent cassava rows, 135 cm between 2 such pairs, and 90 cm between plants within the row) as compared to the pure stand yield in respective spacing, but the increase was not significant (Meera Bai et al. 1991). In pure stand, cassava yield did not differ significantly between normal row spacing and paired row spacing. Here, in both the cases, cassava yield was 19.6 t/ha. Intercropping increased cassava yield to 22 t/ha and 21.0 t/ha in peanut and cowpea, respectively, in both normal and paired row spacing. On the other hand, the yield of intercropped peanut and cowpea significantly decreased in both normal and paired row spacing as compared to their yield in pure stand. In pure stand, the average peanut pod and cowpea grain yield was 1.8 t/ha and 2.7 t/ha, respectively, in both single and paired row spacing. Intercropping reduced peanut yield to

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0.8 t/ha in single row spacing and to 0.9 t/ha in paired row spacing. However, in the case of cowpea, the reduction in grain yield was greater in the paired-row method as compared to the normal row spacing. Intercropped cowpea grain yield was 1.8 t/ha and 2.6 t/ha in paired and normal row spacing, respectively. Thus, as long as optimum plant density is maintained, cassava is flexible toward variations in planting patterns. Fonseca (1981) evaluated three spatial arrangements of planting cowpea in between cassava rows to accommodate more legumes. In both pure stand and intercropped cowpea, grain yields were highest in the 60/3 spatial arrangement with 110,000–140,000 cowpea plants/ha. Here, the average cowpea grain yield was 1.7 t/ha. The yield advantage of the 60/3 spatial arrangement was significant when compared to the 70/2 and 45/2 spatial arrangements with 140,000 cowpea plants/ha. Here, cassava was planted with spacing of 180 cm (between 2 rows of cassava) × 60 cm (between plants within a row). In the 60/3 spatial arrangement, 3 rows of cowpea were planted in between 2 rows of cassava with spacing of 60 cm between cassava and cowpea rows, and 30 cm between 2 cowpea rows. In the 70/2 spatial arrangement, 2 rows of cowpea were planted in between 2 rows of cassava with spacing of 70 cm between cassava and cowpea rows, and 40 cm between 2 rows of cowpea. In the 45/2 spatial arrangement, 2 rows of cowpea were planted in between 2 rows of cassava with spacing of 45 cm between cassava and cowpea rows, and 90 cm between 2 rows of cowpea. In intercropping, the differences in cowpea grain yields in different planting arrangements (60/3, 70/2, and 45/2 with 80,000–140,000 cowpea plants/ha) were not significant except in the 60/3 planting arrangement. Here, the average cowpea yield was 1.2 t/ha. Planting cowpea at the density of 140,000 plants/ha in the 60/3 arrangement significantly increased the grain yield to 1.4 t/ha. Similar results were obtained in the 60/3 and 75/2 arrangements in the cassava + peanut system. Planting cassava and peanut in the 60/3 arrangement resulted in the highest peanut yield compared to that of the 70/2 arrangement over the peanut plant densities between 150,000 and 300,000 plants/ha. Here, the highest peanut yield was 1.1 t/ha and 0.9 t/ha in pure stand and intercropping, respectively, in the 60/3 planting arrangement. In one study, the cassava yield decreased by 29, 42, and 30% when cassava and cowpea were grown in 1:1, 1:2, and 2:2 row arrangements, respectively, as compared to pure stand yield (Olasantan 1988). Here, cassava density was 13,900 plants/ha in pure stand, 7,000 plants/ha in the 1:2 row arrangement (cassava 1 row:cowpea 2 rows, 50 cm between rows, 100 cm between plants within the cassava row and 30 cm between plants within the cowpea row), and 11,000 plants/ha in the 1:1 and 2:2 row arrangements (cassava 1 row:cowpea 1 row or cassava 2 rows:cow-

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pea 2 rows). Cowpea density was 42,000 plants/ha in pure stand, 48,000 plants/ha in the 1:2 row arrangement, and 34,000 plants/ha in the 1:1 and 2:2 row arrangements. When intercropped with cowpea, cassava yield significantly decreased to 11.4 t/ha as compared to pure stand yield (18.9 t/ha), only when cassava and cowpea were planted in the 1:2 row arrangement. Cassava intercropped with cowpea in the 1:1 or 2:2 row arrangements yielded more (average yield 13.1 t/ha) as compared to the 1:2 row arrangement (11.4 t/ha). The significant decrease in storage root yield of cassava in the 1:2 row arrangement as compared to pure stand yield was mainly due to the 50% reduction in its plant density as compared to its pure stand density. The reduction in storage root yield of cassava in the 1:1 and 2:2 row arrangements were due to the 21% reduction in cassava plant density as compared to its pure stand density. On the other hand, cowpea grain yield was not significantly reduced due to intercropping. Intercropped cowpea grain yield was 0.7 t/ha, 0.9 t/ha, and 0.8 t/ha in cassava:cowpea planted in the 1:1, 1:2, and 2:2 row arrangements, respectively. The decrease in cowpea yields in cassava:cowpea planted in the 1:1 or 2:2 row arrangements was due to the 19% reduction in cowpea plant density as compared to pure stand density. The highest cowpea yield in the 1:2 row arrangement was due to the 14% increase in cowpea plant density as compared to pure stand density. In one study, cassava was planted in wide rows at 180 cm (between rows) × 60 cm (between plants within a row) spacing at a population of 9,259 plants/ha. Cowpea or peanut was planted in 3 rows at 60 cm (between cassava and the legume) × 30 cm (between the legume rows) at a population of 111,111 plants/ha. Here, dry cassava yield decreased from 17.5 t/ha in pure stand to 15.3 t/ha with cowpea and to 14.1 t/ha with peanut as intercrops, but the decrease was insignificant. Cowpea seed yield significantly decreased from 2.7 t/ha in pure stand to 1.7 t/ha in intercropping. Peanut seed yield significantly decreased from 2.1 t/ha in pure stand to 1.3 t/ha in intercropping (Mason et al. 1986a). In the cassava + soybean system, the differences in cassava yields in pure stand and intercropping were not significant with both narrow and wider spacing (Tsay et al. 1987). In narrow row spacing, cassava was planted in single row spacing at 90 × 90 cm (90 cm between two cassava rows and 90 cm between plants within the row) with 2 rows of soybean planted 30 cm apart. In wide row spacing, cassava was planted at 2.7 m spacing between two cassava rows and 30 cm between plants within the row, with 6 rows of soybean planted 30 cm apart but 60 cm away from the cassava rows. Cassava planted in wide row spacing at 2.7 m × 30 cm had a lower dry storage root yield (average yield of pure stand and intercropping 11.5 t/ha) as compared to that planted at narrow row spacing

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(average yield of pure stand and intercropping 18.0 t/ha). The differences in soybean yields between wide and narrow row spacings were not significant and in both cases soybean yield was 1.4 t/ha. Sinthuprama (1979) studied three planting patterns of mungbean, soybean, and peanut with cassava. Here, cassava was planted at 1.0 × 1.0 m spacing (square method with 10,000 plants/ha). The intercrop (legume) was planted with cassava in 1, 2, and 3 rows at a population of 80,000 plants/ha, 200,000 plants/ha, and 280,000 plants/ha, respectively. In the cassava + mungbean system, the highest grain yield (0.8 t/ha) was achieved with 3 rows of mungbean. Cassava yield was 27.6 t/ha in pure stand and 24.6 t/ha in intercropping (with 3 rows of mungbean) and the difference in cassava yield was insignificant. In the cassava + soybean system, the highest soybean yield (0.7 t/ha) was achieved with 3 rows of soybean, but soybean yields in three populations were not significant. Cassava yield was 32.3 t/ha in pure stand, and 27.8 t/ha in intercropping, and the difference in yield was significant. In the cassava + peanut system, the highest peanut yield (0.75 t/ha) was achieved with 3 rows of peanut, but the peanut yield was not significantly different from the yield with 2 peanut rows. Cassava yield was 30.5 t/ha in pure stand and 27.2 t/ha in intercropping with 3 peanut rows, and the difference in yield was significant. Thus, in soybean and peanut, populations of legumes up to 200,000–280,000 plants/ha can be planted with cassava to obtain the highest productivity of the intercropping system. Thus, in wide paired row spacing, cassava yield is not significantly reduced but the yield of intercrop (legume) may be increased. The more evenly distributed the legumes are within the space available between cassava rows, the greater their yield due to a more complete utilization of available resources along with a low level of intraspecific competition. However, legumes should not be spread too widely within the available space, and placing them too close to the cassava would increase the competition between the two crops. In a cassava + maize intercropping system, cassava yield did not increase due to an increase in cassava plant density, whereas maize yield increased due to an increase in maize plant density. In one study, cassava planted at 8,333 plants/ha (1.0 × 1.2 m) and maize planted at 12,500 plants/ha (2 × 1.2 m) when compared with a more intensive system where cassava was planted at 10,417 plants/ha, and maize at 41,667 plants/ha, no change in cassava yield was observed, but maize production was tripled in the more intensive system (CIAT 1980). In this situation, cassava yield did not decrease at a higher maize density because of differences in spatial arrangement (1.6 × 1.6 m), which minimized intercrop competition by using a vigorous cultivar of cassava at a slightly

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higher plant density. Thus, in the case of the cassava + maize system, use of pure stand density for cassava and maize densities between 20,000 and 40,000 plants/ha is a highly efficient productive intercropping system (Meneses 1980). In one study, cassava yield decreased by 20, 38, and 17% when cassava and maize were grown in the 1:1, 1:2, and 2:2 row arrangements, respectively, as compared to pure stand yield (Olasantan 1988). Here, cassava density was 139,000 plants/ha in pure stand, 7,000 plants/ha in the 1:2 row arrangement (cassava 1 row:maize 2 rows, 50 cm between rows, 100 cm between plants within the cassava row and 60 cm between plants within the maize row), and 11,000 plants/ha in the 1:1 and 2:2 row arrangements (cassava 1 row:maize 1 row or cassava 2 rows:cowpea 2 rows). Maize density was 37,000 plants/ha in pure stand, 24,000 plants/ha in the 1:2 row arrangement, and 16,700 plants/ha in the 1:1 and 2:2 row arrangements. Cassava yield significantly decreased to 12.9, 10.2, and 13.6 t/ha when cassava and maize were planted in the 1:1, 2:2, and 1:2 row arrangements, respectively, as compared to pure stand yield (17.3 t/ha). The 38% reduction in storage root yield of cassava in the 1:2 row arrangement was mainly due to the 50% reduction in its plant density as compared to pure stand density apart from the competition for light and nutrients, especially N. The high population of maize in the 1:2 row arrangement might also have caused initial slow growth of cassava for 1–3 months after planting, thereby delaying storage root formation. The 20 and 17% reduction in storage root yield of cassava in the 1:1 and 2:2 row arrangements, respectively, were due to the 21% reduction in cassava plant density as compared to its pure stand density. On the other hand, maize grain yield was not significantly reduced due to intercropping. Maize plants grown with cassava in the 1:2 row arrangement (cassava 1 row:maize 2 rows) produced a greater yield than those in the 1:1 or 2:2 row arrangements. Intercropped maize grain yield was 2.4, 2.8, and 2.0 t/ha in cassava:maize planted in the 1:1, 1:2, and 2:2 row arrangements, respectively. The 51, 35, and 52% reduction in maize yields in cassava:maize in the 1:1, 1:2, and 2:2 row arrangements were due to the 54, 35, and 54% reduction in maize plant density as compared to pure stand density. The differences in maize yield in different row arrangements were insignificant. Cassava planted in paired rows and intercropped with maize or cowpea had a similar growth rate, dry matter accumulation and partitioning, leaf dry weight, and LAI. Here, cassava was planted in pure stand in single rows at 1.0 m × 80 cm spacing (100 cm between rows and 80 cm between plants within the row), and in paired rows at 60/200 cm × 60 cm spacing (60 cm between 2 subsequent cassava rows, 200 cm

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between 2 such paired rows and 60 cm between plants within the row). In both pure stand and intercropping, cassava was planted at the same density (12,500 plants/ha). No intercrops were planted in single row spacing. Two rows of maize (50,000 plants/ha) were planted between the two adjacent paired rows of cassava, leaving 100 cm spacing between the maize rows and 50 cm between the maize and cassava rows. Cowpea (83,333 plants/ha) was planted in 4 rows between the two adjacent paired rows of cassava, leaving 40 cm space between the cowpea and the cassava plants. Cassava growth rates were similar (average 3.5 g/plant/day) in both single row and paired row spacing in pure stand. In paired row spacing, cassava intercropped with maize or cowpea had a similar but reduced growth rate (2.5 g/plant/day) as compared to pure stand planted in paired rows. Similarly, the dry weight of storage root was higher in pure stand (635.5 g/plant) than in intercropped cassava (427.5 g/plant, average of association with maize and cowpea) both planted in the paired row arrangement (Porto 1990). In the cassava + maize + peanut system, the cassava storage root yield from plants in paired row spacing at 100/550 × 50 cm spacing (100 cm between 2 subsequent cassava rows × 550 cm between 2 cassava paired rows × 50 cm between cassava plants within the row) did not significantly differ from single row planting with wider spacing (25 cm between cassava rows and 50 cm between plants within the row). Here, in both paired row and wide row spacing, the average cassava yield was 33.3 t/ha. However, the intercropped maize grain yield was higher (3.2 t/ha) in paired row spacing than in single row spacing (3.0 t/ha) (Guritno and Sugito 1990). Prabhakar et al. (1982) intercropped cassava with maize and soybean or grain cowpea using three spatial arrangements: single row spacing (100 cm × 100 cm, 100 cm between cassava rows × 100 cm between plants within the row), paired row spacing (65/135 × 100 cm, 65 cm between two subsequent cassava rows making up a pair, 135 cm between two such pairs and 100 cm between plants within the row), and wide row spacing (200 cm × 50 cm, 200 cm between cassava rows × 50 cm between plants within the row). Between 2 rows of cassava, 1 row of maize and 2 rows of cowpea or soybean were sown in single row spacing, while the number of legume rows were doubled in paired row and wide row spacing. Cassava was planted at a density of 10,000 plants/ha in single row spacing and 11,360 plants/ha in paired and wide row spacing in both pure stand and intercrop. The intercropped cassava storage root yield was 22, 22, and 25.1 t/ha with maize, soybean, and cowpea, respectively. Here, the intercropped cassava storage root yield was 22.7, 24.6, and 23.9 t/ha in single row, paired row, and wide row spacing, respectively.

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However, the reduction in storage root yield of intercropped cassava was insignificant as compared to the pure stand yield (26.1 t/ha). The minimal reduction in storage root yield of cassava caused by cowpea was due to its shorter duration as compared to soybean. The differences in storage root yield of cassava among different spatial arrangements were insignificant. Mohankumar and Hrishi (1979) intercropped cassava with maize and legumes at different spatial arrangements. Cassava was planted at normal spacing (90 × 90 cm) and 1 row of maize and 2 rows of a legume were planted in between 2 rows of cassava, or cassava was planted in paired rows at 45/135 × 90 cm spacing (45cm between 2 cassava rows × 135 cm between 2 subsequent cassava rows × 90 cm between plants within the row) and 2 rows of maize and 4 rows of legumes were planted in between 2 paired rows of cassava. In these arrangements, the cassava storage root yields were 18.6, 18.4, 18.4, and 17.2 t/ha in soybean, mungbean, maize, and peanut, respectively, as intercrops, as compared to pure stand yield (21.2 t/ha). The differences in the yield of intercropped cassava were not significant as compared to pure stand yield. D. Nutrient Management 1. Fertilization. A crop’s ability to absorb nutrients is influenced by the type of soil, fertilizer, response of the cultivar, general condition of the crop, cropping pattern, and the availability of nutrients (Howeler 1981; Wargiono 1988). Because of wide variations in climate, soil conditions, and response of the cultivar, no definite quantity of any fertilizer can be prescribed as an optimum requirement, even for the same crop, for all regions. Thus, fertilizer recommendations for specific producing conditions vary because crop response to fertilization depends on the nature of the crop itself, the characteristics of the soil, the climate at the location where it grows, and the management practices employed in growing the crop. Optimum rates of N, P, and K required to produce maximum cassava yields in a pure stand or in an intercropping system, as reported by researchers in various countries, are given in Table 9.2. In general, it is recommended that cassava be fertilized with N, P, and K ratios of 2:1:2 or 2:1:3 (Howeler 2001). However, optimum fertilizer requirements depend on soil fertility, which varies greatly from field to field. Thus, specific fertilizer recommendations should be based on soil analysis results, supplemented with the analysis of the youngest, fully expanded leaf (YFEL) blade taken 3–4 MAP (Howeler 2001). Critical levels for each nutrient in the soil and YFEL blades have been reported (Pushpadas et al. 1976; ICAR 1980; Aiyer and Nair 1985; Nair et al.

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1988; Howeler 2001). According to these findings, medium (normal) soils contain 5–20 µg P, and 0.0015–0.0025 me K per gram. In other words, medium fertile (normal) soils contain 280–560 kg N, 10–25 kg P, and 110–280 kg K in available form, per hectare. The normal YFEL blades of cassava at 3–4 MAP contain 5.0–6.0% N, 0.3–0.5% P, and 1.2–1.9% K. For cassava pure stand, most researchers recommend the full application of P at the time of planting, while N and K should be split at planting, and at 1 MAP or alternatively, all fertilizers should be applied at 1 MAP (Mandal et al. 1971; Mohankumar et al. 1971; Abenoja 1978; CIAT 1978; Zheng Xuequin et al. 1992; Howeler 2001; Li Jun et al. 2001). At the time of planting, 50% of N and K are applied per hectare, while the remaining 50% of N and K are applied to cassava after the harvest of the intercrops (Prabhakar et al. 1983). Application of organic manure (farm yard manure, FYM) in combination with chemical fertilizers improves soil fertility and yield. In Vietnam, 5–10 tonnes of pig manure is recommended per hectare. In the Philippines, 10 tonnes of poultry manure is recommended per hectare. In India, 12.5 tonnes of cattle manure is recommended per hectare (Mohankumar et al. 1976; Pillai et al. 1985; Howeler 2001). Cassava yields will decline when the crop is grown continuously on the same land without adequate fertilizer inputs, especially K and N (Chan 1980; Kabeerathumma 1990; Tongglum et al. 2001; Nguyen Huu Hy et al. 2001; Wargiono et al. 2001; Li Jun et al. 2001). If no fertilizers were applied annually, cassava yields of 25 t/ha during the first year decreased to 5 t/ha in the 8th year (Wargiono et al. 2001). This is because the amount of nutrients removed from the soil by cassava is high when yields are high or when stems and leaves are also removed from the field (CTCRI 1983a; Wichmann 1992; Howeler 2001). Cassava removes 60–242 kg N, 13–40 kg P, and 50–187 kg K from one hectare of land to produce storage root yields of 15–30 t/ha (Kanapathy 1974; CTCRI 1983a,b; Roy and Braun 1983; Mohankumar and Nair 1996; Nayar et al. 1986; Gosh 1987; Nguyen Huu Hy et al. 2001; Howeler 1978, 2001). Thus, cassava removes a large amount of N and K but only lesser amounts of P from the soil. The nutrient removal by cassava is influenced by factors such as cultivar, fertilizers applied, water management, and the cropping system. An increase in the amount of fertilizers and irrigation (high soil moisture) increases nutrient uptake (Nayar et al. 1986). In soils with low amounts of available P, cassava benefits greatly from mycorrhizal association for the absorption of P (Howeler 1981). Applying organic matter annually or every two years improved both soil fertility and physical conditions, increased fertilizer use efficiency, and maintained cassava yields of 20 t/ha (Wargiono et al. 2001). The annual incorporation of cassava tops after harvest, especially in the absence of

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Table 9.2. Fertilizers applied for cassava production (pure stands except where noted) in various locations. Location

Condition

China

N:P:K (kg/ha)

Reference

50:22:83

Tian Yinong et al. 1995 Li Jun et al. 2001

100–200:22–43:83–166 India

Acid, laterite soils

100:22:83

Rainfed conditions Irrigated conditions

50:28:104 60:39:125

Susan Jhon et al. 1998 Ranganathan 2000 Ranganathan 2000

Indonesia

Monocropping Intercropping

60-90:11–17:37–50 90–180:22–39:75–149

Wargiono et al. 2001 Wargiono et al. 2001

Malaysia

Mineral soils Peat soils

60:13:133 50:13:33

Chan 1980 Tan 2001

High K soils

60:13:25 100–120:22–26:83–100 60:39:50 60:13:25

Abenoja 1978 Evangelio et al. 1995 Evangelio 2001 Evangelio and Ladera 1998

Sandy loam entisols

50:0–22:42–83

Sandy loam ultisols

80:0–13:25–42

Low P, K soils Low P, high K soils High P, low K soils High P, high K soils Most cassava soils Tops incorporated

126:31:57 84:12:29 0:0:58 119:5:0 100:22:83 50:22:42

Ho and Sittibusaya 1984 Ho and Sittibusaya 1984 Sittibusaya 1993 Sittibusaya 1993 Sittibusaya 1993 Sittibusaya 1993 Sittibusaya et al. 1995 Tongglum et al. 2001

Most cassava soils

80:17:66 to 160:34:69

Central region

100:43:125

Coastal region

70-120:22:83

Southeastern region

120:52:149

Peat soils

80:17:16

Philippines

Thailand

Vietnam

Nguyen Huu Hy et al. 1998 Nguyen Thanh Thuy 1999 Nguyen Thanh Thuy 1999 Nguyen Huu Hy et al. 2001 Nguyen Hong Linh 1999

chemical fertilizers, markedly increased cassava yields (Tongglum et al. 2001). Intercropped legumes (peanut, soybean, mungbean) had no adverse effect on soil productivity, and the yield of a cassava pure stand planted without fertilizers at every 5th year was not affected over the period of

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15 years (Tongglum et al. 1987). The long-term cassava intercropping resulted in an increase in the soil organic matter by the incorporation of the residues of the intercrops (Tongglum et al. 1987; Nguyen Huu Hy et al. 2001). A legume crop leaves a residual effect equivalent to a fertilizer application of 15–50 kg N/ha (Reddy et al. 1983; Roy and Braun 1983). Thus, crop residues of cowpea, soybean, and peanut incorporated into the soil increases soil fertility, particularly N, and cassava yields (Molina 1983; Miramble 1983; Castroverde 1983; Ratilla 1983; Quirol and Amora 1987). Intercropping is also considered advantageous due to the effect it has on nutrient uptake. In various associations of cassava with other crops, absorption of soil nutrients by the crops is greater than the loss of nutrients through leaching and erosion, whereas in a cassava pure stand, the potential for nutrient loss through leaching and erosion is several times greater than what may be utilized by the crop. When cassava is intercropped, the demand for nutrients is intensified, particularly when each associate crop is planted at its normal pure stand density. In this situation, the removal of nutrients from the soil is potentially greater in the intercropping system. If these nutrients are not replaced by adequate fertilization, soil fertility deterioration occurs (Leihner 1983). A significant increase in the storage root yield of cassava as well as the yield of the intercrop was recorded when both the crops were fertilized as per the fertilizer requirements for pure stand, determined on the basis of response to applied fertilizers (Mohankumar and Hrishi 1973). Under tropical soil conditions, at different amounts of fertilizers applied, the cassava storage root yield decreased by 7–24% due to intercropping with peanut or cowpea or French bean, as compared to pure stand yield (Mohankumar and Ravindran 1991). The reduction in cassava yield was higher (19.3 t/ha) in plots that received fertilizers recommended for cassava alone than in plots that received fertilizers recommended for both cassava and the intercrop (20.7 t/ha) as compared to pure stand yield (24.4 t/ha). In the yam + maize + cassava mixture, application of fertilizers (120 kg N, 52 kg P, and 100 kg K) increased yields of component crops as compared to yields in an unfertilized field. Here, the yields in yam, maize, and cassava were 3.6, 1.9, and 12.0 t/ha, respectively, in an unfertilized field. Application of fertilizers increased the yam, maize, and cassava yields to 4.5, 3.2, 16.5 t/ha, respectively (Ikeorgu and Odurukwe 1994). In India, depending on the cultivar, cassava yields are highest with the application of 75–150 kg N (Mandal et al. 1971b; Mohankumar and Hrishi 1973; Saraswat and Chettiar 1976; Nair 1982), 19.4–43 kg P (Vijayan and Aiyer 1969; Nair and Rajendran 1973; Nair et al. 1988), and

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77.2–166 kg K (Mandal and Mohankumar 1969; Mohankumar et al. 1971; Rajendran et al. 1976; Ashokan and Sreedharan 1977; Nair et al. 1980; Nair and Aiyer 1985; Nayar and Sadanandan 1985). At these rates of fertilizer application, cassava yields are maximized in a pure stand as well as in an intercrop with legumes (Cock et al. 1979; Prabhakar et al. 1983; Bridgit et al. 1985; Anilkumar et al. 1991). In a pure stand cowpea crop, the highest grain yields are obtained with a fertilizer application in the range of 10–25 kg N, 7–32 kg P, and 8–62 kg K per hectare (Prabhakar et al. 1983; Srivastava 2001). Fodder cowpea requires 25 kg N, 25.8 kg P, and 24.9 kg K per hectare (Anilkumar et al. 1991). Cowpea removes 85 kg N, 7 kg P, and 25 kg K per hectare of land to produce a grain yield of 1.5 tonnes (Roy and Braun 1983). Peanut cultivars require 10–30 kg N, 4–26 kg P, and 17–37 kg K per hectare to produce the highest yield of pod (Prabhakar et al. 1983; Soedomo and Soegiyanto 1983; Yakadri et al. 1992; Gnanamurthy and Balasubramaniyan 1992; Bhalerao et al. 1993; Singh et al. 1994; Patra et al. 1995; Samui and Ahasan 1997). Peanut removes 49–121 kg N, 5–19 kg P, and 27–37 kg K per hectare of land to produce a pod yield of 1–1.9 tonnes (ICAR 1980; Roy and Braun 1983; Tandon and Messick 2001). Peanut yields are maximized when N and K are applied as basal (at the time of sowing), and at 60 and 90 DAP. Pigeonpea cultivars require 20–30 kg N, 17–32 kg P, and no K per hectare to produce the highest yield of seed (Chatterjee and Bhattacharyya 1986; Padmalatha and Rao 1993; Sarvaiya et al. 1993). Pigeonpea removes 32–85 kg N, 8–10 kg P, and 11–16 kg K per hectare of land to produce a seed yield of 1.2–1.8 tonnes (Roy and Braun 1983; Tandon and Messick 2001). Soybean cultivars produce the highest seed yield with fertilizers applied in the range of 11–85 kg N, 24–44 kg P, and 45–83 K per hectare (Ghorashy et al. 1972; Herbert and Litchfield 1984; Willcott et al. 1984; Gardner and Auma 1989; Khelkar et al. 1991; Majumdar and Behera 1991). Soybean removes 49–125 kg N, 7–43 kg P, and 21–101 kg K per hectare of land to produce a seed yield of 1.2–1.8 tonnes (Roy and Braun 1983; Tandon and Messick 2001). Maize cultivars produce the highest grain yield with fertilizers applied in the range of 60–225 kg N, 26–35 kg P, and 33–60 kg K (Mukeshkumar et al. 1992; Mongia 1992; Sinha and Umar 1972; Edmeades and Lafitte 1993; Mishra 1993; Paradkar and Sharma 1993; Olasantan et al. 1994; Lal and Singh 1998). Maize removes 36–200 kg N, 9–34 kg P, and 32–130 kg K per hectare of land to produce a grain yield of 2–7 tonnes (ICAR 1980; Roy and Braun 1983; Tandon and Messick 2001). Rice cultivars produce the highest grain yield with the application of 40–240 kg N, 10–29 kg P, and 17–25 kg K per hectare (Rao 1985ab). Here, the time of N application depends on the cultivar, soil

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conditions, rainfall, and duration of the crop. In general, it is beneficial to apply N over 2–4 time periods, particularly for long-duration cultivars, heavy rainfall seasons, and for light, sandy loam soils. For heavy, clayey soils (soils containing more than 40% clay), N may be applied at one time at the time of planting or 50% at the time of planting and 50% at 1 MAP. Rice removes 42–64 kg N, 8–12 kg P, and 56–67 kg K per hectare of land to produce a grain yield of 1.5–3 tonnes (ICAR 1980; Roy and Braun 1983; Tandon and Messick 2001). French bean requires 20–40 kg N, 13–26 kg P, and 33–42 kg K per hectare (Prabhakar and Nair 1988; Ashok Kumar 2001). Grain legumes have the capacity to fix atmospheric N through nitrogenfixing symbiotic bacteria in nodules they produce, thus they can partially or fully satisfy their N requirement. For example, cowpea can fix 73–240 kg N/ha annually through Rhizobium (Nutman 1971), and pigeonpea can fix up to 69 kg N/ha per season (Rao et al. 1981). Thus, leguminous crops require a limited amount of inorganic N. Application of an excess amount of inorganic N substantially reduces the yield of legumes because, first, N concentration of more than 25–50 ppm in the soil decreases nodulation and the nitrogenase activity of Rhizobium in the nodules of legumes, and hence reduces N fixation (Dart 1974; Lie 1974; Latimore et al. 1977; Quilt and Dalal 1979; Rao et al. 1981). Second, legumes utilize the excess N for vegetative growth, leading to a decrease in dry matter partitioning to pod growth (Summerfield et al. 1977). Seed inoculation with Rhizobium at the time of sowing led to a 9.8–40.8% increased pod yield in peanut (Iswaran and Sen 1971; Bajpai et al. 1974; Nambiar et al. 1982; Kulkarni et al. 1984), 27.6–80.6% seed yield in soybean (Saxena et al. 1971; Chatterjee et al. 1972; Ghorashy et al. 1972; Gulati 1989), 57–78.6% grain yield in cowpea (Summerfield et al. 1976, 1977), and 12–25% grain yield in pigeonpea (Quilt and Dalal 1979), compared to the non-inoculated plants. In peanut and soybean, application of Ca and S substantially increases yield (Chatterjee et al. 1972; Bahl et al. 1986; Agasimani et al. 1992; Adams et al. 1993; Tandon and Messick 2001). Application of gypsum (90% CaSO4⋅2H2O, 500 kg/ha), or S (40 kg/ha), or calcium oxide (CaO, 250 kg/ha) at the pegging stage substantially increased the pod yield in peanut (Agasimani et al. 1992; Patra et al. 1995). The fertilizer application method to be practiced in intercropping system, as is the case with pure stand, is determined by soil characteristics, precipitation, type of fertilizer, and crops grown (Leihner 1983). In a sandy soil, broadcast application exposes the fertilizer to more loss through leaching than does the band application. In acid soil, Fe and Al precipitate, adsorb P, and form insoluble iron and aluminum phos-

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phates, and in alkaline soil, calcium precipitates and adsorbs P and forms low soluble tri-calcium phosphates, rendering P unavailable to the crop (Donahue et al. 1983). The crops use fertilizers with high nutrient concentration and solubility more efficiently when band applied. A cassava crop grown on ridges during the rainy season yields maximally when one-half of the fertilizer is broadcasted and the other half is applied in bands. Conversely, in dry season plantings on flat land, cassava yields the best when the fertilizer is broadcasted (Howeler 1981). Annual crops such as grain legumes or maize have deep and finely branched root systems. Conversely, cassava has a rather sparse root system with a small number of root hairs. This means that the absorption efficiency of both cassava and its intercrops could be similar in spite of morphological differences in the root system. Therefore, the mode of fertilizer application in intercropping systems with cassava may be determined more by the soil, climatic conditions, and the type of fertilizer to be applied than by the absorption characteristics of the crops (Leihner 1983). In acid P fixing soils, cowpea responds slightly better to band application than to broadcasting P when triple superphosphate, a highly soluble form of P, is used (CIAT 1980). Cassava, however, does not respond differently to broadcasting or band application. Cowpea yield does not differ significantly when N in the soluble form of urea is applied in bands or broadcast. On the other hand, cassava responds better to broadcast application of N and this could be related to a better uptake of N by the sparse cassava root system when N is broadcasted rather than band applied. When K was applied as KCl, neither cassava nor cowpea showed a different response to the two methods of application. 2. Nutrient Competition. The competition for nutrients in intercropping systems occurs when the absorption zones of two or more plants overlap. This overlapping is more frequent and occurs sooner when competition is for the mobile nutrients, because these nutrients move more readily through the soil. Thus, the zone of depletion around the roots increases in size fast, and overlaps sooner. Differences in nutritional requirements and in absorption efficiency are causes of competition between the component crops in an intercrop system. Competition for one nutrient at the same time may alter the ability of the component crops to compete for other nutrients. Usually, root systems of different crops do not interfere with each other in intercropping systems, possibly due to root antagonism and the tendency of the growing root to avoid moisture depleted zones. This helps to avoid competition for the more immobile nutrients, but, at the same time, restricts the soil volume

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explored by the roots. The stratification of the root systems, that is, expansion of roots of different crops to different soil depths, can help to reduce competition for nutrients. In the case of the cassava + cowpea system (CIAT 1980), the response of cassava to N, as compared to its response as a pure stand, shows that cassava suffered from competition for this nutrient. Conversely, the absence of a negative response of cowpea to N, and the legume’s minimal difference in grain yield when grown as a pure stand or intercropped suggests that cowpea does not suffer from competition for N by cassava. This is presumably due to its ability to fix atmospheric N, and the rapid root expansion both in width and depth, which might have enabled cowpea to take up N from the soil levels to which cassava roots did not reach (Leihner 1983). Similarly, the yield increase of intercropped cassava at higher levels of K suggests that this nutrient might have been limiting in the association at low levels of applied K, and the competition is corrected by increased K levels. Both cassava and cowpea compete for P fertilizer applied in soils of very low P and high P fixing capacity (CIAT 1980). The specific response of cassava in association with cowpea is due to the differences in the tolerance of the two crops to low available soil P. With a small amount of P added, cassava shows a positive yield response. However, this response is not distinct at higher P fertilization when cowpea becomes more competitive for N, P, and K, causing a reduction in cassava yield. On the other hand, cowpea shows the highest grain yield with the highest P applied (Leihner 1983). In one study, when cassava, and an intercrop such as cowpea or peanut or urd bean (Vigna mungo) or mungbean were planted on raised beds between cassava rows, the vegetative growth and storage root yield of intercropped cassava was similar to that of pure stand cassava (Ashokan et al. 1985). Here, because of a non-competitive co-existence of cassava and legumes, even when the intercrops are not fertilized, the yield of intercropped cassava did not decrease. In this situation, the root system of leguminous crops may use the nutrients washed down from the raised beds and those that are present in the deeper layers. In one study, the N, P, and K requirement was greater for a cassava + peanut system than for a cassava + cowpea system. Here, the highest storage root yield was found in cassava + cowpea plots that received 50 kg N, 26.9 kg P, and 51.9 kg K per hectare, whereas the highest storage root yield was found in cassava + peanut plots that received 93.8 kg N, 32.2 kg P, and 77.9 kg K per hectare (Sheela and Mohamed Kunju 1988). The higher quantity of fertilizer application to the cassava + peanut system was because peanut tends to uptake more nutrients than cowpea. The N, P, and K uptake by peanut was 78.4, 6.3, and 33.5 kg/ha, respectively, and cow-

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pea uptakes were 44.0, 5.9, and 15.7 kg/ha, respectively, in association with cassava (Mohankumar and Nair 1996), and also because of the longer crop duration and greater biomass production in peanut than in cowpea. Tissue analysis indicates the correct nutritional status of the crop. Although nutrient concentration in a plant varies with different parts of the plant and the stage of growth, the metabolically active leaf reflects the correct nutritional status of the plant. Thus, the identification of the proper leaf, and the correct stage of growth of the plant to be sampled are of great importance in foliar diagnosis to determine the nutritional status of the plant. Through tissue analysis, it is possible to determine whether a crop suffers more nutrient competition in association than in pure stand (Leihner 1983). Tissue analysis of petioles and leaves of cassava and cowpea revealed that cowpea competes for N and K with cassava, whereas cowpea itself is not affected by competition for these two nutrients (CIAT 1980). On the other hand, P concentration in both cassava and cowpea tissue decreased in the intercrop system, which indicates that both crops compete strongly for P, apparently affecting cassava more than cowpea. The fact that at higher P levels, foliar P concentration in intercropped cowpea increases, while it does not increase in intercropped cassava, suggests that as P levels increase, cowpea becomes a stronger competitor, leaving less P for uptake by cassava. Thus, in a cassava + cowpea system, P application had little effect on cassava yield. However, increasing P application from 0 to 22 kg/ha increased cowpea yield by 48%. The P content of cassava and cowpea leaves increases with an increase in P application (Mason and Leihner 1988). Thus, cassava is a crop well adapted to low P soils and very competitive even without P application, whereas cowpea in the same soil requires the addition of P for adequate growth and yield. High productivity and a good competitive balance between the two crops are reached with 22 kg P per hectare, demonstrating the great potential of the cassava + cowpea system on infertile acid soils. A cassava + mungbean (Vigna radiata) system removes twice as much N and P and more K, Mg, and S compared to a cassava pure stand (Leihner 1983). Intercropping cassava with cowpea decreases P and N in cassava stems, leaves, and storage roots when compared to pure stand cassava at 50 DAP, but it does not influence the N, P, and K of cassava at a later period or cowpea at any period of growth (Mason et al. 1986c). Similar results occurred when cassava was intercropped with peanut, although peanut is a less vigorous competitor with cassava for P than cowpea. The cassava + cowpea and cassava + peanut systems remove

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more N, P, and K than the pure stand cassava crop. Thus, intercropping systems remove more nutrients than pure stands, which emphasizes the need for higher rates of fertilizer application to the intercropping systems. In a cassava + soybean system, the total dry matter of cassava decreased below that of pure stand cassava regardless of the time of N application (Tsay et al. 1989). Nitrogen applied at the time of planting significantly enhanced total dry matter in cassava both in pure stand and in intercropping with soybean. Application of N at the time of planting resulted in a higher harvest index (HI) in intercropped than in pure stand cassava, while the storage root yield remained similar in the two crops. Nitrogen content in leaves of the intercropped cassava was lower than that of the pure stand cassava, indicating the adverse effect of intercropping on growth of cassava through N deficiency. In intercropping, the N content of soybean remains greater than that of cassava, indicating that the intercropped soybean competes with cassava for N and reduces the N available to cassava. Thus, the competition for N is a major factor that reduces growth of intercropped cassava before soybean is harvested (Tsay et al. 1989). The advantage of intercropping cassava with quick-maturing soybean is reduced when the N supply is low. Therefore, in areas with low soil fertility, cassava storage root yield may be adversely affected by intercropping with soybean if N-containing fertilizer is not applied. 3. Problem Soils. To obtain good yields on poor soils that have features such as nutrient deficiency, acidity, and Al, Fe, and Mg toxicity, crops that adapt well to unfavorable conditions should be selected. These crops should produce reasonable yields with minimal inputs. About 2.54 × 109 ha, out of a total land area of 4.95 × 109 ha situated between the Tropic of Cancer and the Tropic of Capricon, are moderately to strongly acid soils, and are the major soils used for cassava production (Engelstad and Russel 1975; Edwards and Kang 1978). Cassava is well adapted to extremely infertile acid soils and yields considerably when most other crops would either fail or give very poor yields (Rogers and Appan 1972; Cock and Howler 1978; Edwards and Kang 1978). Cassava cultivars are capable of growing on acid soils ranging in pH between 3.7 and 5.0 (Rogers 1965; Chew 1970; Spain et al. 1975; Edwards and Kang 1978). In acid soils with pH 4.0, storage root yields up to 79–84% of maximum yields were obtained at moderate rates (1.0–1.6 t/ha) of lime application (Edwards and Kang 1978). In acid soils, high aluminum (Al) can drastically reduce plant growth and storage root yields for most cassava cultivars (Howeler 1985). However, some cassava cultivars tolerate high aluminum toxicity (up to 80% soil saturation) with no

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decrease in storage root yield (CIAT 1978; Howeler 1981; Manrique 1985). The effects of Al on plant growth and root yield are (1) a triggering of leaf drop and the stunting of plant canopy regeneration, and (2) a halting of DM partitioning to storage roots (Manrique 1985). The relation between soil Al toxicity and storage root yields also appears to depend on branching habit, and the storage root yield drastically decreased in cultivars with early branching habit with increasing soil Al content (Manrique 1985). Thus, for acid soils with Al toxicity, Al-tolerant cultivars in combination with soil amendments sustain cassava yield. In acid soils, the cassava storage root yield is also limited by phosphorus (P) deficiency (Howeler 1985), and application of P up to 100 kg/ha for 2 consecutive years improved cassava yield (Pellet and El-Sharkawy 1993, 1997). However, the response of cassava to P application gradually declined in subsequent years because application of P to acid soils with low P for 4–5 years resulted in a build up of P up to 87.4–399 kg/ha (Pillai et al. 1985; Nair et al. 1988). Cowpea, peanut, and maize are tolerant to acidic, infertile soil conditions, whereas mungbean, soybean, and winged bean (Psophocarpus tetragonolobus) do not tolerate extreme soil acidity (Hegewald and Leihner 1980; Oplinger et al. 1990). In acidic soils (pH 5.0), maize, soybean, and cowpea yields were reduced to 73, 60, and 42%, respectively, of their highest yields obtained at soil pH 6.8 (Thompson 1957). The soybean yield on unlimed soils with high Al saturation averaged 70% of that obtained on limed soils (Dunphy and Schmitt 1981). In extremely acid soils (pH less than 5), yields of cassava, French bean, maize, cowpea, soybean, and rice increased with the application of lime (CaCO3, 1.0–2.0 t/ha) (Chatterjee et al. 1972; Cock and Howeler 1978; Edwards and Kang 1978; Mohankumar and Nair 1980; Patiram 1996). This is because lime raises soil pH, increases the available N through the decomposition of soil organic matter by increasing the activity of microoraganisms, increases available P, eliminates Al toxicity, and causes many other favorable effects (Donahue et al. 1983). The exact quantity of lime required depends on both the pH requirement of the crop to be grown, and the pH and cation exchange capacity of the soil. After 5 years of lime application, N may become the most important limiting factor in the growth of non-legumes. Therefore, an adequate quantity of organic matter has to be applied to maintain soil fertility. However, in many countries, lime is costly and difficult to obtain. Further, where topsoil liming is practiced, the residual effects of subsoil Al may continue to limit yield potential (Hammel et al. 1985). Calcareous soil (soil with 1.5–32.4% CaCO3) with high pH (pH more than 8.0) exhibit P, Mn, Fe, and Zn deficiencies. Excessive CaCO3 in the

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soil causes the transformation of available phosphorus to di(2CaHPO4⋅2H2O) and tricalcium phosphates (Ca3(PO4)2), and transformation of Fe++ to insoluble ferric hydroxide or ferric oxide, reducing the availability of P and Fe (Singh and Dahiya 1976). This soil has less than 4.5 ppm Fe and 0.6 ppm Zn (Pillai and Mohankumar 1994). Plants growing in this soil exhibit chlorosis because of lime-induced Fe deficiency, caused by the reduction in iron uptake, the iron inactivation in tissues, or the prevention of iron transport and utilization. Foliar application of 1.0% ZnSO4 and 1.5–2.0% Fe2SO4 can improve cassava yields in this soil. Alternatively, cultivars tolerant of Zn and Fe deficiency can be grown (Muthuswamy and Narayanan 1983; CIAT 1984; Pillai 1990). 4. Green Manuring. Green manuring means growing a quick-growing crop and then ploughing it under to incorporate it into the soil. A green manure crop supplies organic matter as well as additional N, particularly if it is a legume crop. A leguminous crop producing 8–25 t/ha of green matter will add about 60–90 kg N when ploughed under the soil (ICAR 1980). Green manure can improve the physical characteristics of the soil, maintain soil fertility, increase fertilizer use efficiency, and thus can improve soil production capacity (Wargiono et al. 1995; Nguyen The Dang et al. 1998). Green manures such as cowpea and sunhemp (Crotolaria juncea), planted during the early rainy season and incorporated into the soil 60 DAP before planting cassava, increased cassava yield by 32.8–66% and 13.7–114%, respectively (Paisarncharoen et al. 1990; Tongglum et al. 1992). Cowpea has been found to be a superior green manure for the acid, infertile soils that are low in organic matter (CIAT 1975; Sasidhar and Sadanandan 1976; Mohankumar and Nair 1990; Nayar and Potty 1996). By 60 DAP, cowpea pods can be harvested for vegetable purposes, and the haulms can be incorporated into the soil as green manure prior to planting cassava. Green manuring with cowpea improves the N content of soil by adding 25–50 kg N, and enhances the biomass productivity and storage root yield of cassava (Mohankumar and Nair 1990; Sasidhar and Sadanandan 1976; Nayar and Potty 1996). The cowpea green matter incorporated was estimated to be 20–25 t/ha, and cassava was planted without adding FYM (Mohankumar and Nair 1990). Thus, use of green manure replaces FYM in the cultivation of cassava, and can substantially reduce the cost of inputs (Chen Shiping 1983; Prabhakar and Nair 1987). Howeler (1993) reported that normal planting of cassava in the early rainy season, without green manure, resulted in higher yields even without fertilizers, because cassava benefits from an additional 2–3 months of rainy season. If a green manure crop is ever to be established, these rainy months would be used for

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growing the green manure. However, in areas with a longer rainy season, growing and incorporation of green manure with soil may be beneficial in improving cassava yield. Alternatively, the green manure crops can be sown 1–2 months prior to cassava, and after harvesting green manure and ploughing under the soil, cultivars that mature early (7 months) can also be planted. Although there are substantial advantages to be derived from green manuring, most farmers in Asia opt for the use of animal manures or chemical fertilizers because, first, they cannot afford to use their limited land for an unproductive green manure crop (Howeler 2001), and second, cassava responded faster to chemical fertilizers than to manures and green manures (Dinh Ngoc Land and Nguyen The Dang 2000; Howeler 2001). E. Weed Control In a cassava pure stand, because the crop has slow initial growth and requires wide spacing to accommodate later growth, the space not covered by the crop canopy during its early growth (1–4 months) provides a location for weeds to flourish. Supression of weed growth during the storage root initiation period is an important requirement for cassava production (Kasasian and Seeyava 1969; Tongglum et al. 2001). But, once a canopy ground cover is attained, further weeding is no longer necessary (Onochie 1975). Without effective weed control, the use of other improved cultural practices will generally lead to low yields. Cassava storage root yield losses due to weeds range from 25 to 100% (Doll and Piedrahita 1976; Akobundu 1980; Hahn and Keyser 1985; Ambe et al. 1992) in pure stands. Weed control is traditionally done by hand weeding. The number of weedings necessary for cassava varies considerably, depending on the weed population, soil fertility, rainfall, cropping system, and the response of a particular cultivar to competition from weeds. One to six hand weedings resulted in the highest storage root yield (Onochie 1975; Doll and Piedrahita 1976; Godfrey-Sam-Aggrey 1978; Ambe et al. 1992). About 45–50% of the time a farmer spends (Doll et al. 1977; CIAT 1976) or 25–55% of total labor input in cassava production is devoted to weeding (Krochmal 1966; Onochie 1975; Doll et al. 1977; Sinthuprama and Tiraporn 1984; Hahn and Keyser 1985). The use of herbicides by farmers is increasing in areas with limited availability and high cost of labor. Several herbicides have been found to be effective in controlling weeds in cassava, which reduces labor input (Krochmal 1966; Doll and Piedrahita 1976). Pre-emergence application of oxyflourfen (0.5 kg/ha) with alachlor (1.4 kg/ha) (CIAT 1980), or primextra (atrazine + metolachlor) (2.5 kg/ha) (IITA 1980), metolachlor

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(1.6 kg/ha) (Tirawatsakul et al. 1988), a mixture of paraquat + diuron (3.5 l/ha) at 30 DAP (Bangun 1990), a mixture of 2 liters alachlor + 2 kg fluometuron/ha, followed by post-emergence hand weeding or a spray of 2 liters/ha of paraquat (Tan 1988) controlled weeds and increased storage root yield in cassava pure stand. Thus, the integration of chemical and manual weed control measures reduces labor requirements, eliminates early weed competition, and enhances yields. In an intercropping system, a better soil coverage is obtained from the beginning. This decreases light penetration to the soil surface and reduces weed growth. Thus, growing an intercrop, that rapidly covers the soil without competing excessively with cassava, can offer great scope for weed control. In one study, intercropping common bean with cassava reduced the total weed dry weight to 30–33% of the amount observed in the cassava pure stand between 45 and 135 DAP (CIAT 1978, 1980; Leihner 1983). Only at 180 DAP, the amount of weeds were found equal under cassava pure stand and the cassava + French bean system. When intercropped, cassava yield was the same under conditions either with or without weed control measures. However, in pure stand, cassava suffered a yield reduction of 30% under similar conditions. The cost of weeding can be reduced by about 50% by growing cowpea as an intercrop with cassava (Ashokan et al. 1985). Several pre-emergence herbicides can be used along with manual weeding in cassava-based intercropping systems with legumes and nonlegumes. In peanut, 2 or 3 hoeings between rows at an interval of 15 days, or hoeing and weeding up to 3 weeks after sowing, or preemergence application of oxadiazon (1.0 kg/ha), fluchloralin (0.75–1.5 kg/ha), metolachlor (1.0 kg/ha), pendimethalin (1.0–1.5 kg/ha), butachlor (0.75 kg/ha) with one hand weeding at 30 DAS or trifluralin (40%, 2.0 l/ha) control weeds, resulting in the highest pod yield (Bell et al. 1987; Mishra et al. 1991; Nimje 1992; Mohanty et al. 1997; Patel et al. 1997; Gnanamurthy and Balasubramaniyan 1998). In pigeonpea, crop yield losses due to weeds have been estimated to be as high as 90% in pure stand (Saxena and Yadav 1975). In pigeonpea planted under rainfed conditions, weeds can be controlled by 1 or 2 hand weedings between 20 and 45 days after planting. Pre-emergence application of fluchloralin (1.0–1.5 kg/ha), pendimethalin (1.5 kg/ha), alachlor (0.5–2 kg/ha), metalachlor (0.5 kg/ha), ametrin, prometrin (1.0–2.2 kg/ha), prometone (1.1–4.5 kg/ha), diphenamide (2.2–9.0 kg/ha), chloroxuron (1.7 kg/ha), and nitrofen (1 kg/ha) reduces weed growth, resulting in the highest seed yield (Kasasian 1964; Hammerton 1972; Jurgens 1972; Abrams and Julia 1974; Saxena and Yadav 1975; Singh and

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Faroda 1977; Prasad et al. 1985; Ahlawat and Venkateswarlu 1987; Goyal et al. 1991; Maheshwarappa and Nanjappa 1994; Rajput and Pandey 1994; Sharma et al. 1994; Singh et al. 1998). In soybean, the pre-emergence application of herbicides controls weeds. Pre-emergence application of alachlor (1.7–2.5 kg/ha), oxadiazon (1.0 kg/ha), oxyfluorfen (0.25 kg/ha), clomozon (1.5 kg/ha), linuron (0.85 kg/ha), fluchloralin (1.0 kg/ha), trifluralin (0.56 kg/ha), alachlor (3.3 kg/ha) in combination with metribuzin (0.6 kg/ha), a mixture of imazaquin (0.75 kg/ha) + pendimethalin (1.25 kg/ha), post-emergence application of a mixture of sethoxydim (0.37 kg/ha) + imazethapyr (0.1 kg/ha), and a mixture of fluazifop (0.25 kg/ha) + imazethapyr (0.1kg/ha) controls weeds, resulting in the highest seed yield (Singh and Mani 1976; Herbert and Litchfield 1984; Willcott et al. 1984; Porwal et al. 1990; Buhler et al. 1992; Jain and Tiwari 1992; Tavav et al. 1995; Dubey 1998; Joshi and Billore 1998). If herbicides are not used, one to three manual weedings during the initial 30–45 days can control weeds. In mungbean, weed can be controlled by both mechanical and chemical means. The methods recommended are either two hand weedings at 15 and 30 DAS or the use of herbicides. Recommended pre-emergence herbicides are alachlor or metolachlor 1.5–2.2 kg/ha. Post-emergence herbicides fluazifop-butyl (150g) + fomesafen (125g)/ha are sprayed at the 3–4 leaf growth stage of weeds (Jai-Jit Su-Jit 1994). In maize, the initial 20–40 days after sowing are most critical for weed removal because keeping the field weedy up to 40 DAS reduced grain yield by 43.8% compared to the weed-free conditions. Weeding at 40 DAS removed weeds to almost 50%, and reduced weed dry matter yield up to 57% compared to weedy plot (Varshney 1991). Pre-emergence application of metolachlor (1.5 kg/ha) with atrazine (0.75 kg/ha), atrazine (0.5–1.0 kg/ha), glyphosate (1.0 kg) in combination with 2,4-D sodium salt, cyanazine (1.8 kg/ha), and alachlor (2.2 kg/ha) controls weed growth, resulting in the highest grain yield (Balyan and Bhan 1987; HashemiDezfouli and Herbert 1992; Olasantan et al. 1994; Sreenivas and Satyanarayana 1994; Sharma et al. 1998). Maize is slightly susceptible to 2,4-D if it is used on very hot days with high soil moisture content. At this time the rate of 2,4-D (2,4-dichlorophenoxy acetic acid) may be reduced (Thakur 1979). Pre-emergence application of alachlor (2.5 kg/ha) in combination with diuron (3.75 kg/ha), and fluometuron (3.0) also effectively controlled weeds in a cassava + maize system (Enyinnia et al. 1983). In rice, under upland conditions, application of thiobencarb and butachlor (1.5 kg/ha) reduces weed growth, resulting in the highest grain yield (Gogoi and Sarma 1991). In semi-arid rice, pre-emergence application of pendimethalin (1.25 kg/ha) followed by post-emergence

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application of 2,4-D sodium salt (1.0 kg/ha), pre-emergence application of oxyfluorfen (0.15 kg/ha) with one hand weeding at 25 DAS, and butachlor (1.5 kg/ha) with one hand weeding reduce the weed growth, resulting in the highest grain yield (Ramiah and Muthukrishnan 1992; Ramamoorthy et al. 1998). Lowland conditions favor the growth of aquatic and semi-aquatic weeds. Grassy weeds compete aggressively with the rice crop for water and nutrients. In transplanted rice (lowland conditions), post-emergence application of herbicides reduced weed growth and resulted in better growth and biomass production, and higher grain yield compared to pre-emergence application. Post-emergence application of 2,4-D (0.5 kg/ha) in combination with butachlor (0.5– 1.5 kg/ha), pretilachlor (1.0 kg/ha) in combination with piperophos (1.25 kg/ha), tridipane (0.48 kg/ha), anilophos (0.4–0.6 kg/ha), oxadiazon (0.4 kg/ha), thiabencarb (0.4 kg/ha) in combination with 2,4-D sodium salt, pyrazosulfuron ethyl (5 g/ha) in combination with oxadiazon (0.4 kg/ha), pyrazosulfuron ethyl (10 g/ha), butachlor (1.25 kg/ha) in combination with oxadiazon (0.5 kg) and one manual weeding at 40 DAT, fluchloralin (0.75 kg/ha) in combination with nitrofen (2.0 kg/ha) reduced weed growth, and resulted in the highest grain and straw yields (Patel and Patel 1985; Kulmi 1992; Kurmi 1993; Gill et al. 1992; Gogoi and Gogoi 1993; Rao et al. 1993; Bali et al. 1994; Dwivedi et al. 1994; Sing and Singh 1994). In directly sown rice, application of pendimethalin (0.75–1.25 kg/ha) at 6 DAS followed by post-emergence application of 2,4-D (1.0 kg/ha) at 25 DAS, application of thiobencarb (1.0 kg/ha) in combination with 2,4D (0.5 kg/ha), application of butachlor (0.5 kg/ha) followed by hand weeding, application of bensulfuron methyl (0.04 kg/ha), and pretilachlor (0.45 kg/ha) in combination with fenclorim (0.2 kg/ha) reduced weed growth, and resulted in the highest grain yield (Gogoi and Kalita 1992; Ramakrishnan et al. 1992). F. Irrigation The total water requirement for a crop depends on factors such as climate, agronomic factors, and cultivar. Rainfall in the semi-arid regions is erratic in duration and distribution, which leads to droughts of varying intensities during the crop season. Cassava needs adequate soil moisture for sprouting and subsequent establishment of planted stakes. The crop is grown in rainfed conditions in areas with annual rainfall ranging between 750 and 3,000 mm/year or in irrigated conditions. Although storage root yields are highest in areas with no pronounced dry season,

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or in irrigated conditions, the crop can be grown where there is no rainfall for up to 6 months (Cock 1983). Usually, an irrigation given on the day of planting is followed by two irrigations at an interval of 3–7 days, until the plants are established. Further irrigations are given depending on the distribution of rainfall, soil moisture, and evapo-transpiration demands. To ensure a maximum storage root yield, cassava needs to be irrigated at the depletion of 25–30% available soil moisture or 75–100% of cumulative pan evaporation rate during dry spell (Nayar et al. 1985; Pardales and Esquivel 1996). Withholding irrigation at least 45 days before the harvest can effectively mobilize accumulated carbohydrates from the shoot toward the storage root. Thus, starch content of cassava storage root was higher when the crop experienced drought during the last 2 months before harvest than in crops with no dry period (Vichukit et al. 1994; Fauzan and Puspitorini 2001). Cassava has a shallow root system, and about 86 to 96% of the root system is confined to the upper 10 cm and 40 cm of soil, respectively (Connor et al. 1981; Opara-Nadi and Lal 1987; Muhr et al. 1995). Drought during the early establishment period (9–82 DAP) substantially reduced the number and length of adventitious roots (Pardales and Esquivel 1996). Therefore, in drought conditions, the crop stops producing new leaves, and as the older leaves senescence and abscise, the crop becomes dormant. Drought thus causes significant reduction in LAI, photosynthesis, light interception, total dry matter production, and storage root yield (Connor and Cock 1981; Connor et al. 1981; Ramanujam 1990; Fauzan and Puspitorini 2001). Cassava yields were best correlated with rainfall between 3–5 months (Zhang Weite et al. 1998), 1–7 months (Villamayor and Davines 1987), or 4–11 months (CIAT 1998) in various climatic conditions, and in various cultivars grown. Cassava yields are seriously reduced if the rainfall is limiting growth during the period of the initial 3–5 months (Howeler 2001). The reduction in storage root yield, starch content, and starch yield of cassava cultivars drastically increases with an increase in the length of the dry period (less than 100 mm rainfall) (Fauzan and Puspitorini 2001). The mean storage root and starch yields of cassava cultivars were highest (43.2 and 11.5 t/ha, respectively) in the absence of a dry period. A dry period of 2, 3, 4, and 5 months reduced the storage root yield 38, 39.6, 39.1, and 59.2%, respectively, and the starch yield 6.9, 46.9, 50.9, and 71.3%, respectively. If water is available, supplementary irrigations during the dry period significantly increase the storage root yield compared to the crop that grew under rainfed conditions (Sushama et al. 1982; Vijayakumar et al. 1984; Villamayor and Destriza 1985; Kuruvilla et al. 1986; Nayar et al. 1985; Pardales et al. 1999).

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For leguminous annual crops, growth and development are very rapid, and thus the growth period is 75–120 days shorter compared to cassava. Moisture supply is very important in initiating germination. Therefore, planting is done after a good rain or irrigation. But, germination is also poor when soil moisture is excessive. Thus, a proper balance has to be maintained between optimal aeration and moisture content. At the early seedling stage, the plant is usually very fragile, and water must be available for survival. Leguminous crops also need water during pod filling or grain development to support the very rapid rate at which photosynthates are directed to the products. The availability of water during this period can significantly affect yield. The cropping pattern is determined by the rainfall pattern. For instance, short-duration cassava and mungbean with good drought tolerance can be grown toward the end of the monsoon season, whereas rice, a crop that requires more water, is grown in the early monsoon season so that the crop growth period coincides with the rainfall period. For many grain crops, heavy rain may adversely affect grain maturation. However, crops such as maize and cowpea, the grains of which are not adversely affected by heavy rain, can be planted even during the early monsoon season. The total water requirement of peanut ranges between 400 and 831 mm (ICAR 1980; Sivakumar and Sarma 1986) at various agro-climatic conditions. Although the rooting depth of peanut extends up to 2 m, a major portion of the roots occupies the top 30 cm of soil (Hammond et al. 1978; Robertson et al. 1980), and extracts more water from the top 30–45 cm of soil (Mantell and Goldin 1964; Shalhevet et al. 1976; Hammond and Boote 1981; Avasarmal et al. 1982). A peanut crop requires four irrigations at the vegetative, flowering, pegging, and pod development stages, respectively, for maximum haulm and pod yields (Sakarvadia and Yadav 1994; Singh et al. 1994). Because the flower is borne above ground, and after it withers, the stalk elongates, bends down, and forces the ovary below ground, soil surface moisture content is critical for peg entrance into the soil. Peanut withstands soil water deficit stress (WDS) during the vegetative phase. Stress during the start of flowering to the pegging/pod formation decreases pod yield (Sivakumar and Sarma 1986; Williams et al. 1986; Naveen et al. 1992). Soil-water deficiency depresses LAI (Vivekanandan and Gunasena 1976; Sivakumar and Sarma 1986). When the stress is relieved, peanut crop exposed to WDS during the vegetative to the start of pegging phase recovered LAI faster than those exposed to continuous WDS from emergence to maturity. The proportion of dry matter partitioned to pods was highest in the case of plants exposed to WDS during the vegetative to pegging phase. Soil

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WDS during the start of flowering to the start of seed growth, however, reduced the proportion of dry matter partitioned to the kernel, resulting in a slower rate of pod growth even after the stress was released (Billaz and Ochs 1961; Sivakumar and Sarma 1986). Soil water deficiency during the vegetative to the start of pegging phase resulted in an 8.9% decrease in pod yield (Williams et al. 1986), compared to plants that were irrigated, because stress during this phase had not affected the total dry matter produced and the rate of pod growth. Thus, irrigations can be withheld during much of the vegetative period without substantial reduction in pod yield (Rao et al. 1985; Sivakumar and Sarma 1986; Williams et al. 1986). On the other hand, WDS during the start of flowering to the start of seed growth reduced pod yield by 18–56.5% compared to plants that were irrigated (Sivakumar and Sarma 1986; Williams et al. 1986). Because pod initiation continues after the start of kernel growth due to the indeterminate nature of the crop, soil WDS during the pod filling phase reduces the initiation and development of pods, and pod yield (Boote et al. 1976; Pallas et al. 1979; Underwood et al. 1971; Ono et al. 1974; Velu 1998). Supplementary irrigations during the dry period significantly increase the storage root yield of cassava and the pod yield of peanut both in pure stand as well as in the intercrop system (Prabhakar and Nair 1992). In a cassava + peanut system, yield reductions of both crops were greater in rainfed conditions than in irrigated conditions. On the other hand, irrigation improved the peanut yield by 37–43% as compared to unirrigated conditions. Thus, irrigation is advantageous for increasing yields in intercropping systems. Cowpeas are grown as a rainfed crop, and are well adapted to drought conditions compared to other legumes. Under conditions of very low rainfall (181 mm) and high evaporative demand, grain yield as much as 1.0 t/ha has been achieved (Hall and Patel 1985). In irrigated conditions, it can yield up to 4 t/ha. It is a “water saver” with stomatal closure occurring at relatively high leaf water potential (LWP) after little water loss. Once plants are well established, they are tolerant to WDS, and pod set is not significantly affected. After the onset of water deficit stress (WDS), cowpea growth slows substantially. Stem apices are partially protected during drought, and the shoot apex remains alive long after the rest of the plant appears dead. If the crop gets water after a period of drought, the terminal meristem can start growth again, forming new leaves and flowers, and eventually set pods. Cowpea leaves exhibit strong paraheliotropy (the plane of leaf surface oriented along the direction of the sun’s rays), thus minimizing interception of radiation and loss of water through transpiration. Seed yield of cowpea is not significantly reduced

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by drought during the vegetative growth (Wien et al. 1979; Turk et al. 1980). But, repeated WDS prior to flowering substantially reduces seed yield compared with the irrigated plants (Summerfield et al. 1976). Flowers and young pods are shed even during a mild drought, though more nearly mature pods are retained. Although drought during the flowering stage substantially reduces seed yield due to the abscission of all the flowers, the seed yield is partially recovered after irrigation is resumed due to a new flush of flowers, that produce new pods. Drought during the pod filling stage substantially reduces seed yield, primarily due to the reduction in the number of seeds/pod, and to a lesser extent, the seed size (Summerfield et al. 1976; Wien et al. 1979; Turk et al. 1980). Soybean extracts more water than cowpea and is a “water spender” with leaf water potential (LWP) falling to comparatively low levels before the stomata completely close. Under WDS conditions, soybean leaves wilt and show minimal paraheliotropy, because of lower LWP, and therefore lower turgor. Water deficit stress reduces leaf area development (Sivakumar and Shaw 1978; Ramseur et al. 1985), photosynthesis (Baldocchi et al. 1985; Planchon et al. 1986), and N fixation in soybean (Chatterjee and Bhattacharyya 1986). Soybean uptakes the largest amount of water at the flowering and seed enlargement stages (Runge and Odell 1960; Doss and Thurlow 1974). Thus, reproductive development is more sensitive to WDS than is vegetative growth (Matson 1964; Doss and Thurlow 1974; Doss et al. 1974; Sionit and Kramer 1977; Ashley and Ethridge 1978; Korte et al. 1983a,b; Meckel et al. 1984). Drought stress during flowering (Thompson 1970; Singh and Tripathi 1972; Ashley and Ethridge 1978) and the seed enlargement (pod development) stage (Shaw and Laing 1966; Singh and Tripathi 1972; Sionit and Kramer 1977; Momen et al. 1979; Boyer 1983; Korte et al. 1983a,b; Meckel et al. 1984; Carter and Rufty 1993; Reicosky and Heatherly 1990) reduces soybean seed yield up to 53% as compared to seed yield in irrigated conditions. Drought stressed soybean plants produced fewer pods, followed by fewer seeds per pod, and smaller seed mass than well-watered plants (Shaw and Laing 1966; Pandey et al. 1984). Therefore, irrigation during flowering and pod elongation enhances seed yield (Runge and Odell 1960; Shaw and Laing 1966; Korte et al. 1983a,b). Soybean needs to be irrigated when there is depletion of 25% of available soil moisture to obtain the highest seed yields (2.5–13.8 t/ha). The decrease in seed yield, at the depletion of 50 and 75% of available soil moisture, varied among cultivars between 43–77 and 64–98%, respectively, as compared to the irrigation at the depletion of 25% of available soil moisture (Chandal et al. 1995).

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Mungbean is sensitive to waterlogging. It can be grown during early rainy season, late rainy season, or under irrigated conditions during dry season. For maximum grain yields, the total amount of water required is around 180–250 mm, which is split into irrigation intervals of 10–14 days with 30–40 mm for each irrigation. Adequate soil moisture is required from flowering to late pod fill. Flowering during high temperature and low moisture will reduce the yield. Excess rainfall in the late season can lead to disease problems and harvesting losses due to delayed maturity (Kuo et al. 1978; Jain and Mehra 1980; Oplinger et al. 1990). The irrigation requirement of maize varies with the amount of rainfall. Initially 2 or 3 irrigations (100–150 mm of water) are required to establish the crop before the onset of the monsoon. Further irrigations are given when the soil moisture falls below 60% of available soil moisture. During the rainy season 2 or 3 irrigations (100 mm) are given. During the dry, but cool season (average temperature 20–22°C), 11 irrigations are required. During the dry-hot weather season, 18 irrigations (900 mm) are required. Sandy soils require 500 mm water (ICAR 1980). Some studies have also reported that 400–644 mm of water are required for maximum grain yield (Musick and Dusek 1980; Howell et al. 1995). The critical stages of growth that are sensitive to WDS are the early vegetative period (30–40 DAS), and tasseling (45–50 DAS) (ICAR 1980). Water deficit stress for a week during the early vegetative stage can reduce maize yield by 25%, whereas that during tasseling can affect it to the extent of 50%. Water requirement of the rice crop varies between 884 and 2,500 mm in lowland conditions, depending on the soil, climate, rainfall, cultivar, and management practices (Vamadevan and Jha 1985). In heavy soils (soils with 40–100% clay content) with high water table, and hardpan in sub-soil, short-duration cultivars may require 1,000–1,500 mm of water through irrigation during the rainy season. In light soils (soils with 70–100% sand and 0–15% clay) with deep water table, long-duration cultivars may require 2,000–3,000 mm of water through irrigation during the rainy season (ICAR 1980). Maintaining soil moisture at saturation or shallow field submergence of the crop up to 5 cm through the growth period is beneficial to the crop (Vamadevan and Jha 1985; Raju et al. 1992). Tiller initiation, primordium initiation, and flowering are the most critical stages (Sen and Dutta 1967; Chaudhury and Pande 1968; Ray and Pande 1969; Vamadevan and Dastane 1972), and a shortage of water during these stages significantly reduces grain yield. When water resources are limited, the land may be submerged during the critical stages of growth and maintained only at the saturation level at other stages. During the cloudy-rainy season, when the weather is humid,

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evapo-transpiration rates are low, and the water table is near the surface, maintaining the soil moisture near saturation is adequate. When weather is hot and arid, the shallow submergence is beneficial for obtaining maximum yield (ICAR 1980). Rice planted in upland conditions is irrigated whenever there is a break in the rain. It can be grown in medium and heavy soils under evenly distributed rainfall of 1,600 mm.

VII. CONCLUSION AND FUTURE PROSPECTS There is considerable potential for simultaneous cultivation of shortduration (65–100 days) crops as intercrops during the initial three months of the cassava growth period. Short stature, bushy grain legumes such as mungbean, cowpea, and black gram; oil seed legumes such as peanut and soybean; vegetable legumes such as urd bean; and vegetable crops such as okra, tomato, onion, and cucumber are suitable crops to grow with cassava because they do not significantly reduce the yield per unit area of cassava. The possibility of growing pigeonpea with cassava is limited because of its tall stature and longer duration, and the yields of both cassava and pigeonpea are significantly reduced. Maize and rice can be grown successfully with cassava. Sometimes, cassava yield per unit area may be significantly reduced or even increased due to intercropping. The yield variation is because cassava yields per unit area in intercropping may be influenced by the kind of intercrop, spacing, growth duration, time of planting the main crop, fertility of the soil, weeds and pests, and the climatic conditions. When selecting cultivars to grow with cassava, the best results will be achieved by choosing early flowering, quick maturing, short, bushy types because they can reduce competition for solar radiation with cassava. On the other hand, either erect, little or late branching cassava cultivars with medium vigor must be selected for intercropping because they cause less shade and impose little competition on the intercrop. Planting of both cassava and the intercrop at the same time or with a difference of one week ensures a better yield of both crops. Neither the spatial arrangement of cassava nor the planting density of the intercrop significantly affects the yield of cassava or of the intercrop. Thus, as long as an optimum pure stand cassava plant density is maintained, cassava is flexible to variations in planting pattern in intercropping without causing an excessive yield reduction of the associate crop and at the same time produces a storage root yield near to that in pure stand. For legumes, soil moisture should be adequate during the early seedling and

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pod development period of growth. When moisture is not limited, cassava can also be planted as a relay crop following annuals such as maize, peanut, sorghum, selected vegetables, tobacco, and rice. The fertilizer requirement for optimum intercrop productivity may often differ considerably from the mere addition of fertilizer requirements of the individual crops, because growing two crops in association may result either in better exploitation of soil resources (due to different root distribution systems) or in competition between the crops for nutrients, and other growth factors. Therefore, no single uniform recommendation is possible for any system. Any system of intensive cropping drains the soil heavily of available plant nutrients. Therefore, optimum fertilizer requirements of the intercropping systems have to be determined at a given site, and integrated with the corresponding soil tests and the nutrient uptake by the crops involved in the system. In formulating N rates, due consideration should be given to the contributions from the associated leguminous crops grown in the system. Inoculation of legumes with efficient strains of Rhizobia will lead to better growth of the legumes. When cassava is intercropped with other crops, the demand for nutrients is intensified, particularly when each component crop is planted at its normal pure stand density. Under these conditions, the removal of nutrients from the soil is greater in the intercropping systems. If these nutrients are not replaced, soil fertility deteriorates. Thus, it may be necessary to apply fertilizers to both crops. Cassava is normally fertilized at 1 to 3 months after planting. But in intercropping, fertilization for cassava may be delayed until the intercrop is harvested. The intercrop residues can be incorporated into the soil, and thereby, the inorganic requirement of the cassava crop can be met. For the cassava + cowpea or soybean system, late-maturing cowpea or soybean cultivars strongly compete with cassava for N. A lower N content in the leaves of cassava than that in pure stand suggests an adverse effect of intercropping on the growth of cassava through N deficiency. As a result, cassava becomes deficient in N, and growth and yield are reduced when intercropped with late-maturing cultivars of cowpea or soybean. Therefore, in areas with low soil fertility, cassava yield may be reduced substantially by intercropping with soybean or cowpea. With perennials, the banana + cassava + cowpea or French bean crop combination is the most profitable system. Although intercropping can be adopted in cassava with suitable cultivars and additional nutrients, there is some degree of competition between the component crops. This accounts for about 10–25% of the reduction in the yield of intercropped cassava compared to that in the pure stand. However, the net

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income in intercropping was always higher than that in the pure stand of cassava. Cassava can be successfully relay cropped following maize, peanut, sorghum, selected vegetables, and tobacco. Cassava can also be planted following vegetable cowpea or rice under lowland conditions. In lowland conditions, due to better soil moisture status throughout the growth period, cassava yields more than double the yield that is normally obtained under upland conditions. In upland rainfed conditions, planting cassava after harvest of a short-duration crop was not found to be profitable. This is mainly due to the short rainfall season and the lack of soil moisture during the bulking period of storage roots. The economic yield of a component crop in pure stand and in an intercropping system, and the efficiency of an intercropping system depend on several factors, including the morphology of cultivars, spatial arrangement, crop duration, and the cultivars’ period of competition for light, water, and fertilizer. Differences in the value of the crops between regions may alter which system is most profitable. The system with the largest net income may be different from the system with the highest productivity. In this situation, a grower can plant a cassava-based intercropping system, although the productivity of cassava may not be maximized. Future research is needed to (1) evaluate the short-duration cassava cultivars (that yield highest in 6–7 months) + intercrop systems; (2) evaluate the productivity of cassava with perennials such as short and bushy mango (Mangifera indica), tall teak (Tectona grandis) plantations, cashewnut (Anacardium occidentale), and similar systems; (3) evaluate the productivity of cassava with vegetable crops such as pumpkin (Cucurbita pepo, C. maxima), cucumber (Cucumis sativus), muskmelon (C. melo), watermelon (Citrulis vulgaris, C. colocyanthis), ridge-guard (Luffa acutangula), and leafy vegetables (Amaranthus tricolor, A. tristis); (4) determine the photosynthesis and respiration processes and their relation to the nutrient uptake in various cassava-based intercropping systems; (5) evaluate cassava-based intercropping systems suitable for low rainfall areas where the annual rainfall varies between 900 and 1,000 mm; (6) develop micro-irrigation systems suitable for cassava-based intercropping systems; (7) determine optimum ideotypes for various cassava-based intercropping systems; (8) determine the optimum fertilizer requirement for various cassava-based intercropping systems on the basis of soil testing and plant tissue analysis; (9) evaluate the effect of biofertilizers and organic fertilizers in various intercropping systems; and (10) develop models for various cassava-based intercropping systems.

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Wien, H. C., E. J. Littleton, and A. Ayanaba. 1979. Drought stress of cowpea and soybean under tropical conditions. p. 283–301. In: H. Mussell and R. C. Staples (eds.), Stress physiology in crop plants. Wiley Interscience, New York. Wilcox, J. R. 1974. Response of three soybean strains to equidistant spacing. Agron. J. 66:409–412. Willcott, J., S. J. Herbert, and Liu-Zhi-Yi. 1984. Leaf area display and light interception in short-season soybeans. Field Crops Res. 9:173–182. Willey, R. W. 1979. Intercropping—Its importance and research needs. Part 1. Competition and yield advantages. Field Crops Abst. 32:1–10. Willey, R. W., and D. S. O. Osiru. 1972. Studies on mixtures of maize and beans with particular reference to plant population. J. Agr. J. (Camb.) 79:519–529. Willey, R. W., M. R. Rao, and M. Natarajan. 1981. Traditional cropping systems with pigeonpea and their improvement. p. 11–25. In: Y. L. Nene (ed.), ICRISAT (Int. Crop Res. Inst. For Semi Arid Tropics), Proc. Int. Workshop on Pigeonpea. Vol. 1. 15–19 Dec. 1980, Patancheru, A.P., Hyderabad, India. Williams, C. N. 1972. Growth and productivity of tapioca (Manihot utilissima) III. Crop ratio, spacing and yield. Expt. Agr. 8:15–23. Williams, C. N. 1974. Growth and productivity of tapioca (Manihot utilissima). IV. Development and yield of tubers. Expt. Agr. 10:9–16. Williams, C. N., and S. M. Ghazali. 1969. Growth and productivity of tapioca (Manihot utilissima) I. Leaf characteristics and yield. Expt. Agr. 5:183–194. Williams, J. H., R. C. N. Rao, R. Matthews, and D. Harris. 1986. Response of groundnut genotypes to drought. p. 99–106. In: M. V. K. Sivakumar and S. M. Virmani (eds.), Agrometeorology of groundnut. Proc. Int. Symp., Int. Crop Res. Inst. Semi Arid Trop., Andhra Pradesh, India. Wilson, G. F., and T. L. Lawson. 1982. Increased resource exploitation through intercropping with cassava—Summary. p. 74–75. In: C. L. Keswani and B. J. Ndunguru (eds.), Intercropping. Proc. 2nd Symp. Intercropping in Semi-arid Areas, Morogoro, Tanzania, 1980, Ottawa, Ont. IDRC. Woodroof, J. G. 1966. Peanuts, production, processing, products. AVI Publ., Westport, Connecticut. Wu, G., L. T. Wilson, A. M. McClung. 1998. Contribution of rice tillers to dry matter accumulation and yield. Agron. J. 90:317–323. Wynne, J. C., and W. C. Gregory. 1981. Peanut breeding. Adv. Agron. 34:39–72. Wynne, J. C., D. A. Emery, and R. J. Downs. 1973. Photoperiodic response of peanuts. Crop Sci. 13:511–514. Yakadri, M., M. M. Husain, and V. Satyanarayana. 1992. Response of rainfed groundnut (Arachis hypogaea) to potassium with varying levels of nitrogen and phosphorus. Ind. J. Agron. 37:202–203. Yamaguchi, J. 1974. Varietal traits limiting the grain yield of tropical maize. IV. Plant traits and productivity of tropical varieties. Soil Sci. Plant Nutr. 20:287–304. Yoshida, S., and F. T. Paraw. 1987. Climatic influence on yield and yield components of low land rice in the tropics, Climate and rice. Los Banos, Philippines, IRRI, p. 471–494. Zandstra, H. G. 1978. Techniques for on-farm cropping systems research. Philippines, Int. Rice Res. Inst. (Mimeo). Zandstra, H. G. 1979. Cassava intercropping research: agroclimatic and biological interactions. p. 67–76. In: E. Weber, B. Nestel, and M. Campbell (eds.), Intercropping with cassava. Proc.. Int. Workshop, Trivandrum, India, 1978, Ottawa, Ont. IDRC. Zang Weite, Lin Xiong, Li Kaimian, Huang Jie, Tian Yinong, Lee Jun, Fu Quohui. 1998. Cassava agronomy research in China. p. 191–210. In: R. H. Howeler (ed.), Cassava

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breeding, agronomy, and farmers participatory research in Asia. Proc. 5th Reg. Workshop, Danzhou, Hainan, China, Nov. 3–8, 1996. Zheng Xuequin, Lin Xiong, Zhang Weite, Ye Kaifu, and Tian Yinong. 1992. Recent progress in cassava varietal and agronomic research in China. p. 64–80. In: R. H. Howeler (ed.), Cassava breeding, agronomy and utilization research in Asia. Proc. 3rd Reg. Workshop, Malang, Indonesia, Oct. 22–27, 1990.

Subject Index Volume 30 Anatomy & morphology, red bayberry, 92–96 Carrot postharvest physiology, 284–288 Cassava: multiple cropping, 355–500 postharvest physiology, 288–295 China, protected cultivation, 115–162 Citrus, irrigation, 37–82 Dedication, Kester, D.E., xiiixvii Floricultural crops, China protected culture, 141–148 Flower & flowering, girdling, 1–26 Fruit: fresh cut, 185–251 red bayberry, 83–11g tomato cracking, 163–184 Fruit crops greenhouses, Chinese, 149–158 citrus irrigation, 37–82 Ginger postharvest physiology, 297–299 Girdling, 1–26 Greenhouse & greenhouse crops, China protected cultivation, 115–162 Growth substances, girdling, 1–26 Irrigation, citrus, 37–83

Morphology, red bayberry, 92–96 Multiple cropping, 355–500 Myrica, see Red bayberry Physiology: citrus irrigation, 55–67 girdling, 1–26 red bayberry, 96–99 Postharvest physiology: carrot storage, 284–288 cassava storage, 288–295 fresh-cut fruits & vegetables, 85–255 ginger storage, 297–299 Jerusalem artichoke storage, 271–276 potato low temperature sweetening, 317–355 potato storage, 259–271 root & tuber crops, 253–316 sweet potato storage, 276–284 taro storage, 295–297 Potato: low temperature sweetening, 317–353 postharvest physiology, 259–271 Red bayberry, 83–113 Root & tuber crops: carrot postharvest physiology, 284–288 cassava multiple cropping, 355–500 cassava postharvest physiology, 288–295 ginger postharvest physiology, 297–299

Jerusalem artichoke postharvest physiology, 271–276 potato postharvest physiology, 259–271 potato low temperature sweetening, 317–354 Root & tuber crops (cont.) sweet potato postharvest physiology, 276–284 taro postharvest physiology, 295–297 Salinity, citrus irrigation, 37–83 Storage: carrot postharvest physiology, 284–288 cassava postharvestg physiology, 288–295 ginger postharvest physiology, 297–299 Jerusalem artichoke postharvest physiology, 271–276 Potato low temperature sweetening, 30:317–354 potato postharvest physiology, 259–271 root & tuber crops, 253–316 sweet potato postharvest physiology, 276–284 taro postharvest physiology, 295–297 Sweet potato postharvest physiology, 276–284 Taro postharvest physiology & storage, 295–297 Tomato fruit cracking, 163–184

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502 Vegetable crops: carrot postharvest physiology a& storage, 284–288 cassava postharvest physiology & storage, 288–295 fresh cut, 185–251 ginger postharvest physiology & storage, 297–299 greenhouses in China, 126–141

SUBJECT INDEX Jerusalem artichoke postharvest physiology & storage, 271–276 potato low temperature sweetening, 30:317–354 potato postharvest physiology & storage, 30: 259–271 root & tuber postharvest physiology & storage, 253–316

sweet potato physiology & storage, 276–284 taro postharvest physiology &storage, 295–297 tomato fruit cracking, 163–184 Water relations, citrus, 37–83

Cumulative Subject Index (Volumes 1–30) A Abscisic acid: chilling injury, 15:78–79 cold hardiness, 11:65 dormancy, 7:275–277 genetic regulation, 16:9–14; 20–21 lychee, 28:437–443 mechanical stress, 17:20 rose senescence, 9:66 stress, 4:249–250 Abscission: anatomy & histochemistry, 1:172–203 citrus, 15:145–182, 163–166 flower & petals, 3:104–107 regulation, 7:415–416 rose, 9:63–64 Acclimatization: foliage plants, 6:119–154 herbaceous plants, 6:379–395 micropropagation, 9:278–281, 316–317 Actinidia, 6:4–12 Adzuki bean, genetics, 2:373 Agapanthus, 25:56–57 Agaricus, 6:85–118 Agrobacterium tumefaciens, 3:34 Air pollution, 8:1–42 Alkaloids, steroidal, 25:171–196 Allium phytonutrients, 28:156–159 Almond: bloom delay, 15:100–101 in vitro culture, 9:313

postharvest technology & utilization, 20:267–311 wild of Kazakhstan, 29:262–265 Alocasia, 8:46, 57, see also Aroids Alternate bearing: chemical thinning, 1:285–289 fruit crops, 4:128–173 pistachio, 3:387–388 Aluminum: deficiency & toxicity symptoms in fruits & nuts, 2:154 Ericaceae, 10:195–196 Amarcrinum, 25: 57 Amaryllidaceae, growth, development, flowering, 25:1–70 Amaryllis, 25:4–15 Amorphophallus, 8:46, 57, see also Aroids Anatomy & morphology: apple flower & fruit, 10:273–308 apple tree, 12:265–305 asparagus, 12:71 cassava, 13:106–112 citrus, abscission, 15:147–156 embryogenesis, 1:4–21, 35–40 fig, 12:420–424 fruit abscission, 1:172–203 fruit storage, 1:314 ginseng, 9:198–201 grape flower, 13:315–337 grape seedlessness, 11:160–164 heliconia, 14:5–13

kiwifruit, 6:13–50 magnetic resonance imaging, 20:78–86, 225–266 orchid, 5:281–283 navel orange, 8:132–133 pecan flower, 8:217–255 petal senescence, 1:212–216 pollution injury, 8:15 red bayberry, 20:92–96 waxes, 23:1–68 Arogenesis, woody species, 10:171–173 Angiosperms, embryogenesis, 1:1–78 Anthurium, see also Aroids, ornamental fertilization, 5:334–335 Antitranspirants, 7:334 cold hardiness, 11:65 Apical meristem, cryopreservation, 6:357–372 Apple: alternate bearing, 4:136–137 anatomy & morphology of flower & fruit, 10:273–309 bioregulation, 10:309–401 bitter pit, 11:289–355 bloom delay, 15:102–104 CA storage, 1:303–306 chemical thinning, 1:270–300 fertilization, 1:105 fire blight control, 1:423–474 flavor, 16:197–234 flower induction, 4:174–203

Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 503

504 Apple (cont.) fruiting, 11:229–287 fruit cracking & splitting, 19:217–262 functional phytonutrients, 27:304 germplasm acquisition & resources, 29:1–61 in vitro, 5:241–243; 9:319–321 light, 2:240–248 maturity indices, 13:407–432 mealiness, 20:200 nitrogen metabolism, 4:204–246 replant disease, 2:3 root distribution, 2:453–456 scald, 27:227–267 stock-scion relationships, 3:315–375 summer pruning, 9:351–375 tree morphology & anatomy, 12:265–305 vegetative growth, 11:229–287 watercore, 6:189–251 weight loss, 25:197–234 wild of Kazakhstan, 29:63–303, 305–315 yield, 1:397–424 Apricot: bloom delay, 15:101–102 CA storage, 1:309 origin & dissemination, 22:225–266 wild of Kazakhstan, 29:325–326 Arabidopsis: molecular biology of flowering, 27:1–39, 41–77 Aroids: edible, 8:43–99; 12:166–170 ornamental, 10:1–33 Arsenic, deficiency & toxicity symptoms in fruits & nuts, 2:154 Artemisia, 19:319–371 Artemisinin, 19:346–359 Artichoke, CA storage, 1:349–350

CUMULATIVE SUBJECT INDEX Asexual embryogenesis, 1:1–78; 2:268–310; 3:214–314; 7:163–168, 171–173, 176–177, 184, 185–187, 187–188, 189; 10:153–181; 14:258–259, 337–339; 24:6–7; 26:105–110 Asparagus: CA storage, 1:350–351 fluid drilling of seed, 3:21 postharvest biology, 12:69–155 Auxin: abscission, citrus, 15:161, 168–176 bloom delay, 15:114–115 citrus abscission, 15:161, 168–176 dormancy, 7:273–274 flowering, 15:290–291, 315 genetic regulation, 16:5–6, 14, 21–22 geotropism, 15:246–267 mechanical stress, 17:18–19 petal senescence, 11:31 Avocado: CA & MA, 22:135–141 flowering, 8:257–289 fruit development, 10:230–238 fruit ripening, 10:238–259 rootstocks, 17:381–429 Azalea, fertilization, 5:335–337 B Babaco, in vitro culture, 7:178 Bacteria: diseases of fig, 12:447–451 ice nucleating, 7:210–212; 11:69–71 pathogens of bean, 3:28–58 tree short life, 2:46–47 wilt of bean, 3:46–47 Bacteriocides, fire blight, 1:450–459 Bacteriophage, fire blight control, 1:449–450 Banana: CA & MA, 22:141–146 CA storage, 1:311–312

fertilization, 1:105 in vitro culture, 7:178–180 Banksia, 22:1–25 Barberry, wild of Kazakhstan, 29:332–336 Bean: CA storage, 1:352–353 fluid drilling of seed, 3:21 resistance to bacterial pathogens, 3:28–58 Bedding plants, fertilization, 1:99–100; 5:337–341 Beet: CA storage, 1:353 fluid drilling of seed, 3:18–19 Begonia (Rieger), fertilization, 1:104 Biennial bearing. See Alternate bearing Bilberry, wild of Kazakhstan, 29:347–348 Biochemistry, petal senescence, 11:15–43 Bioreactor technology, 24:1–30 Bioregulation, see also Growth substances apple & pear, 10:309–401 Bird damage, 6:277–278 Bitter pit in apple, 11:289–355 Blackberry: harvesting, 16:282–298 wild of Kazakhstan, 29:345 Black currant, bloom delay, 15:104 Bloom delay, deciduous fruits, 15:97 Blueberry: developmental physiology, 13:339–405 harvesting, 16:257–282 nutrition, 10:183–227 Boron: deficiency & toxicity symptoms in fruits & nuts, 2:151–152 foliar application, 6:328 nutrition, 5:327–328 pine bark media, 9:119–122 Botanic gardens, 15:1–62 Bramble, harvesting, 16:282–298

CUMULATIVE SUBJECT INDEX Branching, lateral: apple, 10:328–330 pear, 10:328–330 Brassica classification, 28:27–28 Brassicaceae, in vitro, 5:232–235 Breeding, see Genetics & breeding Broccoli, CA storage, 1:354–355 Brussels sprouts, CA storage, 1:355 Bulb crops, see also Tulip development, 25:1–70 flowering, 25:1–70 genetics & breeding, 18:119–123 growth, 25: 1–70 in vitro, 18:87–169 micropropagation, 18:89–113 root physiology, 14:57–88 virus elimination, 18:113–123 C CA storage. see Controlledatmosphere storage Cabbage: CA storage, 1:355–359 fertilization, 1:117–118 Cactus: crops, 18:291–320 grafting, 28:106–109 reproductive biology, 18:321–346 Caladium, see Aroids, ornamental Calciole, nutrition, 10:183–227 Calcifuge, nutrition, 10:183–227 Calcium: bitter pit, 11:289–355 cell wall, 5:203–205 container growing, 9:84–85 deficiency & toxicity symptoms in fruits & nuts, 2:148–149 Ericaceae nutrition, 10:196–197 foliar application, 6:328–329

fruit softening, 10:107–152 nutrition, 5:322–323 pine bark media, 9:116–117 tipburn, disorder, 4:50–57 Calmodulin, 10:132–134, 137–138 Caparis, see Caper bush Caper bush, 27:125–188 Carbohydrate: fig, 12:436–437 kiwifruit partitioning, 12:318–324 metabolism, 7:69–108 partitioning, 7:69–108 petal senescence, 11:19–20 reserves in deciduous fruit trees, 10:403–430 Carbon dioxide, enrichment, 7:345–398, 544–545 Carnation, fertilization, 1:100; 5:341–345 Carrot: CA storage, 1:362–366 fluid drilling of seed, 3:13–14 postharvest physiology, 30:284–288 Caryophyllaceae, in vitro, 5:237–239 Cassava: crop physiology, 13:105–129 molecular biology, 26:85–159 multiple cropping, 30:355–50 postharvest physiology, 30:288–295 root crop, 12:158–166 Cauliflower, CA storage, 1:359–362 Celeriac, CA storage, 1:366–367 Celery: CA storage, 1:366–367 fluid drilling of seed, 3:14 Cell culture, 3:214–314 woody legumes, 14:265–332 Cell membrane: calcium, 10:126–140 petal senescence, 11:20–26

505 Cellular mechanisms, salt tolerance, 16:33–69 Cell wall: calcium, 10:109–122 hydrolases, 5:169–219 ice spread, 13:245–246 tomato, 13:70–71 Chelates, 9:169–171 Cherimoya, CA & MA, 22:146–147 Cherry: bloom delay, 15:105 CA storage, 1:308 origin, 19:263–317 wild of Kazakhstan, 29:326–330 Chestnut: blight, 8:281–336 in vitro culture, 9:311–312 Chicory, CA storage, 1:379 Chilling: injury, 4:260–261; 15:63–95 injury, chlorophyll fluorescence, 23:79–84 pistachio, 3:388–389 China, protected cultivation, 30:37–82 Chlorine: deficiency & toxicity symptoms in fruits & nuts, 2:153 nutrition, 5:239 Chlorophyll fluorescence, 23:69–107 Chlorosis, iron deficiency induced, 9:133–186 Chrysanthemum fertilization, 1:100–101; 5:345–352 Citrus: abscission, 15:145–182 alternate bearing, 4:141–144 asexual embryogenesis, 7:163–168 CA storage, 1:312–313 chlorosis, 9:166–168 cold hardiness, 7:201–238 fertilization, 1:105 flowering, 12:349–408 functional phytochemicals, fruit, 27:269–315 honey bee pollination, 9:247–248

506 Citrus (cont.) in vitro culture, 7:161–170 irrigation, 30:37–82 juice loss, 20:200–201 navel orange, 8:129–179 nitrogen metabolism, 8:181 practices for young trees, 24:319–372 rootstock, 1:237–269 viroid dwarfing, 24:277–317 Classification: Brassica, 28:27–28 lettuce, 28:25–27 potato, 28:23–26 tomato, 28:21–23 Clivia, 25:57 Cloche (tunnel), 7:356–357 Coconut palm: asexual embryogenesis, 7:184 in vitro culture, 7:183–185 Cold hardiness, 2:33–34 apple & pear bioregulation, 10:374–375 citrus, 7:201–238 factors affecting, 11:55–56 herbaceous plants, 6:373–417 injury, 2:26–27 nutrition, 3:144–171 pruning, 8:356–357 Colocasia, 8:45, 55–56, see also Aroids Common blight of bean, 3:45–46 Compositae, in vitro, 5:235–237 Container production, nursery crops, 9:75–101 Controlled-atmosphere (CA) storage: asparagus, 12:76–77, 127–130 chilling injury, 15:74–77 flowers, 3:98; 10:52–55 fruit quality, 8:101–127 fruits, 1:301–336; 4:259–260 pathogens, 3:412–461 seeds, 2:134–135 tropical fruit, 22:123–183 tulip, 5:105 vegetable quality, 8:101–127

CUMULATIVE SUBJECT INDEX vegetables, 1:337–394; 4:259–260 Controlled environment agriculture, 7:534–545, see also Greenhouse greenhouse crops; hydroponic culture; protected culture Copper: deficiency & toxicity symptoms in fruits & nuts, 2:153 foliar application, 6:329–330 nutrition, 5:326–327 pine bark media, 9:122–123 Corynebacterium flaccumfaciens, 3:33, 46 Cotoneaster, wild of Kazakhstan, 29:316–317 Cowpea: genetics, 2:317–348 U.S. production, 12:197–222 Cranberry: botany & horticulture, 21:215–249 fertilization, 1:106 harvesting, 16:298–311 wild of Kazakhstan, 29:349 Crinum, 25:58 Crucifers phytochemicals, 28:150–156 Cryopreservation: apical meristems, 6:357–372 cold hardiness, 11:65–66 Cryphonectria parasitica. See Endothia parasitica Crytosperma, 8:47, 58, see also Aroids Cucumber: CA storage, 1:367–368 grafting, 28:91–96 Cucurbita pepo, cultivar groups history, 25:71–170 Currant: harvesting, 16:311–327 wild of Kazakhstan, 29:341 Custard apple, CA & MA, 22:164 Cyrtanthus, 25:15–19

Cytokinin: cold hardiness, 11:65 dormancy, 7:272–273 floral promoter, 4:112–113 flowering, 15:294–295, 318 genetic regulation, 16:4–5, 14, 22–23 grape root, 5:150, 153–156 lettuce tipburn, 4:57–58 petal senescence, 11:30–31 rose senescence, 9:66 D Date palm: asexual embryogenesis, 7:185–187 in vitro culture, 7:185–187 Daylength, see Photoperiod Dedication: Bailey, L.H., 1:v–viii Beach, S.A., 1:v–viii Bukovac, M.J., 6:x–xii Campbell, C.W., 19:xiii Cummins, J.N., 15:xii–xv Dennis, F.G., 22:xi–xii De Hertogh, A.A., 26:xi–xii Faust, Miklos, 5:vi–x Hackett, W.P., 12:x–xiii Halevy, A.H., 8:x–xii Hess, C.E., 13:x–xii Kader, A.A., 16:xii–xv Kamemoto, H., 24:x–xiii Kester, D.E., 30:xiii–xvii Looney, N.E., 18:xiii Magness, J.R., 2:vi–viii Moore, J.N., 14:xii–xv Possingham, J.V., 27:xi–xiii Pratt, C., 20:ix–xi Proebsting, Jr., E.L., 9:x–xiv Rick, Jr., C.M., 4:vi–ix Ryugo, K., 25:x–xii Sansavini, S., 17:xii–xiv Sherman, W.B., 21:xi–xiii Smock, R.M., 7:x–xiii Sperling, C.E., 29:ix–x Stevens, M.A., 28:xi–xiii Weiser, C.J., 11:x–xiii Whitaker, T.W., 3:vi–x Wittwer, S.H., 10:x–xiii Yang, S.F., 23:xi Deficit irrigation, 21:105–131

CUMULATIVE SUBJECT INDEX Deficiency symptoms, in fruit & nut crops, 2:145–154 Defoliation, apple & pear bioregulation, 10:326–328 ‘Delicious’ apple, 1:397–424 Desiccation tolerance, 18:171–213 Dieffenbachia, see Aroids, ornamental Dioscorea., see Yam Disease: air pollution, 8:25 aroids, 8:67–69; 10:18; 12:168–169 bacterial, of bean, 3:28–58 cassava, 12:163–164 control by virus, 3:399–403 controlled-atmosphere storage, 3:412–461 cowpea, 12:210–213 fig, 12:447–479 flooding, 13:288–299 hydroponic crops, 7:530–534 lettuce, 2:187–197 mycorrhizal fungi, 3:182–185 ornamental aroids, 10:18 resistance, acquired, 18:247–289 root, 5:29–31 stress, 4:261–262 sweet potato, 12:173–175 tulip, 5:63, 92 turnip moasic virus, 14:199–238 waxes, 23:1–68 yam (Dioscorea), 12:181–183 Disorder, see also Postharvest physiology: bitterpit, 11:289–355 fig, 12:477–479 pear fruit, 11:357–411 watercore, 6:189–251; 11:385–387 Dormancy, 2:27–30 blueberry, 13:362–370 fruit trees, 7:239–300 tulip, 5:93 Drip irrigation, 4:1–48 Drought resistance, 4:250–251 cassava, 13:114–115

Durian, CA & MA, 22:147–148 Dwarfing: apple, 3:315–375 apple mutants, 12:297–298 by virus, 3:404–405 E Easter lily, fertilization, 5:352–355 Eggplant: grafting, 28:103–104 phytochemicals, 28:162–163 Elderberry, wild of Kazakhstan, 29:349–350 Embryogenesis. See Asexual embryogenesis Endothia parasitica, 8:291–336 Energy efficiency, in greenhouses, 1:141–171; 9:1–52 Environment: air pollution, 8:20–22 controlled for agriculture, 7:534–545 controlled for energy efficiency, 1:141–171; 9:1–52 embryogenesis, 1:22, 43–44 fruit set, 1:411–412 ginseng, 9:211–226 greenhouse management, 9:32–38 navel orange, 8:138–140 nutrient film technique, 5:13–26 Epipremnum, see Aroids, ornamental Eriobotrya japonica. see Loquat Erwinia: amylovora, 1:423–474 lathyri, 3:34 Essential elements: foliar nutrition, 6:287–355 pine bark media, 9:103–131 plant nutrition, 5:318–330 soil testing, 7:1–68 Ethylene: abscission, citrus, 15:158–161, 168–176 apple bioregulation, 10:366–369

507 avocado, 10:239–241 bloom delay, 15:107–111 CA storage, 1:317–319, 348 chilling injury, 15:80 citrus abscission, 15:158–161, 168–176 cut flower storage, 10:44–46 dormancy, 7:277–279 flowering, 15:295–296, 319 flower longevity, 3:66–75 genetic regulation, 16:6–7, 14–15, 19–20 kiwifruit respiration, 6:47–48 mechanical stress, 17:16–17 petal senescence, 11:16–19, 27–30 rose senescence, 9:65–66 Eucharis, 25:19–22 Eucrosia, 25:58 F Feed crops, cactus, 18:298–300 Feijoa, CA & MA, 22:148 Fertilization & fertilizer: anthurium, 5:334–335 azalea, 5:335–337 bedding plants, 5:337–341 blueberry, 10:183–227 carnation, 5:341–345 chrysanthemum, 5:345–352 controlled release, 1:79–139; 5:347–348 Easter lily, 5:352–355 Ericaceae, 10:183–227 foliage plants, 5:367–380 foliar, 6:287–355 geranium, 5:355–357 greenhouse crops, 5:317–403 lettuce, 2:175 nitrogen, 2:401–404 orchid, 5:357–358 poinsettia, 5:358–360 rose, 5:361–363 snapdragon, 5:363–364 soil testing, 7:1–68 trickle irrigation, 4:28–31 tulip, 5:364–366 Vaccinium, 10:183–227 zinc nutrition, 23:109–128

508 Fig: industry, 12:409–490 ripening, 4:258–259 Filbert, in vitro culture, 9:313–314 Fire blight, 1:423–474 Flooding, fruit crops, 13:257–313 Floral scents, 24:31–53 Floricultural crops, see also individual crops: Amaryllidaceae, 25:1–70 Banksia, 22:1–25 China, protected culture, 30:141–148 fertilization, 1:98–104 growth regulation, 7:399–481 heliconia, 14:1–55 Leucospermum, 22:27–90 postharvest physiology & senescence, 1:204–236; 3:59–143; 10:35–62; 11:15–43 Protea, 26:1–48 Florigen, 4:94–98 Flower & flowering: Amaryllidaceae, 25:1–70 apple anatomy & morphology, 10:277–283 apple bioregulation, 10:344–348 Arabidopsis, 27:1–39, 41–77 aroids, ornamental, 10:19–24 avocado, 8:257–289 Banksia, 22:1–25 blueberry development, 13:354–378 cactus, 18:325–335 citrus, 12:349–408 control, 4:159–160; 15:279–334 development (postpollination), 19:1–58 fig, 12:424–429 girdling, 20:1–26 grape anatomy & morphology, 13:354–378 homeotic gene regulation, 27:41–77 honey bee pollination, 9:239–243

CUMULATIVE SUBJECT INDEX induction, 4:174–203, 254–256 initiation, 4:152–153 in vitro, 4:106–127 kiwifruit, 6:21–35; 12:316–318 Leucospermum, 22:27–90 lychee, 28:397–421 orchid, 5:297–300 pear bioregulation, 10:344–348 pecan, 8:217–255 perennial fruit crops, 12:223–264 phase change, 7:109–155 photoperiod, 4:66–105 pistachio, 3:378–387 postharvest physiology, 1:204–236; 3:59–143; 10:35–62; 11:15–43 postpollination development, 19:1–58 protea leaf blackening, 17:173–201 pruning, 8:359–362 raspberry, 11:187–188 regulation in floriculture, 7:416–424 rhododendron, 12:1–42 rose, 9:60–66 scents, 24:31–53 senescence, 1:204–236; 3:59–143; 10:35–62; 11:15–43;18:1–85 strawberry, 28:325–349 sugars, 4:114 thin cell layer morphogenesis, 14:239–256 tulip, 5:57–59 water relations, 18:1–85 Fluid drilling, 3:1–58 Foliage plants: acclimatization, 6:119–154 fertilization, 1:102–103; 5:367–380 Foliar nutrition, 6:287–355 Freeze protection, see Frost protection Frost: apple fruit set, 1:407–408 citrus, 7:201–238 protection, 11:45–109 Fruit: abscission, 1:172–203

abscission, citrus, 15:145–182 apple anatomy & morphology, 10:283–297 apple bioregulation, 10:348–374 apple bitter pit, 11:289–355 apple flavor, 16:197–234 apple maturity indices, 13:407–432 apple ripening & quality, 10:361–374 apple scald, 27:227–267 apple weight loss, 25:197–234 avocado development & ripening, 10:229–271 bloom delay, 15:97–144 blueberry development, 13:378–390 cactus physiology, 18:335–341 CA storage & quality, 8:101–127 chilling injury, 15:63–95 coating physiology, 26:161–238 cracking, 19:217–262; 30:163–184 diseases in CA storage, 3:412–461 drop, apple fresh cut, 30:185–251 functional phytochemicals, 27:269–315 growth measurement, 24:373–431 kiwifruit, 6:35–48; 12:316–318 loquat, 23:233–276 lychee, 28:433–444 maturity indices, 13:407–432 navel orange, 8:129–179 nectarine, postharvest, 11:413–452 nondestructive postharvest quality evaluation, 20:1–119 olive processing, 25:235–260 peach, postharvest, 11:413–452

CUMULATIVE SUBJECT INDEX pear, bioregulation, 10:348–374 pear, fruit disorders, 11:357–411 pear maturity indices, 13:407–432 pear ripening & quality, 10:361–374 pear scald, 27:227–267 pear volatiles, 28:237–324 pistachio, 3:382–391 phytochemicals, 28:125–185 plum, 23:179–231 quality & pruning, 8:365–367 red bayberry, 30: 83–113 ripening, 5:190–205 set, 1:397–424; 4:153–154 set in navel oranges, 8:140–142 size & thinning, 1:293–294; 4:161 softening, 5:109–219; 10:107–152 splitting, 19:217–262 strawberry growth & ripening, 17:267–297 texture, 20:121–224 thinning, apple & pear, 10:353–359 tomato cracking, 30:163–184 tomato parthenocarpy, 6:65–84 tomato ripening, 13:67–103 volatiles, pear, 28:237–324 Fruit crops, see also Individual crop alternate bearing, 4:128–173 apple bitter pit, 11:289–355 apple flavor, 16:197–234 apple fruit splitting & cracking, 19:217–262 apple germplasm, 29:1–61, 63–303 apple growth, 11:229–287 apple maturity indices, 13:407–432 apple scald, 27:227–267 apple, wild of Kazakhstan, 29:63–303, 305–315

509 apricot, origin & dissemination, 22:225–266 apricot, wild of Kazakhstan, 29–325–326 avocado flowering, 8:257–289 avocado rootstocks, 17:381–429 barberry, wild of Kazakhstan, 29:332–336 berry crop harvesting, 16:255–382 bilberry, wild of Kazakhstan, 29:347–348 blackberry, wild of Kazakhstan, 29:345 bloom delay, 15:97–144 blueberry developmental physiology, 13:339–405 blueberry harvesting, 16:257–282 blueberry nutrition, 10:183–227 bramble harvesting, 16:282–298 cactus, 18:302–309 carbohydrate reserves, 10:403–430 CA & MA for tropicals, 22:123–183 CA storage, 1:301–336 CA storage diseases, 3:412–461 cherry origin, 19:263–317 cherry, wild of Kazakhstan, 29:326–330 chilling injury, 15:145–182 chlorosis, 9:161–165 citrus abscission, 15:145–182 citrus cold hardiness, 7:201–238 citrus, culture of young trees, 24:319–372 citrus dwarfing by viroids, 24:277–317 citrus flowering, 12:349–408 citrus irrigation, 30:37–82 cotoneaster, wild of Kazakhstan, 29:316–317 cranberry, 21:215–249 cranberry harvesting, 16:298–311

cranberry, wild of Kazakhstan, 29:349 currant harvesting, 16:311–327 currant, wild of Kazakhstan, 29:341 deficit irrigation, 21:105–131 dormancy release, 7:239–300 elderberry, wild of Kazakhstan, 29:349–350 Ericaceae nutrition, 10:183–227 fertilization, 1:104–106 fig, industry, 12:409–490 fireblight, 11:423–474 flowering, 12:223–264 foliar nutrition, 6:287–355 frost control, 11:45–109 gooseberry, wild of Kazakhstan, 29:341–342 grape flower anatomy & morphology, 13:315–337 grape harvesting, 16:327–348 grape irrigation, 27:189–225 grape nitrogen metabolism, 14:407–452 grape pruning, 16:235–254, 336–340 grape root, 5:127–168 grape seedlessness, 11:164–176 grape, wild of Kazakhstan, 29:342–343 grapevine pruning, 16:235–254, 336–340 greenhouse, China, 30:149–158 honey bee pollination, 9:244–250, 254–256 jojoba, 17:233–266 in vitro culture, 7:157–200; 9:273–349 irrigation, deficit, 21:105–131 kiwifruit, 6:1–64; 12:307–347 lingonberry, 27:79–123 lingonberry, wild of Kazakhstan, 29:348–349 longan, 16:143–196 loquat, 23:233–276

510 Fruit crops (cont.) lychee, 16:143–196, 28:393–453 mountain ash, wild of Kazakhstan, 29:322–324 mulberry, wild of Kazakhstan, 29:350–351 muscadine grape breeding, 14:357–405 navel orange, 8:129–179 nectarine postharvest, 11:413–452 nondestructive postharvest quality evaluation, 20:1–119 nutritional ranges, 2:143–164 oleaster, wild of Kazakhstan, 29:351–353 olive salinity tolerance, 21:177–214 orange, navel, 8:129–179 orchard floor management, 9:377–430 peach origin, 17:331–379 peach postharvest, 11:413–452 peach thinning, 28:351–392 pear fruit disorders, 11:357–411; 27:227–267 pear maturity indices, 13:407–432 pear scald, 27:227–267 pear volatiles, 28:237–324 pear, wild of Kazakhstan, 29:315–316 pecan flowering, 8:217–255 photosynthesis, 11:111–157 Phytophthora control, 17:299–330 plum origin, 23:179–231 plum, wild of Kazakhstan, 29:330–332 pruning, 8:339–380 rambutan, 16:143–196 raspberry, 11:185–228 raspberry, wild of Kazakhstan, 29:343–345 roots, 2:453–457 rose, wild of Kazakhstan, 29:353–360 sapindaceous fruits, 16:143–196

CUMULATIVE SUBJECT INDEX sea buckthorn, wild of Kazakhstan, 29:361 short life & replant problem, 2:1–116 strawberry fruit growth, 17:267–297 strawberry harvesting, 16:348–365 strawberry, wild of Kazakhstan, 29:347 summer pruning, 9:351–375 Vaccinium nutrition, 10:183–227 vacciniums, wild of Kazakhstan, 29:347–349 viburnam, wild of Kazakhstan, 29:361–362 virus elimination, 28:187–236 water status, 7:301–344 Functional phytochemicals, fruit, 27:269–315 Fungi: fig, 12:451–474 mushroom, 6:85–118 mycorrhiza, 3:172–213; 10:211–212 pathogens in postharvest storage, 3:412–461 truffle cultivation, 16:71–107 Fungicide, & apple fruit set, 1:416 G Galanthus, 25:22–25 Garlic, CA storage, 1:375 Genetic variation: alternate bearing, 4:146–150 photoperiodic response, 4:82 pollution injury, 8:16–19 temperature-photoperiod interaction, 17:73–123 wild apple, 29:63–303 Genetics & breeding: aroids (edible), 8:72–75; 12:169 aroids (ornamental), 10:18–25 bean, bacterial resistance, 3:28–58 bloom delay in fruits, 15:98–107

bulbs, flowering, 18:119–123 cassava, 12:164 chestnut blight resistance, 8:313–321 citrus cold hardiness, 7:221–223 cranberry, 21:236–239 embryogenesis, 1:23 fig, 12:432–433 fire blight resistance, 1:435–436 flowering, 15:287–290, 303–305, 306–309, 314–315; 27:1–39, 41–77 flower longevity, 1:208–209 ginseng, 9:197–198 grafting use, 28:109–115 in vitro techniques, 9:318–324; 18:119–123 lettuce, 2:185–187 lingonberry, 27:108–111 loquat, 23:252–257 muscadine grapes, 14:357–405 mushroom, 6:100–111 navel orange, 8:150–156 nitrogen nutrition, 2:410–411 pineapple, 21:138–164 plant regeneration, 3:278–283 pollution insensitivity, 8:18–19 potato tuberization, 14:121–124 rhododendron, 12:54–59 sweet potato, 12:175 sweet sorghum, 21:87–90 tomato parthenocarpy, 6:69–70 tomato ripening, 13:77–98 tree short life, 2:66–70 Vigna, 2:311–394 waxes, 23:50–53 woody legume tissue & cell culture, 14:311–314 yam (Dioscorea), 12:183 Geophyte, see Bulb, Tuber Geranium, fertilization, 5:355–357 Germination, seed, 2:117–141, 173–174; 24:229–275

CUMULATIVE SUBJECT INDEX Germplasm: acquisition, apple, 29:1–61 characterization, apple, 29:45–56 cryopreservation, 6:357–372 in vitro, 5:261–264; 9:324–325 pineapple, 21:133–175 resources, apple, 29:1–61 Gibberellin: abscission, citrus, 15:166–167 bloom delay, 15:111–114 citrus, abscission, 15:166–167 cold hardiness, 11:63 dormancy, 7:270–271 floral promoter, 4:114 flowering, 15:219–293, 315–318 genetic regulation, 16:15 grape root, 5:150–151 mechanical stress, 17:19–20 Ginger postharvest physiology, 30:297–299 Ginseng, 9:187–236 Girdling, 1;416–417; 4:251–252, 30:1–26 Glucosinolates, 19:99–215 Gooseberry, wild of Kazakhstan, 29:341–342 Gourd, history, 25:71–171 Graft & grafting: herbaceous, 28:61–124 incompatibility, 15:183–232 phase change, 7:136–137, 141–142 rose, 9:56–57 Grape: CA storage, 1:308 chlorosis, 9:165–166 flower anatomy & morphology, 13:315–337 functional phytochemicals, 27:291–298 irrigation, 27:189–225 harvesting, 16:327–348 muscadine breeding, 14:357–405 nitrogen metabolism, 14:407–452

pollen morphology, 13:331–332 pruning, 16:235–254, 336–340 root, 5:127–168 seedlessness, 11:159–187 sex determination, 13:329–331 wild of Kazakhstan, 9:342–343 Gravitropism, 15:233–278 Greenhouse & greenhouse crops: carbon dioxide, 7:357–360, 544–545 China protected cultivation, 30:115–162 energy efficiency, 1:141–171; 9:1–52 growth substances, 7:399–481 nutrition & fertilization, 5:317–403 pest management, 13:1–66 vegetables, 21:1–39 Growth regulators, see Growth substances Growth substances, 2:60–66; 24:55–138, see also Abscisic acid, Auxin, Cytokinins, Ethylene, Gibberellins abscission, citrus, 15:157–176 apple bioregulation, 10:309–401 apple dwarfing, 3:315–375 apple fruit set, 1:417 apple thinning, 1:270–300 aroids, ornamental, 10:14–18 avocado fruit development, 10:229–243 bloom delay, 15:107–119 CA storage in vegetables, 1:346–348 cell cultures, 3:214–314 chilling injury, 15:77–83 citrus abscission, 15:157–176 cold hardiness, 7:223–225; 11:58–66 dormancy, 7:270–279 embryogenesis, 1:41–43; 2:277–281

511 floriculture, 7:399–481 flower induction, 4:190–195 flowering, 15:290–296 flower storage, 10:46–51 genetic regulation, 16:1–32 ginseng, 9:226 girdling, 20:1–26 grape seedlessness, 11:177–180 hormone reception, 26:49–84 in vitro flowering, 4:112–115 mechanical stress, 17:16–21 meristem & shoot-tip culture, 5:221–227 navel oranges, 8:146–147 pear bioregulation, 10:309–401 petal senescence, 3:76–78 phase change, 7:137–138, 142–143 raspberry, 11:196–197 regulation, 11:1–14 rose, 9:53–73 seedlessness in grape, 11:177–180 triazole, 10:63–105 H Haemanthus, 25:25–28 Halo blight of beans, 3:44–45 Hardiness, 4:250–251 Harvest: flower stage, 1:211–212 index, 7:72–74 lettuce, 2:176–181 mechanical of berry crops, 16:255–382 Hawthorne, wild of Kazakhstan, 29:317–322 Hazelnut. See Filbert wild of Kazakhstan, 29:365–366 Health phytochemicals: fruit, 27:269–315 vegetables, 28:125–185 Heat treatment (postharvest), 22:91–121 Heliconia, 14:1–55 Herbaceous plants, subzero stress, 6:373–417 Hippeastrum, 25:29–34

512 Histochemistry: flower induction, 4:177–179 fruit abscission, 1:172–203 Histology, flower induction, 4:179–184, see also Anatomy & morphology Honey bee, 9:237–272 Honeysuckle, wild of Kazakhstan, 29:350 Horseradish, CA storage, 1:368 Hydrolases, 5:169–219 Hydroponic culture, 5:1–44; 7:483–558 Hymenocallis, 25:59 Hypovirulence, in Endothia parasitica, 8:299–310 I Ismene, 25:59 Ice, formation & spread in tissues, 13:215–255 Ice-nucleating bacteria, 7:210–212; 13:230–235 Industrial crops, cactus, 18:309–312 Insects & mites: aroids, 8:65–66 avocado pollination, 8:275–277 fig, 12:442–447 hydroponic crops, 7:530–534 integrated pest management, 13:1–66 lettuce, 2:197–198 ornamental aroids, 10:18 tree short life, 2:52 tulip, 5:63, 92 waxes, 23:1–68 Integrated pest management, greenhouse crops, 13:1–66 In vitro: abscission, 15:156–157 apple propagation, 10:325–326 aroids, ornamental, 10:13–14 artemisia, 19:342–345 bioreactor technology, 24:1–30 bulbs, flowering, 18:87–169

CUMULATIVE SUBJECT INDEX cassava propagation, 13:121–123; 26:99–119 cellular salinity tolerance, 16:33–69 cold acclimation, 6:382 cryopreservation, 6:357–372 embryogenesis, 1:1–78; 2:268–310; 7:157–200; 10:153–181 environmental control, 17:123–170 flowering bulbs, 18:87–169 flowering, 4:106–127 pear propagation, 10:325–326 phase change, 7:144–145 propagation, 3:214–314; 5:221–277; 7:157–200; 9:57–58, 273–349; 17:125–172 thin cell layer morphogenesis, 14:239–264 woody legume culture, 14:265–332 Iron: deficiency & toxicity symptoms in fruits & nuts, 2:150 deficiency chlorosis, 9:133–186 Ericaceae nutrition, 10:193–195 foliar application, 6:330 nutrition, 5:324–325 pine bark media, 9:123 Irrigation: citrus, 30:37–82 deficit, deciduous orchards, 21:105–131 drip or trickle, 4:1–48 frost control, 11:76–82 fruit trees, 7:331–332 grape, 27:189–225 grape root growth, 5:140–141 lettuce industry, 2:175 navel orange, 8:161–162 root growth, 2:464–465 J Jojoba, 17:233–266 Juvenility, 4:111–112 pecan, 8:245–247

tulip, 5:62–63 woody plants, 7:109–155 K Kale, fluid drilling of seed, 3:21 Kazakhstan, see Wild fruits & nuts Kiwifruit: botany, 6:1–64 vine growth, 12:307–347 L Lamps, for plant growth, 2:514–531 Lanzon, CA & MA, 22:149 Leaves: apple morphology, 12:283–288 flower induction, 4:188–189 Leek: CA storage, 1:375 fertilization, 1:118 Leguminosae, in vitro, 5:227–229; 14:265–332 Lemon, rootstock, 1:244– 246, see also Citrus Lettuce: CA storage, 1:369–371 classification, 28:25–27 fertilization, 1:118 fluid drilling of seed, 3:14–17 industry, 2:164–207 seed germination, 24:229–275 tipburn, 4:49–65 Leucojum, 25:34–39 Leucospermum, 22:27–90 Light: fertilization, greenhouse crops, 5:330–331 flowering, 15:282–287, 310–312 fruit set, 1:412–413 lamps, 2:514–531 nitrogen nutrition, 2:406–407 orchards, 2:208–267 ornamental aroids, 10:4–6 photoperiod, 4:66–105 photosynthesis, 11:117–121 plant growth, 2:491–537 tolerance, 18:215–246

CUMULATIVE SUBJECT INDEX Lingonberry, 27:79–123 wild of Kazakhstan, 29:348–349 Longan, see also Sapindaceous fruits CA & MA, 22:150 Loquat: botany & horticulture, 23:233–276 CA & MA, 22:149–150 Lychee, see also Sapindaceous fruits CA & MA, 22:150 flowering, 28:397–421 fruit abscission, 28–437–443 fruit development, 28:433–436 pollination, 28:422–428 reproductive biology, 28:393–453 Lycoris, 25:39–43 M Magnesium: container growing, 9:84–85 deficiency & toxicity symptoms in fruits & nuts, 2:148 Ericaceae nutrition, 10:196–198 foliar application, 6:331 nutrition, 5:323 pine bark media, 9:117–119 Magnetic resonance imaging, 20:78–86, 225–266 Male sterility, temperaturephotoperiod induction, 17:103–106 Mandarin, rootstock, 1:250–252 Manganese: deficiency & toxicity symptoms in fruits & nuts, 2:150–151 Ericaceae nutrition, 10:189–193 foliar application, 6:331 nutrition, 5:235–326 pine bark media, 9:123–124 Mango: alternate bearing, 4:145–146 asexual embryogenesis, 7:171–173

CA & MA, 22:151–157 CA storage, 1:313 in vitro culture, 7:171–173 Mangosteen, CA & MA, 22:157 Mechanical harvest, berry crops, 16:255–382 Mechanical stress regulation, 17:1–42 Media: fertilization, greenhouse crops, 5:333 pine bark, 9:103–131 Medicinal crops: artemisia, 19:319–371 poppy, 19:373–408 Melon grafting, 28:96–98 Meristem culture, 5:221–277 Metabolism: flower, 1:219–223 nitrogen in citrus, 8:181–215 seed, 2:117–141 Micronutrients: container growing, 9:85–87 pine bark media, 9:119–124 Micropropagation, see also In vitro; propagation: bulbs, flowering, 18:89–113 environmental control, 17:125–172 nuts, 9:273–349 rose, 9:57–58 temperate fruits, 9:273–349 tropical fruits & palms, 7:157–200 Microtu, see Vole Modified atmosphere (MA) for tropical fruits, 22:123–183 Moisture& seed storage, 2:125–132 Molecular biology: cassava, 26:85–159 floral induction, 27:3–20 flowering, 27:1–39;41–77 hormone reception, 26:49–84 Molybdenum nutrition, 5:328–329 Monocot, in vitro, 5:253–257 Monstera, see Aroids, ornamental

513 Morphology: navel orange, 8:132–133 orchid, 5:283–286 pecan flowering, 8:217–243 red bayberry, 30: 92–96 Moth bean, genetics, 2:373–374 Mountain ash, wild of Kazakhstan, 29:322–324 Mulberry, wild of Kazakhstan, 29:350–351 Multiple cropping, 30:355–500 Mung bean, genetics, 2:348–364 Mushroom: CA storage, 1:371–372 cultivation, 19:59–97 spawn, 6:85–118 Muskmelon, fertilization, 1:118–119 Mycoplasma-like organisms, tree short life, 2:50–51 Mycorrhizae: container growing, 9:93 Ericaceae, 10:211–212 fungi, 3:172–213 grape root, 5:145–146 Myrica, see Red baybery N Narcissus, 25:43–48 Navel orange, 8:129–179 Nectarine: bloom delay, 15:105–106 CA storage, 1:309–310 postharvest physiology, 11:413–452 Nematodes: aroids, 8:66 fig, 12:475–477 lettuce, 2:197–198 tree short life, 2:49–50 Nerine, 25:48–56 NFT (nutrient film technique), 5:1–44 Nitrogen: CA storage, 8:116–117 container growing, 9:80–82 deficiency & toxicity symptoms in fruits & nuts, 2:146 Ericaceae nutrition, 10:198–202

514 Nitrogen (cont.) fixation in woody legumes, 14:322–323 foliar application, 6:332 in embryogenesis, 2:273–275 metabolism in apple, 4:204–246 metabolism in citrus, 8:181–215 metabolism in grapevine, 14:407–452 nutrition, 2:395, 423; 5:319–320 pine bark media, 9:108–112 trickle irrigation, 4:29–30 vegetable crops, 22:185–223 Nomenclature, 28:1–60 Nondestructive quality evaluation of fruits & vegetables, 20:1–119 Nursery crops: fertilization, 1:106–112 nutrition, 9:75–101 Nut crops, see also Individual crop almond postharvest technology & utilization, 20:267–311 almond, wild of Kazakhstan, 29:262–265 chestnut blight, 8:291–336 fertilization, 1:106 hazelnut, wild of Kazakhstan, 29:365–366 honey bee pollination, 9:250–251 in vitro culture, 9:273–349 nutritional ranges, 2:143–164 pine, wild of Kazakhstan, 29:368–369 pistachio culture, 3:376–396 pistachio, wild of Kazakhstan, 29:366–368 walnut, wild of Kazakhstan, 29:369–370 Nutrient: concentration in fruit & nut crops, 2:154–162 film technique, 5:1–44 foliar-applied, 6:287–355 media, for asexual embryogenesis, 2:273–281

CUMULATIVE SUBJECT INDEX media, for organogenesis, 3:214–314 plant & tissue analysis, 7:30–56 solutions, 7:524–530 uptake, in trickle irrigation, 4:30–31 Nutrition (human): aroids, 8:79–84 CA storage, 8:101–127 phytochemicals in fruit, 27:269–315 phytochemicals in vegetables, 28:125–185 steroidal alkaloids, 25:171–196 Nutrition (plant): air pollution, 8:22–23, 26 blueberry, 10:183–227 calcifuge, 10:183–227 cold hardiness, 3:144–171 container nursery crops, 9:75–101 cranberry, 21:234–235 ecologically based, 24:156–172 embryogenesis, 1:40–41 Ericaceae, 10:183–227 fire blight, 1:438–441 foliar, 6:287–355 fruit & nut crops, 2:143–164 ginseng, 9:209–211 greenhouse crops, 5:317–403 kiwifruit, 12:325–332 mycorrhizal fungi, 3:185–191 navel orange, 8:162–166 nitrogen in apple, 4:204–246 nitrogen in vegetable crops, 22:185–223 nutrient film techniques, 5:18–21, 31–53 ornamental aroids, 10:7–14 pine bark media, 9:103–131 raspberry, 11:194–195 slow-release fertilizers, 1:79–139 O Oil palm: asexual embryogenesis, 7:187–188

in vitro culture, 7:187–188 Okra: botany & horticulture, 21:41–72 CA storage, 1:372–373 Oleaster, wild of Kazakhstan, 29:351–353 Olive: alternate bearing, 4:140–141 salinity tolerance, 21:177–214 processing technology, 25:235–260 Onion: CA storage, 1:373–375 fluid drilling of seed, 3:17–18 Opium poppy, 19:373–408 Orange, see also Citrus alternate bearing, 4:143–144 sour, rootstock, 1:242–244 sweet, rootstock, 1:252–253 trifoliate, rootstock, 1:247–250 Orchard & orchard systems: floor management, 9:377–430 light, 2:208–267 root growth, 2:469–470 water, 7:301–344 Orchid: fertilization, 5:357–358 pollination regulation of flower development, 19:28–38 physiology, 5:279–315 Organogenesis, 3:214–314, see also In vitro; tissue culture Ornamental plants, see also individual plant Amaryllidaceae Banksia, 22:1–25 cactus grafting, 28–106–109 chlorosis, 9:168–169 cotoneaster, wild of Kazakhstan, 29:316–317 fertilization, 1:98–104, 106–116 flowering bulb roots, 14:57–88 flowering bulbs in vitro, 18:87–169

CUMULATIVE SUBJECT INDEX foliage acclimatization, 6:119–154 heliconia, 14:1–55 honeysuckle, wild of Kazakhstan, 29:350 Leucospermum, 22:27–90 oleaster, wild of Kazakhstan, 29:351–353 orchid pollination regulation, 19:28–38 poppy, 19:373–408 protea leaf blackening, 17:173–201 rhododendron, 12:1–42 rose, wild of Kazakhstan, 29:353–360 viburnam, wild of Kazakhstan, 29:361–362 P Paclobutrazol, see Triazole Papaya: asexual embryogenesis, 7:176–177 CA & MA, 22:157–160 CA storage, 1:314 in vitro culture, 7:175–178 Parsley: CA storage, 1:375 drilling of seed, 3:13–14 Parsnip, fluid drilling of seed, 3:13–14 Parthenocarpy, tomato, 6:65–84 Passion fruit: in vitro culture, 7:180–181 CA & MA, 22:160–161 Pathogen elimination, in vitro, 5:257–261 Peach: bloom delay, 15:105–106 CA storage, 1:309–310 origin, 17:333–379 postharvest physiology, 11:413–452 short life, 2:4 summer pruning, 9:351–375 thinning, 28:351–392 wooliness, 20:198–199 Peach palm (Pejibaye): in vitro culture, 7:187–188 Pear: bioregulation, 10:309–401 bloom delay, 15:106–107 CA storage, 1:306–308 decline, 2:11

fire blight control, 1:423–474 fruit disorders, 11:357–411; 27:227–267 fruit volatiles, 28:237–324 in vitro, 9:321 maturity indices, 13:407–432 root distribution, 2:456 scald, 27:227–267 short life, 2:6 wild of Kazakhstan, 29:315–316 Pecan: alternate bearing, 4:139–140 fertilization, 1:106 flowering, 8:217–255 in vitro culture, 9:314–315 Pejibaye, in vitro culture, 7:189 Pepper (Capsicum): CA storage, 1:375–376 fertilization, 1:119 fluid drilling in seed, 3:20 grafting, 28:104–105 phytochemicals, 28:161–162 Persimmon: CA storage, 1:314 quality, 4:259 Pest control: aroids (edible), 12:168–169 aroids (ornamental), 10:18 cassava, 12:163–164 cowpea, 12:210–213 ecologically based, 24:172–201 fig, 12:442–477 fire blight, 1:423–474 ginseng, 9:227–229 greenhouse management, 13:1–66 hydroponics, 7:530–534 sweet potato, 12:173–175 vertebrate, 6:253–285 yam (Dioscorea), 12:181–183 Petal senescence, 11:15–43 pH: container growing, 9:87–88 fertilization greenhouse crops, 5:332–333 pine bark media, 9:114–117

515 soil testing, 7:8–12, 19–23 Phase change, 7:109–155 Phenology: apple, 11:231–237 raspberry, 11:186–190 Philodendron , see Aroids, ornamental Phosphonates, Phytophthora control, 17:299–330 Phosphorus: container growing, 9:82–84 deficiency & toxicity symptoms in fruits & nuts, 2:146–147 nutrition, 5:320–321 pine bark media, 9:112–113 trickle irrigation, 4:30 Photoautotrophic micropropagation, 17:125–172 Photoperiod, 4:66–105, 116–117; 17:73–123 flowering, 15:282–284, 310–312 Photosynthesis: cassava, 13:112–114 efficiency, 7:71–72; 10:378 fruit crops, 11:111–157 ginseng, 9:223–226 light, 2:237–238 Physiology, see also Postharvest physiology bitter pit, 11:289–355 blueberry development, 13:339–405 cactus reproductive biology, 18:321–346 calcium, 10:107–152 carbohydrate metabolism, 7:69–108 cassava, 13:105–129 citrus cold hardiness, 7:201–238 citrus irrigation, 30:55–67 conditioning 13:131–181 cut flower, 1:204–236; 3:59–143; 10:35–62 desiccation tolerance, 18:171–213 disease resistance, 18:247–289 dormancy, 7:239–300 embryogenesis, 1:21–23; 2:268–310

516 Physiology (cont.) floral scents, 24:31–53 flower development, 19:1–58 flowering, 4:106–127 fruit ripening, 13:67–103 fruit softening, 10:107–152 ginseng, 9:211–213 girdling, 30: 1–26 glucosinolates, 19:99–215 grafting, 28:78–84 heliconia, 14:5–13 hormone reception, 26:49–84 juvenility, 7:109–155 lettuce seed germination, 24:229–275 light tolerance, 18:215–246 loquat, 23:242–252 lychee reproduction, 28:393–453 male sterility, 17:103–106 mechanical stress, 17:1–42 nitrogen metabolism in grapevine, 14:407–452 nutritional quality & CA storage, 8:118–120 olive salinity tolerance, 21:177–214 orchid, 5:279–315 petal senescence, 11:15–43 photoperiodism, 17:73–123 pollution injury, 8:12–16 polyamines, 14:333–356 potato tuberization, 14:89–188 pruning, 8:339–380 raspberry, 11:190–199 red bayberry, 30:96–99 regulation, 11:1–14 root pruning, 6:158–171 roots of flowering bulbs, 14:57–88 rose, 9:3–53 salinity hormone action, 16:1–32 salinity tolerance, 16:33–69 seed, 2:117–141 seed priming, 16:109–141 strawberry flowering, 28:28:325–349 subzero stress, 6:373–417

CUMULATIVE SUBJECT INDEX summer pruning, 9:351–375 sweet potato, 23:277–338 thin cell layer morphogenesis, 14:239–264 tomato fruit ripening, 13:67–103 tomato parthenocarpy, 6:71–74 triazoles, 10:63–105; 24:55–138 tulip, 5:45–125 vernalization, 17:73–123 volatiles, 17:43–72 watercore, 6:189–251 water relations cut flowers, 18:1–85 waxes, 23:1–68 Phytochemicals, functional: fruits, 27:269–315 vegetables, 28:125–185 Phytohormones. see Growth substances Phytophthora control, 17:299–330 Phytotoxins, 2:53–56 Pigmentation: flower, 1:216–219 rose, 9:64–65 Pinching, by chemicals, 7:453–461 Pine, wild of Kazakhstan, 29:368–369 Pineapple: CA & MA, 22:161–162 CA storage, 1:314 genetic resources, 21:138–141 in vitro culture, 7:181–182 Pine bark, potting media, 9:103–131 Pistachio: alternate bearing, 4:137–139 culture, 3:376–393 in vitro culture, 9:315 wild of Kazakhstan, 29:366–368 Plantain: CA & MA, 22:141–146 in vitro culture, 7:178–180 Plant: classification, 28:1–60 protection, short life, 2:79–84

systematics, 28:1–60 Plastic cover, sod production, 27:317–351 Plum: CA storage, 1:309 origin, 23:179–231 wild of Kazakhstan, 29:330–332 Poinsettia, fertilization, 1:103–104; 5:358–360 Pollen, desiccation tolerance, 18:195 Pollination: apple, 1:402–404 avocado, 8:272–283 cactus, 18:331–335 embryogenesis, 1:21–22 fig, 12:426–429 floral scents, 24:31–53 flower regulation, 19:1–58 fruit crops, 12:223–264 fruit set, 4:153–154 ginseng, 9:201–202 grape, 13:331–332 heliconia, 14:13–15 honey bee, 9:237–272 kiwifruit, 6:32–35 lychee, 28:422–428 navel orange, 8:145–146 orchid, 5:300–302 petal senescence, 11:33–35 protection, 7:463–464 rhododendron, 12:1–67 Pollution, 8:1–42 Polyamines, 14:333–356 chilling injury, 15:80 Polygalacturonase, 13:67–103 Poppy, opium, 19:373–408 Postharvest physiology: almond, 20:267–311 apple bitter pit, 11:289–355 apple maturity indices, 13:407–432 apple scald, 27:227–257 apple weight loss, 25:197–234 aroids, 8:84–86 asparagus, 12:69–155 CA for tropical fruit, 22:123–183 CA for storage & quality, 8:101–127 carrot storage: 30:284–288

CUMULATIVE SUBJECT INDEX cassava storage, 30:288–295 chlorophyll fluorescence, 23:69–107 coated fruits & vegetables, 26:161–238 cut flower, 1:204–236; 3:59–143; 10:35–62 foliage plants, 6:119–154 fresh-cut fruits & vegetables, 30:85–255 fruit, 1:301–336 fruit softening, 10:107–152 ginger storage, 30:297–299 Jerusalem artichoke storage, 30:271–276 heat treatment, 22:91–121 lettuce, 2:181–185 low-temperature sweetening, 17:203–231, 30:317–355 MA for tropical fruit, 22:123–183 navel orange, 8:166–172 nectarine, 11:413–452 nondestructive quality evaluation, 20:1–119 pathogens, 3:412–461 peach, 11:413–452 pear disorders, 11:357–411; 7:227–267 pear maturity indices, 13:407–432 pear scald, 27:227–257 petal senescence, 11:15–43 potato low temperature sweetening, 30:317–355 potato storage, 30:259–271 protea leaf blackening, 17:173–201 quality evaluation, 20:1–119 scald, 27:227–267 seed, 2:117–141 sweet potato storage, 30:276–284 texture in fresh fruit, 20:121–244 taro storage, 30:295–297 tomato fruit ripening, 13:67–103 vegetables, 1:337–394 watercore, 6:189–251; 11:385–387

Potassium: container growing, 9:84 deficiency & toxicity symptoms in fruits & nuts, 2:147–148 foliar application, 6:331–332 nutrition, 5:321–322 pine bark media, 9:113–114 trickle irrigation, 4:29 Potato: CA storage, 1:376–378 classification, 28:23–26 fertilization, 1:120–121 low temperature sweetening, 17:203–231; 30:317–353 phytochemicals, 28:160–161 postharvest physiology & storage, 259–271 tuberization, 14:89–198 Processing, table olives, 25:235–260 Propagation, see also In vitro apple, 10:324–326; 12:288–295 aroids, ornamental, 10:12–13 bioreactor technology, 24:1–30 cassava, 13:120–123 floricultural crops, 7:461–462 ginseng, 9:206–209 orchid, 5:291–297 pear, 10:324–326 rose, 9:54–58 tropical fruit, palms 7:157–200 woody legumes in vitro, 14:265–332 Protaceous flower crop, see also Protea Banksia, 22:1–25 Leucospermum, 22:27–90 Protea, leaf blackening, 17:173–201 Protected crops, carbon dioxide, 7:345–398 Protoplast culture, woody species, 10:173–201 Pruning, 4:161; 8:339–380 apple, 9:351–375 apple training, 1:414

517 chemical, 7:453–461 cold hardiness, 11:56 fire blight, 1:441–442 grapevines, 16:235–254 light interception, 2:250–251 peach, 9:351–375 phase change, 7:143–144 root, 6:155–188 Prunus, see also Almond; Cherry; Nectarine; Peach; Plum in vitro, 5:243–244; 9:322 root distribution, 2:456 Pseudomonas: phaseolicola, 3:32–33, 39, 44–45 solanacearum, 3:33 syringae, 3:33, 40; 7:210–212 Pumpkin, history, 25:71–170 Q Quality evaluation: fruits & vegetables, 20:1–119, 121–224 nondestructive, 20:1–119 texture in fresh fruit, 20:121–224 R Rabbit, 6:275–276 Radish, fertilization, 1:121 Rambutan. see Sapindaceous fruits CA & MA, 22:163 Raspberry: harvesting, 16:282–298 productivity, 11:185–228 wild of Kazakhstan, 29:343–345 Red bayberry, 30:83–113 Rejuvenation: rose, 9:59–60 woody plants, 7:109–155 Replant problem, deciduous fruit trees, 2:1–116 Respiration: asparagus postharvest, 12:72–77 fruit in CA storage, 1:315–316 kiwifruit, 6:47–48 vegetables in CA storage, 1:341–346 Rhizobium, 3:34, 41

518 Rhododendron, 12:1–67 Rice bean, genetics, 2:375–376 Root: apple, 12:269–272 cactus, 18:297–298 diseases, 5:29–31 environment, nutrient film technique, 5:13–26 Ericaceae, 10:202–209 grape, 5:127–168 kiwifruit, 12:310–313 physiology of bulbs, 14:57–88 pruning, 6:155–188 raspberry, 11:190 rose, 9:57 tree crops, 2:424–490 Root & tuber crops: Amaryllidaceae, 25:1–79 aroids, 8:43–99; 12:166–170 carrot postharvest physiology, 30:284–288 cassava crop physiology, 13:105–129 cassava molecular biology, 26:85–159 cassava multiple cropping, 30:355–50 cassava postharvest physiology, 30:288–295 cassava root crop, 12:158–166 low-temperature sweetening, 17:203–231, 30:317 -354 minor crops, 12:184–188 potato low temperature sweetening, 30:317–354 potato tuberization, 14:89–188 sweet potato, 12:170–176 sweet potato physiology, 23:277–338 sweet potato postharvest physiology, 30:276–284 taro postharvest physiology, 30:295–297 yam (Dioscorea), 12:177–184 Rootstocks: alternate bearing, 4:148 apple, 1:405–407; 12:295–297 avocado, 17:381–429

CUMULATIVE SUBJECT INDEX citrus, 1:237–269 cold hardiness, 11:57–58 fire blight, 1:432–435 light interception, 2:249–250 navel orange, 8:156–161 root systems, 2:471–474 stress, 4:253–254 tree short life, 2:70–75 Rosaceae, in vitro, 5:239–248 Rose: fertilization, 1:104; 5:361–363 growth substances, 9:3–53 in vitro, 5:244–248 wild of Kazakhstan, 29:353–360 S Salinity: air pollution, 8:25–26 citrus irrigation, 30:37–83 olive, 21:177–214 soils, 4:22–27 tolerance, 16:33–69 Sapindaceous fruits, 16:143–196 Sapodilla, CA & MA, 22:164 Scadoxus, 25:25–28 Scald, apple & pear, 27:227–265 Scoring & fruit set, 1:416–417 Sea buckthorn, wild of Kazakhstan, 29:361 Seed: abortion, 1:293–294 apple anatomy & morphology, 10:285–286 conditioning, 13:131–181 desiccation tolerance, 18:196–203 environmental influences on size & composition, 13:183–213 flower induction, 4:190–195 fluid drilling, 3:1–58 grape seedlessness, 11:159–184 kiwifruit, 6:48–50 lettuce, 2:166–174 lettuce germination, 24:229–275

priming, 16:109–141 rose propagation, 9:54–55 vegetable, 3:1–58 viability & storage, 2:117–141 Secondary metabolites, woody legumes, 14:314–322 Senescence: chlorophyll senescence, 23:88–93 cut flower, 1:204–236; 3:59–143; 10:35–62; 18:1–85 petal, 11:15–43 pollination-induced, 19:4–25 rose, 9:65–66 whole plant, 15:335–370 Sensory quality: CA storage, 8:101–127 Shoot-tip culture, 5:221–277, see also Micropropagation Short life problem, fruit crops, 2:1–116 Signal transduction, 26:49–84 Small fruit, CA storage, 1:308 Snapdragon fertilization, 5:363–364 Sod production, 27:317–351 Sodium, deficiency & toxicity symptoms in fruits & nuts, 2:153–154 Soil: grape root growth, 5:141–144 management & root growth, 2:465–469 orchard floor management, 9:377–430 plant relations, trickle irrigation, 4:18–21 stress, 4:151–152 testing, 7:1–68; 9:88–90 zinc, 23:109–178 Soilless culture, 5:1–44 Solanaceae: in vitro, 5:229–232 steroidal alkaloids, 25:171–196 Somatic embryogenesis. See Asexual embryogenesis Sorghum, sweet, 21:73–104

CUMULATIVE SUBJECT INDEX Spathiphyllum, see Aroids, ornamental Squash, history, 25:71–170 Stem, apple morphology, 12:272–283Sternbergia, 25:59 Steroidal alkaloids, solanaceous, 25:171–196 Storage, see also Postharvest physiology, Controlledatmosphere (CA) storage carrot postharvest physiology, 30:284–288 cassava postharvest physiology, 30: 288–295 cut flower, 3:96–100; 10:35–62 ginger postharvest physiology, 30:297–299 Jerusalem artichoke postharvest physiology, 30:259–271 low temperature sweetening, 17:203–231; 30:317–354 potato low temperature sweetening, 30–317–353 potato postharvedst physiology, 30:259–271 root & tuber crops, 30:253–316 rose plants, 9:58–59 seed, 2:117–141 sweetpotato postharvest physiology, 30:295–297 taro postharvest physiology, 30:295–297 Strawberry: fertilization, 1:106 flowering, 28:325–349 fruit growth & ripening, 17:267–297 functional phytonutrients, 27:303–304 harvesting, 16:348–365 in vitro, 5:239–241 wild of Kazakhstan, 29:347 Stress: benefits of, 4:247–271 chlorophyll fluorescence, 23:69–107 climatic, 4:150–151 flooding, 13:257–313

mechanical, 17:1–42 petal, 11:32–33 plant, 2:34–37 protectants (triazoles), 24:55–138 protection, 7:463–466 salinity tolerance in olive, 21:177–214 subzero temperature, 6:373–417 waxes, 23:1–68 Sugar, see also Carbohydrate allocation, 7:74–94 flowering, 4:114 Sugar apple, CA & MA, 22:164 Sugar beet, fluid drilling of seed, 3:18–19 Sulfur: deficiency & toxicity symptoms in fruits 7 nuts, 2:154 nutrition, 5:323–324 Sweet potato: culture, 12:170–176 fertilization, 1:121 physiology, 23:277–338 postharvest physiology & storage, 30:276–284 Sweet sop, CA & MA, 22:164 Symptoms, deficiency & toxicity symptoms in fruits & nuts, 2:145–154 Syngonium, see Aroids, ornamental Systematics, 28:1–60 T Taro, see Aroids, edible postharvest physiology & storage, 30:276–284 Taxonomy, 28:1–60 Tea, botany & horticulture, 22:267–295 Temperature: apple fruit set, 1:408–411 bloom delay, 15:119–128 CA storage of vegetables, 1:340–341 chilling injury, 15:67–74 cryopreservation, 6:357–372 cut flower storage, 10:40–43 fertilization, greenhouse crops, 5:331–332

519 fire blight forecasting, 1:456–459 flowering, 15:284–287, 312–313 interaction with photoperiod, 4:80–81 low temperature sweetening, 17:203–231 navel orange, 8:142 nutrient film technique, 5:21–24 photoperiod interaction, 17:73–123 photosynthesis, 11:121–124 plant growth, 2:36–37 seed storage, 2:132–133 subzero stress, 6:373–417 Texture in fresh fruit, 20:121–224 Thinning: apple, 1:270–300 peach & Prunus, 28:351–392 Tipburn, in lettuce, 4:49–65 Tissue: see also In vitro culture 1:1–78; 2:268–310; 3:214–314; 4:106–127; 5:221–277; 6:357–372; 7:157–200; 8:75–78; 9:273–349; 10:153–181, 24:1–30 cassava, 26:85–159 dwarfing, 3:347–348 nutrient analysis, 7:52–56; 9:90 Tomato: CA storage, 1:380–386 classification, 28:21–23 chilling injury, 20:199–200 fruit cracking, 30:163–184 fertilization, 1:121–123 fluid drilling of seed, 3:19–20 fruit ripening, 13:67–103 galacturonase, 13:67–103 grafting, 28:98–103 greenhouse quality, 26:239 parthenocarpy, 6:65–84 phytochemicals, 28:160 Toxicity symptoms in fruit & nut crops, 2:145–154 Transport, cut flowers, 3:100–104

520 Tree decline, 2:1–116 Triazoles, 10:63–105; 24:55–138 chilling injury, 15:79–80 Trickle irrigation, 4:1–48 Truffle cultivation, 16:71–107 Tuber, potato, 14:89–188 Tuber & root crops. See Root & tuber crops Tulip, see also Bulb fertilization, 5:364–366 in vitro, 18:144–145 physiology, 5:45–125 Tunnel (cloche), 7:356–357 Turfgrass, fertilization, 1:112–117 Turnip, fertilization, 1:123–124 Turnip Mosaic Virus, 14:199–238 U Urd bean, genetics, 2:364–373 Urea, foliar application, 6:332 V Vaccinium, 10:185–187, see also Blueberry; Cranberry; Lingonberry functional phytonutrients, 27:303 wild of Kazakhstan, 29:347–349 Vase solutions, 3:82–95; 10:46–51 Vegetable crops, see also Specific crop Allium phytochemicals, 28:156–159 aroids, 8:43–99; 12:166–170 asparagus postharvest, 12:69–155 cactus, 18:300–302 carrot postharvest physiology & storage, 30:284–288 cassava:crop physiology, 13:105–129 cassava molecular biology, 26:85–159 cassava multiple cropping, 30:355–50

CUMULATIVE SUBJECT INDEX cassava postharvest physiology & storage, 30:288–295 cassava root crop, 12:158–166 CA storage, 1:337–394 CA storage & quality, 8:101–127 CA storage diseases, 3:412–461 caper bush, 27:125–188 chilling injury, 15:63–95 coating physiology, 26:161–238 crucifer phytochemicals, 28:150–156 cucumber grafting, 28:91–96 ecologically based, 24:139–228 eggplant grafting, 28:103–104 eggplant phytochemicals, 28:162–163 fertilization, 1:117–124 fluid drilling of seeds, 3:1–58 fresh cut, 30:185–251 ginger postharvest physiology & storage, 30:297–299 gourd history, 25:71–170 grafting, 28:61–124 greenhouses in China, 30:126–141 greenhouse management, 21:1–39 greenhouse pest management, 13:1–66 honey bee pollination, 9:251–254 hydroponics, 7:483–558 Jerusalem artichoke postharvest physiology &; storage, 30:271–276 lettuce seed germination, 24:229–275 low-temperature sweetening, 17:203–231 melon grafting, 28:96–98 minor root & tubers, 12:184–188 mushroom cultivation, 19:59–97 mushroom spawn, 6:85–118

N nutrition, 22:185–223 nondestructive postharvest quality evaluation, 20:1–119 okra, 21:41–72 pepper phytochemicals, 28:161–162 phytochemicals, 28:125–185 potato low temperature sweetening, 30:317–353 potato postharvest physiology & storage, 30:271–276 potato phytochemicals, 28:160–161 potato tuberization, 14:89–188 pumpkin history, 25:71–170 root & tuber postharvest & storage, 30: 295–297 seed conditioing, 13:131–181 seed priming, 16:109–141 squash history, 25:71–170 steroidal alkaloids, Solanaceae, 25:171–196 sweet potato, 12:170–176 sweet potato physiology, 23:277–338 tomato (greenhouse) fruit cracking, 30:163–184 tomato fruit ripening, 13:67–103 tomato (greenhouse) quality: 26:239–319 tomato parthenocarpy, 6:65–84 tomato phytochemicals, 28:160 tropical production, 24:139–228 truffle cultivation, 16:71–107 watermelon grafting, 28:86–91 yam (Dioscorea), 12:177–184 Vegetative tissue, desiccation tolerance, 18:176–195 Vernalization, 4:117; 15:284–287; 17:73–123 Vertebrate pests, 6:253–285

CUMULATIVE SUBJECT INDEX Viburnam, wild of Kazakhstan, 29:361–362 Vigna, see also Cowpea genetics, 2:311–394 U.S. production, 12:197–222 Viroid, dwarfing for citrus, 24:277–317 Virus: benefits in horticulture, 3:394–411 dwarfing for citrus, 24:277–317 elimination, 7:157–200; 9:318; 18:113–123; 28:187–236 fig, 12:474–475 tree short life, 2:50–51 turnip mosaic, 14:199–238 Volatiles, 17:43–72; 24:31–53; 28:237–324 Vole, 6:254–274 W Walnut: in vitro culture, 9:312 wild of Kazakhstan, 29:369–370 Water relations: cut flower, 3:61–66; 18:1–85 citrus, 30:37–83 deciduous orchards, 21:105–131 desiccation tolerance, 18:171–213 fertilization, grape & grapevine, 27:189–225 kiwifruit, 12:332–339 light in orchards, 2:248–249

photosynthesis, 11:124–131 trickle irrigation, 4:1–48 Watercore, 6:189–251 apple, 6:189–251 pear, 11:385–387 Watermelon: fertilization, 1:124 grafting, 28:86–91 Wax apple, CA & MA, 22:164 Waxes, 23:1–68 Weed control, ginseng, 9:228–229 Weeds: lettuce research, 2:198 virus, 3:403 Wild fruit & nuts of Kazakhstan, 29:305–371 almond, 29:262–265 apple, 29:63–303, 305–315 apricot, 29:325–326 barberry, 29:332–336 bilberry, 29:347–348 blackberry, 29:345 cherry, 29:326–330 cotoneaster, 29:316–317 cranberry, 29:349 currant, 29:341 elderberry, 29:349–350 gooseberry, 29:341–342 grape, 29:342–343 hazelnut, 29:365–366 lingonberry, 29:348–349 mountain ash, 29:322–324 mulberry, 29:350–351 oleaster, 29:351–353 pear, 29:315–316 pine, 29:368–369 pistachio, 29:366–368 plum, 29:330–332 raspberry, 29:343–345

521 rose, 29:353–360 sea buckthorn, 29:361 strawberry, 29:347 vacciniums, 29:347–349 viburnam, 29:361–362 walnut, 29:369–370 Woodchuck, 6:276–277 Woody species, somatic embryogenesis, 10:153–181 X Xanthomonas phaseoli, 3:29–32, 41, 45–46 Xanthophyll cycle, 18:226–239 Xanthosoma, 8:45–46, 56–57, see also Aroids Y Yam (Dioscorea), 12:177–184 Yield: determinants, 7:70–74; 97–99 limiting factors, 15:413–452 Z Zantedeschi, see Aroids, ornamental Zephyranthes, 25:60–61 Zinc: deficiency & toxicity symptoms in fruits & nuts, 2:151 foliar application, 6:332, 336 nutrition, 5:326; 23:109–178 pine bark media, 9:124

Cumulative Contributor Index (Volumes 1–30) Abbott, J.A., 20:1 Adams III, W.W., 18:215 Afek, U., 30:253 Aldwinckle, H.S., 1:423; 15:xiii, 29:1 Amarante, C., 28:161 Anderson, I.C., 21:73 Anderson, J.L., 15:97 Anderson, P.C., 13:257 Andrews, P.K., 15:183 Ashworth, E.N., 13:215; 23:1 Asokan, M.P., 8:43 Atkinson, D., 2:424 Aung, L.H., 5:45 Bailey, W.G., 9:187 Baird, L.A.M., 1:172 Banks, N.H., 19:217; 25:197; 26:161 Barden, J.A., 9:351 Barker, A.V., 2:411 Bartz, J.A., 30:185 Bass, L.N., 2:117 Bassett, C. L., 26:49 Becker, J.S., 18:247 Beer, S.V., 1:423 Behboudian, M.H., 21:105; 27:189 Bennett, A.B., 13:67 Benschop, M., 5:45 Ben-Ya’acov, A., 17:381 Benzioni, A., 17:233 Bevington, K.B., 24:277 Bewley, J.D., 18:171 Binzel, M.L., 16:33 Blanpied, G.D., 7:xi Blenkinsop, R.W., 30:317 Bliss, F.A., 16:xiii; 28:xi Boardman, K. 27 xi Borochov, A., 11:15 Bower, J.P., 10:229 Bradley, G.A., 14:xiii

Brandenburg, W., 28:1 Brecht, J.K., 30:185 Brennan, R., 16:255 Broadbent, P., 24:277 Broschat, T.K., 14:1 Brown, S. 15:xiii Buban, T., 4:174 Bukovac, M.J., 11:1 Burke, M.J., 11:xiii Buwalda, J.G., 12:307 Byers, R.E., 6:253; 28:351 Caldas, L.S., 2:568 Campbell, L.E., 2:524 Cantliffe, D.J., 16:109; 17:43; 24:229; 28:325 Carter, G., 20:121 Carter, J.V., 3:144 Cathey, H.M., 2:524 Chambers, R.J., 13:1 Chandler, C.K. 28:325 Charron, C.S., 17:43 Chen, K., 30:83 Chen, Z., 25:171 Chin, C.K., 5:221 Clarke, N.D., 21:1 Coetzee, J. H., 26:1 Cohen, M., 3:394 Collier, G.F., 4:49 Collins, G., 25:235 Collins, W.L., 7:483 Colmagro, S., 25:235 Compton, M.E., 14:239 Conover, C.A., 5:317; 6:119 Coppens d’Eeckenbrugge, G., 21:133 Costa, G. 28:351 Coyne, D.P., 3:28 Crane, J.C., 3:376 Criley, R.A., 14:1; 22:27; 24:x Crowly, W., 15:1 Cutting, J.G., 10:229

Daie, J., 7:69 Dale, A., 11:185; 16:255 Darnell, R.L., 13:339, 28:325 Davenport, T.L., 8:257; 12:349 Davies, F.S., 8:129; 24:319 Davies, P.J., 15:335 Davis, T.D., 10:63; 24:55 Decker, H.F., 27:317 DeEll, J.R., 23:69 DeGrandi–Hoffman, G., 9:237 De Hertogh, A.A., 5:45; 14:57; 18:87; 25:1 Deikman, J., 16:1 DellaPenna, D., 13:67 Demers, D.-A., 30:163 Demmig-Adams, B., 18:215 Dennis, F.G., Jr., 1:395 Dickson, E.E ., 29:1 Dorais, M., 26:239; 30:163 Doud, S.L., 2:1 Dudareva, N., 24:31 Duke, S.O., 15:371 Dunavent, M.G., 9:103 Duval, M.-F., 21:133 Düzyaman, E., 21:41 Dyer, W.E., 15:371 Dzhangaliev, A.D., 29:63, 305 Early, J.D., 13:339 Eastman, K., 28:125 Elfving, D.C., 4:1; 11:229 El-Goorani, M.A., 3:412 Esan, E.B., 1:1 Evans, D.A., 3:214 Ewing, E.E., 14:89 Faust, M., 2:vii, 142; 4:174; 6:287; 14:333; 17:331; 19:263; 22:225; 23:179 Felkey, K., 30:185

Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 523

523

524

CUMULATIVE CONTRIBUTOR INDEX

Fenner, M., 13:183 Fenwick, G.R., 19:99 Ferguson, A.R., 6:1 Ferguson, I.B., 11:289; 30:83 Ferguson, J.J., 24:277 Ferguson, L., 12:409 Ferree, D.C., 6:155 Ferreira, J.F.S., 19:319 Fery, R.L., 2:311; 12:157 Fischer, R.L., 13:67 Fletcher, R.A., 24:53 Flick, C.E., 3:214 Flore, J.A., 11:111 Forshey, C.G., 11:229 Forsline, P.L., 29:ix; 1 Franks, R. G., 27:41 Fujiwara, K., 17:125

Hergert, G.B., 16:255 Hess, F.D., 15:371 Hetterscheid, W.L.A., 28:1 Heywood, V., 15:1 Hjalmarsson, I., 27:79–123 Hogue, E.J., 9:377 Hokanson, S.C. 29:1 Holt, J.S., 15:371 Huber, D.J., 5:169 Huberman, M., 30:1 Hunter, E.L., 21:73 Hutchinson, J.F., 9:273 Hutton, R.J., 24:277

Gazit, S., 28:393 Geisler, D., 6:155 Geneve, R.L., 14:265 George, W.L., Jr., 6:25 Gerrath, J.M., 13:315 Gilley, A., 24:55 Giovannetti, G., 16:71 Giovannoni, J.J., 13:67 Glenn, G.M., 10:107 Goffinet, M.C., 20:ix Goldschmidt, E.E., 4:128; 30:1 Goldy, R.G., 14:357 Goren, R., 15:145; 30:1 Gosselin, A., 26:239 Goszczynska, D.M., 10:35 Gradziel, T.M., 30: xiii Grace, S.C., 18:215 Graves, C.J., 5:1 Gray, D., 3:1 Grierson, W., 4:247 Griffen, G.J., 8:291 Grodzinski, B., 7:345 Gucci, R., 21:177 Guest, D.I., 17:299 Guiltinan, M.J., 16:1

Jackson, J.E., 2:208 Janick, J., 1:ix; 8:xi; 17:xiii; 19:319; 21:xi; 23:233 Jarvis, W.R., 21:1 Jenks, M.A., 23:1 Jensen, M.H., 7:483 Jeong, B.R., 17:125 Jewett, T.J., 21:1 Jiang, W., 30:115 Joiner, J.N., 5:317 Jones, H.G., 7:301 Jones, J.B., Jr., 7:1 Jones, R.B., 17:173

Hackett, W.P., 7:109 Halevy, A.H., 1:204; 3:59 Hallett, I.C., 20:121 Hammerschmidt, R., 18:247 Hanson, E.J., 16:255 Harker, F.R., 20:121 Heaney, R.K., 19:99 Heath, R.R., 17:43 Helzer, N.L., 13:1 Hendrix, J.W., 3:172 Henny, R.J., 10:1

Indira, P., 23:277 Ingle, M. 27:227 Isenberg, F.M.R., 1:337 Iwakiri, B.T., 3:376

Kagan-Zur, V., 16:71 Kalt, W. 27:269; 28:125 Kang, S.-M., 4:204 Kato, T., 8:181 Kawa, L., 14:57 Kawada, K., 4:247 Kays, S.J.. 30:253 Kelly, J.F., 10:ix; 22:xi Kester, D.E., 25:xii Khan, A.A., 13:131 Kierman, J., 3:172 Kim, K.-W., 18:87 Kinet, J.-M., 15:279 King, G.A., 11:413 Kingston, C.M., 13:407–432 Kirschbaum, D.S. 28:325 Kliewer, W.M., 14:407 Knight, R.J., 19:xiii Knox, R.B., 12:1 Kofranek, A.M., 8:xi Korcak, R.F., 9:133; 10:183 Kozai, T., 17:125 Krezdorn, A.H., 1:vii Kushad, M.M., 28:125

Lakso, A.N., 7:301; 11:111 Laimer, M., 28:187 Lamb, R.C., 15:xiii Lang, G.A., 13:339 Larsen, R.P., 9:xi Larson, R.A., 7:399 Leal, F., 21:133 Ledbetter, C.A., 11:159 Lee, J.-M., 28:61 Levy, Y., 30:37 Li, P.H., 6:373 Lill, R.E., 11:413 Lin, S., 23:233 Liu, Z., 27:41 Lipton, W.J., 12:69 Littlejohn, G.M., 26:1 Litz, R.E., 7:157 Lockard, R.G., 3:315 Loescher, W.H., 6:198 Lorenz, O.A., 1:79 Lu, R., 20:1 Luby,J.J., 29:1 Lurie, S., 22:91–121 Lyrene, P., 21:xi Maguire, K.M., 25:197 Manivel, L., 22:267 Maraffa, S.B., 2:268 Marangoni, A.G., 17:203; 30:317 Marini, R.P., 9:351 Marlow, G.C., 6:189 Maronek, D.M., 3:172 Martin, G.G., 13:339 Masiunas, J., 28:125 Mayak, S., 1:204; 3:59 Maynard, D.N., 1:79 McConchie, R., 17:173 McNicol, R.J., 16:255 Merkle, S.A., 14:265 Michailides, T.J., 12:409 Michelson, E., 17:381 Mika, A., 8:339 Miller, A.R., 25:171 Miller, S.S., 10:309 Mills, H.A., 2:411; 9:103 Mills, T.M., 21:105 Mitchell, C.A., 17:1 Mizrahi, Y., 18:291, 321 Mohankumar, C.R., 30:355 Molnar, J.M., 9:1 Monk, G.J., 9:1 Monselise, S.P., 4:128 Moore, G.A., 7:157 Mor, Y., 9:53 Morris, J.R., 16:255 Mu, D., 30:115

CUMULATIVE CONTRIBUTOR INDEX Murashige, T., 1:1 Murr, D.P., 23:69 Murray, S.H., 20:121 Myers, P.N., 17:1 Nadeau, J.A., 19:1 Nascimento, W.M., 24:229 Neilsen, G.H., 9:377 Nelson, P.V., 26:xi Nerd, A., 18:291, 321 Niemiera, A.X., 9:75 Nobel, P.S., 18:291 Nyujtò, F., 22:225 Oda, M., 28:61 O’Donoghue, E.M., 11:413 Ogden, R.J., 9:103 O’Hair, S.K., 8:43; 12:157 Oliveira, C.M., 10:403 Oliver, M.J., 18:171 O’Neill, S.D., 19:1 Opara, L.U., 19:217; 24:373; 25:197 Ormrod, D.P., 8:1 Ortiz, R., 27:79 Palser, B.F., 12:1 Papadopoulos, A.P., 21:1; 26:239; 30:163 Pararajasingham, S., 21:1 Parera, C.A., 16:109 Paris, H.S., 25:71 Pegg, K.G., 17:299 Pellett, H.M., 3:144 Perkins-Veazil, P., 17:267 Pichersky, E., 24:31 Piechulla, B., 24:31 Ploetz, R.C., 13:257 Pokorny, F.A., 9:103 Poole, R.T., 5:317; 6:119 Poovaiah, B.W., 10:107 Portas, C.A.M., 19:99 Porter, M.A., 7:345 Possingham, J.V., 16:235 Prange, R.K., 23:69 Pratt, C., 10:273; 12:265 Predieri, S., 28:237 Preece, J.E., 14:265 Priestley, C.A., 10:403 Proctor, J.T.A., 9:187 Puonti–Kaerlas, J., 26:85 Qu, D., 30:115 Quamme, H., 18:xiii Raese, J.T., 11:357 Ramming, D.W., 11:159

Rapparini, F., 28:237 Ravi, V., 23:277; 30:355 Reddy, A.S.N., 10:107 Redgwell, R.J., 20:121 Reid, M., 12:xiii; 17:123 Reuveni, M., 16:33 Richards, D., 5:127 Rieger, M., 11:45 Roper, T.R., 21:215 Rosa, E.A.S., 19:99 Roth-Bejerano, N., 16:71 Roubelakis-Angelakis, K.A., 14:407 Rouse, J.L., 12:1 Royse, D.J., 19:59 Rudnicki, R.M., 10:35 Ryder, E.J., 2:164; 3:vii Sachs, R., 12:xiii Sakai, A., 6:357 Salisbury, F.B., 4:66; 15:233 Salova, T. H., 29:305 Saltveit, M.E., 23:x; 23:185 San Antonio, J.P., 6:85 Sankhla, N., 10:63; 24:55 Saure, M.C., 7:239 Schaffer, B., 13:257 Schenk, M.K., 22:185 Schneider, G.W., 3:315 Schneider, K.R., 30:185 Schuster, M.L., 3:28 Scorza, R., 4:106 Scott, J.W., 6:25 Sedgley, M., 12:223; 22:1; 25:235 Seeley, S.S., 15:97 Serrano Marquez, C., 15:183 Sharp, W.R., 2:268; 3:214 Sharpe, R.H., 23:233 Shattuck, V.I., 14:199 Shear, C.B., 2:142 Sheehan, T.J., 5:279 Shipp, J.L., 21:1 Shirra, M., 20:267 Shorey, H.H., 12:409 Simon, J.E., 19:319 Singh, Z. 27:189 Sklensky, D.E., 15:335 Smith, A.H., Jr., 28:351 Smith, M.A.L., 28:125 Smith, G.S., 12:307 Smock, R.M., 1:301 Sommer, N.F., 3:412 Sondahl, M.R., 2:268

525 Sopp, P.I., 13:1 Soule, J., 4:247 Sozzi, G. O., 27:125 Sparks, D., 8:217 Splittstoesser, W.E., 6:25; 13:105 Spooner, D.M., 28:1 Srinivasan, C., 7:157 Stang, E.J., 16:255 Steffens, G.L., 10:63 Stern, R.A., 28:393 Stevens, M.A., 4:vii Stroshine, R.L., 20:1 Struik, P.C., 14:89 Studman, C.J., 19:217 Stutte, G.W., 13:339 Styer, D.J., 5:221 Sunderland, K.D., 13:1 Sung, Y., 24:229 Surányi, D., 19:263; 22:225; 23:179 Swanson, B., 12:xiii Swietlik, D., 6:287; 23:109 Syvertsen, J.P., 7:301, 30:37 Talcott, S.T., 30:185 Tattini, M., 21:177 Tétényi, P., 19:373 Theron, K.I., 25:1 Tibbitts, T.W., 4:49 Timon, B., 17:331 Tindall, H.D., 16:143 Tisserat, B., 1:1 Titus, J.S., 4:204 Trigiano, R.N., 14:265 Tunya, G.O., 13:105 Turekhanova, P.M., 29:305 Upchurch, B.L., 20:1 Valenzuela, H.R., 24:139 van den Berg, W.L.A., 28:1 van Doorn, W.G., 17:173; 18:1 Van Iepersen. W., 30: 163 van Kooten, O., 23:69 van Nocker, S. 27:1 Veilleux, R.E., 14:239 Vorsa, N., 21:215 Vizzotto, G., 28: 351 Wallace, A., 15:413 Wallace, D.H., 17:73 Wallace, G.A., 15:413 Wang, C.Y., 15:63 Wang, L., 30:115 Wang, S.Y., 14:333

526 Wann, S.R., 10:153 Watkins, C.B., 11:289 Watson, G.W., 15:1 Webster, B.D., 1:172; 13:xi Weichmann, J., 8:101 Wetzstein, H.Y., 8:217 Whiley, A.W., 17:299 Whitaker, T.W., 2:164 White, J.W., 1:141 Williams, E.G., 12:1 Williams, M.W., 1:270

CUMULATIVE CONTRIBUTOR INDEX Wismer, W.V., 17:203 Wittwer, S.H., 6:xi Woodson, W.R., 11:15 Wright, R.D., 9:75 Wutscher, H.K., 1:237 Xu, C., 30:83 Yada, R.Y., 17:203; 30:317 Yadava, U.L., 2:1 Yahia, E.M., 16:197; 22:123

Yan, W., 17:73 Yarborough, D.E., 16:255 Yelenosky, G., 7:201 Zanini, E., 16:71 Zhang, B., 30:83 Zieslin, N., 9:53 Zimmerman, R.H., 5:vii; 9:273 Ziv, M., 24:1 Zucconi, F., 11:1