HORTICULTURAL REVIEWS Volume 37
edited by
Jules Janick Purdue University
HORTICULTURAL REVIEWS Volume 37
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HORTICULTURAL REVIEWS Volume 37
edited by
Jules Janick Purdue University
HORTICULTURAL REVIEWS Volume 37
Horticultural Reviews is sponsored by: American Society of Horticultural Science International Society for Horticultural Science
Editorial Board, Volume 37 Victor Rodov Robert Skirvin Gun Werlemark
HORTICULTURAL REVIEWS Volume 37
edited by
Jules Janick Purdue University
Copyright 2010 by Wiley-Blackwell. All rights reserved. Published by John Wiley & Sons, Inc., Hoboken, New Jersey Published simultaneously in Canada Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientific, Technical, and Medical business with Blackwell Publishing. 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, or online at http://www.wiley.com/go/permission. 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 877-762-2974, 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 formats. For more information about Wiley products, visit our web site at www.wiley.com. Library of Congress Cataloging-in-Publication Data: ISBN 978-0-470-53716-9 (cloth) ISSN 0163-7851 Printed in the United States of America 10 9 8 7 6 5 4 3 2 1
Contents
Contributors Dedication: Irwin L. Goldman
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Molly Jahn
1. Common Bean Rust: Pathology and Control
1
Merion M. Liebenberg and Zacharias A. Pretorius Abbreviations and Acronyms I. Introduction II. Pathogen Nomenclature, Morphology, and Life Cycle III. Symptoms IV. Host Range V. Distribution VI. Epidemiology VII. Economic Importance VIII. Pathogenic Variation IX. Manipulation of the Fungus X. Disease Management XI. Conclusions Acknowledgments Literature Cited
2. Bitter Gourd: Botany, Horticulture, Breeding
2 3 4 8 9 11 19 25 28 37 44 73 75 75
101
Tusar K. Behera, Snigdha Behera, L. K. Bharathi, K. Joseph John, Philipp W. Simon, and Jack E. Staub I. II. III. IV.
Introduction Botany Horticulture Breeding
102 109 113 120 v
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V. Conclusions Literature Cited
3. Dynamics of Carbohydrate Reserves in Cultivated Grapevines
131 132
143
Bruno P. Holzapfel, Jason P. Smith, Stewart K. Field, and W. James Hardie I. II. III. IV. V.
Introduction Carbohydrate Reserves Accumulation of Carbohydrate Reserves Photoassimilation and Storage Processes Mobilization and Utilization of Carbohydrate Reserves VI. Viticultural Management of Carbohydrate Reserves VII. Summary and Conclusions Literature Cited
4. Elderberry: Botany, Horticulture, Potential
144 146 152 165 174 185 199 201
213
Denis Charlebois, Patrick L. Byers, Chad E. Finn, and Andrew L. Thomas I. Introduction II. Botany III. Horticulture IV. Propagation V. Uses VI. Concluding Remarks Literature Cited
5. Modified Humidity Packaging of Fresh Produce
215 215 226 242 249 263 264
281
Victor Rodov, Shimshon Ben-Yehoshua, Nehemia Aharoni, and Shabtai Cohen I. II. III. IV. V.
Introduction Basics of Postharvest Water Relations Water in Postharvest Life of Fresh Produce The Concept of Modified-Humidity Packaging Practical MHP Approaches
282 282 293 300 301
CONTENTS
VI. Summary Acknowledgments Literature Cited
6. Ecological and Genetic Systems Underlying Sustainable Horticulture
vii
319 321 321
331
Autar K. Mattoo and John R. Teasdale Abbreviations I. Introduction II. Ecological Systems III. Genetic Systems IV. An Integrated Approach to Sustainable Horticulture Literature Cited
331 332 333 342 353 355
Subject Index
363
Cumulative Subject Index
365
Cumulative Contributor Index
393
Contributors
Nehemia Aharoni Department of Postharvest Science of Fresh Produce, Institute for Technology and Storage of Agricultural Produce, Agricultural Research Organization—The Volcani Center, Bet Dagan 50250, Israel Snigdha Behera Indian Agricultural Research Institute, New Delhi 11002, India Tusar K. Behera Indian Agricultural Research Institute, New Delhi 11002, India Shimshon Ben-Yehoshua Department of Postharvest Science of Fresh Produce, Institute for Technology and Storage of Agricultural Produce, Agricultural Research Organization—The Volcani Center, Bet Dagan 50250, Israel L. K. Bharathi Indian Agricultural Research Institute, New Delhi 11002, India Patrick L. Byers Cooperative Extension Service, University of Missouri, Springfield, MO 65802, USA Denis Charlebois Agriculture and Agri-Food Canada, Horticultural Research and Development Centre, 430 Gouin Boulevard, Saint-Jean-sur-Richelieu, Que´bec, J3B 3E6 Canada Shabtai Cohen Department of Environmental Physics and Irrigation, Institute of Soil, Water, and Environmental Sciences, Agricultural Research Organization—The Volcani Center, Bet Dagan 50250, Israel Stewart K. Field National Wine and Grape Industry Centre, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales, 2678 Australia Chad E. Finn Horticultural Crops Research Laboratory, U.S. Department of Agriculture, Agricultural Research Service, 3420 NW Orchard Avenue, Corvallis, OR 97330, USA W. James Hardie National Wine and Grape Industry Centre, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales, 2678 Australia Bruno P. Holzapfel National Wine and Grape Industry Centre, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales, 2678 Australia Molly Jahn University of Wisconsin, Madison, 140 Agricultural Hall, Madison, WI 537076, USA K. Joseph John National Bureau of Plant Genetic Resources, KAU (P.O.), Thrissur 680656, Kerala, India
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Merion M. Liebenberg ARC–Grain Crops Institute, Private Bag X 1251, Potchefstroom 2520, South Africa Autar K. Mattoo Sustainable Agricultural Systems Laboratory, USDA-ARS, Animal and Natural Resources Institute, Building 001, The Henry A. Wallace Beltsville Agricultural Research Center, Beltsville, MD 20705, USA Zacharias A. Pretorius Department of Plant Science, University of the Free State, P.O. Box 339, Bloemfontein 9300, South Africa Victor Rodov Department of Postharvest Science of Fresh Produce, Institute for Technology and Storage of Agricultural Produce, Agricultural Research Organization—The Volcani Center, Bet Dagan 50250, Israel Philipp W. Simon Vegetable Crops Research Unit, ARS-USDA Department of Horticulture, University of Wisconsin, Madison, WI 53706, USA Jason P. Smith National Wine and Grape Industry Centre, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales, 2678 Australia Jack E. Staub Forage and Range Research Laboratory, ARS-USDA, Logan, UT 84322, USA John R. Teasdale Sustainable Agricultural Systems Laboratory, USDA-ARS, Animal and Natural Resources Institute, Building 001, The Henry A. Wallace Beltsville Agricultural Research Center, Beltsville, MD 20705, USA Andrew L. Thomas Southwest Research Center, University of Missouri, 14548 Highway H, Mt. Vernon, MO 65712, USA
Irwin L. Goldman
Dedication: Irwin L. Goldman This volume of Horticultural Reviews is dedicated to Irwin L. Goldman in recognition of his accomplishments in plant genetics, breeding, and horticulture. He is known for his brilliance in science and his extraordinary skills in administration. Irwin was born in Chicago in 1963 and raised in Skokie, Illinois. He learned from his parents and his maternal grandmother how to find, preserve, and celebrate the simple joys in life, including the beauty of plants and the wonders of home-grown fruits and vegetables. Early experiences with family in Fond Du Lac, Wisconsin, and Union Pier, Michigan were formative in generating a love of being outside and a deep appreciation of nature and agriculture. Irwin entered the University of Illinois at Urbana-Champaign in 1981 to study writing and literature but found himself drawn to biology and genetics, largely because these subjects were so elusive, abstract, and difficult to master. A close childhood friend, Neal Keeshin, developed an interest in evolutionary biology and read aloud from books by Stephen Jay Gould while they were on camping and canoeing trips during this period. Evolution as an idea combined Irwin’s interests in nature and genetics and proved to be a lifelong passion as well as an instigator of his academic pursuits. Avery positive experience in an introductory botany class led to a parttime student worker position in the Department of Agronomy with Professor Cecil Nickell, a soybean breeder. It was there that Irwin developed a real love for fieldwork and began to learn about the science of plant breeding. He also learned how to drive a combine and conducted an experiment on the interaction of soil compaction and fungicides in soybean disease. Coming home from work physically exhausted and with dirt under his fingernails sealed the deal, and he quickly switched his major to Agricultural Science and obtained a B.S. degree in 1985. Irwin obtained his M.S. in Crop Science from North Carolina State University in 1987 and a Ph.D. in Plant Breeding and Plant Genetics from the University of Wisconsin-Madison in 1991. His thesis research at North Carolina involved breeding soybean for drought resistance and at Wisconsin focused on homeotic mutants of pea that had potential to modify and improve the pea ideotype. The experiences at these two great xiii
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institutions, both of which had outstanding faculties in plant breeding and genetics, as well as a very strong cohort of classmates with whom to study and learn helped make graduate school an incredibly positive introduction to science. His mentors during this period, Professor Thomas E. Carter Jr. at North Carolina State University and Professor Earl Gritton at Wisconsin, gave unselfishly of their ideas and energy and dedicated tremendous amounts of time in the field and in the laboratory to help students learn. After graduate school, Dr. Goldman returned to the University of Illinois for a postdoctoral position in maize genetics. There he worked with Torbert Rocheford and John Dudley on molecular-marker-based investigations of the Illinois Long Term Selection strains, which are part of the longest-running plant breeding experiment in modern times. This work combined classical breeding and marker-based studies to reveal a large quality trait locus (QTL) at sh-2 that explained significant variation for protein and starch concentration in the Illinois High Protein and Illinois Low Protein strains. This finding was consistent with the idea of a candidate gene affecting a major QTL and helped lay some of the groundwork for understanding the genetic changes in these strains over more than 100 generations of mass selection. From Illinois, Dr. Goldman accepted a faculty position in the Department of Horticulture at the University of Wisconsin-Madison and arrived there in late 1992, only to leave immediately for a five-month stint at the Faculty of Agriculture in Rehovot of the Hebrew University of Jerusalem, where he conducted work with Professor Dani Zamir on tomato genetics. This work, supported by a BARD grant, further expanded Dr. Goldman’s interests in vegetable genetics and allowed him another opportunity to work with a very well-characterized genetic map and an abundant set of molecular markers. In addition, Zamir’s group, in collaboration with the Steve Tanksley laboratory at Cornell University, had developed a series of tomato populations that included various wild species as parents. These populations became valuable genetic mapping populations and could be used to ask and answer many questions about useful quantitative traits in tomato. Tomato and maize provided a glimpse into what could be done with well-characterized genetic systems. However, the richness of those systems was only a distant hope for Dr. Goldman in his position at Wisconsin. His job was in breeding and genetics of cross-pollinated vegetable crops, and his predecessor, Professor Warren H. Gabelman, worked with carrot, onion, and table beet. These three biennial root crops were of importance to Wisconsin and many other parts of the world but had relatively few workers in the public sector. Genetic systems were not
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well established. Gabelman had begun hybrid breeding programs in all three crops in 1949, and when he retired some 40 years later, left a great legacy of germplasm and ideas that became an excellent foundation for Dr. Goldman’s program. While still at Illinois, Dr. Goldman developed an interest in human health–based traits in plants and began to explore this area in the scientific literature. He became aware of the work of Professor Leonard Pike at Texas A&M University, one of the first U.S. plant breeders to begin a program that included health-related traits as breeding targets. Later, Dr. Goldman would identify Pike as one who greatly influenced his research in this area. Beginning in 1993 at Wisconsin, Dr. Goldman’s main work focused on three areas: 1. Horticultural approaches to characterization and manipulation of secondary compounds with medicinal and nutritional properties from carrot, onion, and beet 2. Genetic control of processing and disease resistance traits in these crops using classical and molecular methods 3. Population improvement and inbred development in carrot, onion, and beet Spiraling interest in functional foods and their derivative phytopharmaceuticals began to encourage collaboration between medical and agricultural scientists to investigate crop plant–based compounds with potential health benefits. These efforts were fueled by an emerging market for novel agricultural products: medicinally enhanced crops, designed and bred to contain higher levels of health-promoting compounds. Irwin Goldman’s laboratory was among a handful of horticulture-based research groups in the United States investigating vegetable plant–based phytochemicals with medicinal significance. This area became a focal point for his laboratory, and Dr. Goldman contributed several reviews on this subject for a variety of audiences. Irwin Goldman was the first scientist to investigate horticulturally based questions surrounding the biological nature of onion-induced antiplatelet activity. For thousands of years, humans have recognized that native compounds in onion plants promote blood circulation; however, only recently has the mechanism of this enhancement been determined to be the inhibition of platelet aggregation. Platelet aggregation is a major cause of thromboembolic events leading to cardiovascular disease, the leading cause of death in the United States. Dietary intake of onion may thereby decrease cardiovascular risk. Dr.
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Goldman teamed up with Dr. B.S. Schwartz, a hematologist from the Department of Medicine, University of Wisconsin–Madison who offered expertise with human platelets and enabled Irwin’s research group to pursue successful inquiry into this interdisciplinary field. He has also formed an alliance with Dr. John Folts in the Department of Medicine (Cardiology) who provided expertise with an in vivo coronary thrombosis model. Completing the team were Dr. Kirk Parkin, a food chemist in the Department of Food Science and Dr. Michael Havey, a geneticist from the Department of Horticulture. Together, these scientists worked collaboratively on various aspects of onion-induced antiplatelet activity and uncovered both genetic and environmental influences on this trait. Irwin Goldman and his students have demonstrated substantial variability for antiplatelet strength among Allium species accessions and among cultivated germplasm sources. They have shown the antiplatelet factor is sulfur dependent and therefore correlated with certain environmental conditions, a finding that was consistent with the biochemistry of the well-characterized sulfur assimilation pathway in onion, through which sulfate is converted into g-glutamyl peptides and ultimately to S-(alk)-en-yl cysteine sulfoxides (ACSOs). Thiosulfinates and other organosulfur compounds with antiplatelet activity are derived from hydrolysis of these ACSOs by the enzyme alliinase. Irwin Goldman and his students also demonstrated that onion-induced antiplatelet activity is likely a serendipitous by-product of a developmentally regulated flux of organosulfur compounds for control of insect pests. Because organosulfur compounds are thought to be a primary deterrent to insect predators, these compounds cycle through onion plants from old leaf scales to new in protecting the developing bulb and then are shunted to the developing leaves and ultimately to flowers for protection during pollination. This finding demonstrates this unique medicinal character fluctuates dramatically with plant development and is associated likely with a natural flux in defense compounds. Additional research in this area has focused on &
&
&
Investigation of the genetic control of onion-induced antiplatelet activity through quantitative trait locus mapping approaches using cloned regulatory genes in the sulfur assimilation pathway as DNA probes Evaluation of the effects of sulfur fertility on onion-induced antiplatelet activity Temporal aspects of thiosulfinate formation and medicinal activity in onion extracts
DEDICATION &
&
&
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Comparative induction of antiplatelet activity of various Allium thiosulfinates Relationship of onion organosulfur compounds and resistance to onion white rot In vivo canine testing of onion extracts and Allium thiosulfinates in a coronary thrombosis model
These studies have suggested that onion extracts, particularly those that are not processed with heat, have significant potential to inhibit in vivo antiplatelet activity. Carrot roots contain high levels of b-carotene and have long been a significant source (perhaps as much as 20%) of provitamin A in the human diet. Vitamin A may offer significant potential to inhibit carcinogenesis and improve cardiovascular health. Little investigation of carotenoid biosynthesis has been conducted with carrot, in part because of its limitations as an experimental organism. All previous studies on the genetic control of beta-carotene synthesis in carrot root tissue have indicated the presence of pigment (i.e., orange roots) is recessive to white or nonpigmented roots. However, Dr. Goldman identified and characterized a recessive gene that causes a 93% reduction in carotenoid content, suggesting a new interpretation of carotenoid biosynthesis in carrot roots. This gene, designated rp, likely causes a lesion in the carotenoid biosynthetic pathway and may provide new clues as to the details of this important process in carrot. Recent chromatographic analysis indicates the presence of novel carotenoids in rprp roots that are not present in RPRP roots. Further investigation of these carotenoids and related questions surrounding the carotenoid biosynthetic pathway in carrot are continuing in Dr. Goldman’s laboratory. Through analysis of this mutant, Dr. Goldman determined that carrots produce tocopherols, particularly alpha tocopherol or provitamin E. This has led to projects designed to screen carrot germplasm for both provitamins A and E and to a breeding program focusing on increasing both compounds in carrot. Dr. Goldman’s students also developed a protocol for screening carrot tissue for both compounds simultaneously via high performance liquid chromatography (HPLC). Recommended Daily Allowances (RDA) for folic acid, a B-vitamin responsible for the production of red blood cells and development of fetal neural tubes, has increased substantially due to the recognition of widespread damage to fetal brain tissues as a result of deficiencies of this nutrient. In addition, recent epidemiological investigation has shown that folic acid lowers blood homocysteine levels and may be a significant cardiopreventive agent. Despite changes in RDA, variation in native
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plant folic acid concentration complicates dietary recommendations. Plants from the family Chenopodiaceae such as red beet are among the best vegetable sources of folic acid. Work in Dr. Goldman’s laboratory has focused on developing an understanding of the magnitude of genetic variability and the mechanism of genetic control of folic acid content in red beet germplasm. In a series of journal publications, he and his students have successfully characterized variability for folic acid content in a range of red beet germplasm sources, shown that transgressive segregation is important for folic acid content in wide crosses, and demonstrated developmental patterns of folic acid accumulation in root and shoot tissues. Dr. Goldman’s research on carrot processing and disease resistance traits focused primarily on inheritance of northern root-knot nematode resistance, a major pest in carrot production throughout the United States. Min Wang and Irwin Goldman identified two new resistance genes and unequivocally demonstrated that these two recessive genes control the reaction of host and parasite in this system. The carrot seed industry now uses these techniques, and a grant from two of these companies enabled continued research on this problem. Dr. Goldman also characterized processing carrot germplasm for field resistance to aster yellows, a serious carrot pest vectored by the aster leafhopper in the upper midwestern United States. This work led to a better understanding of selection response to aster yellows under field conditions. In addition, Dr. Goldman’s research led to the selection of three aster yellows resistant inbred carrot inbred lines for release to the seed industry. He also investigated genotype environment interactions for both slicing and dicing carrot production in several different planting systems in Wisconsin and developed a model for processing carrot yield optimization. Due to the banning of synthetic red dyes as suspected carcinogens, betalain pigments found in red beet have been adopted for use as natural red food colorings. Dr. Goldman’s work focused on genetic modification of pigment concentration in beet roots and genetic characterization of improved populations. Dr. Goldman and his students investigated the response to selection for increased betalain pigment concentration and demonstrated that simultaneous selection for increased pigment concentration and decreased dissolved solids are incompatible possibly because biosynthesis of the pigment molecule requires sugar; thus the two objectives are in direct competition. Dr. Goldman and his students also investigated the nature of molecular marker frequency changes associated with this selection and identified marker-linked regions of the red beet genome that may be associated with selection for increased
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pigment concentration, a finding that may have implications for future selection schemes. Populations from Dr. Goldman’s program are used by the vegetable processing industry to extract betalain pigments for use as colorants in the food industry in the United States and abroad. Development of novel secondary compounds and genetic enhancement of native secondary compounds in beet and other vegetable crops as natural food additives is a targeted area of current and future research in Dr. Goldman’s program. Additional research has investigated sizeshape relations in cylindrical beet cultivars at varying population densities because cylindrically shaped roots may offer greater efficiencies in processing. Finally, his research has identified three new recessive genes: a gibberellic acid–sensitive dwarfing gene, dw; a blotchy root color mutant, bl; and a gene for fasciation of the flower stem, ffs. An important aspect of Dr. Goldman’s research contributions is the development of improved carrot, onion, and red beet germplasm. These three crops contribute significant value to Wisconsin’s vegetable processing industry, and the commercial seed industry and growers of these three crops rely on public programs such as Dr. Goldman’s for improved populations and inbred lines to fuel their breeding programs. Dr. Goldman is the only publicly funded scientist breeding table beet in the United States and is among a small group of public scientists breeding carrot and onion. For 15 years, Irwin Goldman was fortunate to work closely with D. Nicholas Breitbach on the breeding programs for these three crops. Much of the cumulative wisdom about handling these three crops in breeding was developed by Brietbach over a 37-year career and has been shared with others around the world who are interested in these crops. The breeding program is divided into population improvement and inbred development efforts. Population improvement efforts are aimed at increasing the level of key processing and horticultural attributes in breeding populations through field, greenhouse, and laboratory quality and disease screening trials. In 1997, the first inbred lines of carrot and table beet from Dr. Goldman’s breeding program were released to the seed industry and are now in use in commercial breeding programs and cultivars. Dr. Goldman’s program has also released an open-pollinated yellow-rooted table beet cultivar that is currently marketed by Johnny’s Selected Seeds of Maine. Finally, Dr. Goldman, along with his close colleague Professor James Nienhuis, has taught two courses in Plant Breeding and Plant Genetics (Horticulture 501 and Horticulture 502) and a course on vegetable crops for many years at Wisconsin. He also taught for a number of years in the
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Biocore program, providing lectures on evolutionary biology to honors biology students. Dr. Goldman and Professor Nienhuis have developed a unique historical and cultural approach to these courses, often using this as a platform to explore biological concepts. They have developed a number of programs to supplement their classroom work, including a public radio call-in show about vegetable crops and a giant pumpkin regatta held every year on Lake Mendota. Teaching and mentoring students has been, and continues to be, one of the greatest experiences of campus life and overall the greatest privilege of the job. At this stage in his career, Dr. Goldman has mentored 10 M.S. students and 6 Ph.D. students. Irwin Goldman is one of a handful of scientists in the United States actively engaged in scholarship on the history of the field of plant breeding. His sabbatical leave at Harvard University in 2002 included an investigation of the beginnings of modern scientific plant breeding at the Bussey Institution. Dr. Goldman has been particularly interested in how predictive models, such as the progeny test and the inbred-hybrid method of breeding, have shaped modern conceptions of the field. He has investigated how early plant genetics research at the Bussey Institution generated a platform for both educational programming and research objectives in modern plant breeding. And he has compared the gains made by vegetable breeders with those made by agronomic crop breeders in terms of yield and quality during the 20th century. Dr. Goldman has written widely on these subjects and developed course materials that focus on these aspects of plant breeding and vegetable crops. In 2004, Dr. Goldman was asked by Dean Elton Aberle to join the College of Agricultural and Life Sciences administration on a part-time basis to work on research administrator. His supervisor was the Associate Dean for Research, Professor Margaret Dentine. In 2005, Dean Dentine retired and Dr. Goldman took over responsibility for the Research Division of the college on a 75% time basis, eventually serving as both the Interim Associate Dean for Research and the Interim Executive Associate Dean when Professor David Hogg assumed the deanship upon Aberle’s retirement. After Molly Jahn’s arrival as Dean in 2006, Dr. Goldman has served as both Vice Dean and Associate Dean for Research and continues in these roles. Working in administration has made Irwin Goldman even more optimistic about the future of science, higher education, and agricultural research. In those positions, he is able to come into contact on a more regular basis with inspired faculty, staff, and students who come to Madison to become steeped in the history, knowledge, and pragmatism that is a hallmark of our land-grant system.
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Irwin Goldman is the complete person. Irwin and his wife, Leora, have two children, Eliav and Aviv. He has a warm caring personality and is beloved by his students, admired by his colleagues, and respected by all. Molly Jahn University of Wisconsin, Madison
1 Common Bean Rust: Pathology and Control Merion M. Liebenberg ARC-Grain Crops Institute Private Bag X 1251 Potchefstroom 2520, South Africa Zacharias A. Pretorius Department of Plant Science University of the Free State PO Box 339 Bloemfontein 9300, South Africa ABBREVIATIONS AND ACRONYMS I. INTRODUCTION II. PATHOGEN NOMENCLATURE, MORPHOLOGY, AND LIFE CYCLE A. Nomenclature B. Morphology and Life Cycle 1. Asexual Stage 2. Sexual Stage III. SYMPTOMS IV. HOST RANGE A. Genera and Species B. Gene Pools of Phaseolus vulgaris V. DISTRIBUTION VI. EPIDEMIOLOGY A. Dissemination B. Environmental Influences 1. Temperature 2. Humidity and Leaf Surface Moisture 3. Dew Period 4. Light 5. Nutrition and Volatile Substances 6. pH and Ion Concentration C. Leaf Age Influences Horticultural Reviews, Volume 37 Edited by Jules Janick Copyright 2010 Wiley-Blackwell. 1
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VII. ECONOMIC IMPORTANCE VIII. PATHOGENIC VARIATION A. Standard Differentials B. Designation of Races C. Race Characterization 1. Stability and Reliability of Race Characterization D. Biochemical and Molecular Variation IX. MANIPULATION OF THE FUNGUS A. Purification of Isolates B. Inoculation C. Incubation D. Disease Reaction E. Co-inoculation Effects F. Storage X. DISEASE MANAGEMENT A. Fungicides B. Resistance Breeding 1. Race-Specific Resistance Conferred by Major Genes 2. Race-Nonspecific Resistance 3. Marker-Assisted Breeding C. Biological Control and Induced (Acquired) Resistance D. Cultural Practices 1. Cultivar Mixtures and Multilines 2. Intercropping and Multiple Cropping 3. Sanitation 4. Crop Rotation 5. Planting Time 6. Overhead Irrigation XI. CONCLUSIONS ACKNOWLEDGMENTS LITERATURE CITED
ABBREVIATIONS AND ACRONYMS AFLP ALS APR AS BCMV BCMNV Bel BGMV BIOAGRO
Amplified fragment length polymorphisms Angular leaf spot caused by Pseudocercospora griseola (previously Phaeoisariopsis griseola) Adult plant resistance ‘Actopan’/‘Sanilac’ selection Bean common mosaic virus Bean common mosaic necrotic virus Beltsville (USDA) Bean golden mosaic virus Instituto de Biotechnologia Aplicada a Agropecuaria (at the Federal University of Vic¸osa, Minas Gerais, Brazil)
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
CIAT
CNC Co Crg DNA DPO FAO FRAC GRIN HR IBRN KW MAS NIL PC PI PCR RAPD RFLP RH RIL RSA SCAR SSR Ur USDA
3
Centro Internacional de Agricultura Tropical (International Centre for Tropical Agurculture, in Cali, Colombia, with a subsidiary office in Kampala, Uganda) Compuesto Negro Chimaltenango Gene conferring resistance to Colletotrichum lindemuthianum Complements resistance gene Deoxyribonucleic acid Dry Bean Producers Organization Food and Agriculture Organization of the United Nations Fungicide Resistance Action Committee Germplasm Resources Information Network Hypersensitive reaction International Bean Rust Nursery ‘Kentucky Wonder’ Marker-assisted selection Near-isogenic line Pompadour Checa Plant introduction (U.S. Germplasm collection) Polymerase chain reaction Random amplified polymorphic DNA Restriction fragment length polymorphism Relative humidity Recombinant inbred line Republic of South Africa Sequence characterized amplified region Simple sequence repeat Gene conferring resistance to Uromyces appendiculatus United States Department of Agriculture
I. INTRODUCTION The common bean (Phaseolus vulgaris L.) is an important and versatile commodity, comprising both dry beans and green (snap) beans. It is grown in almost all parts of the populated world, particularly in temperate and subtropical South, Central and North America, Africa, India, and Asia, but also in Europe and Australia (FAO 2007). Broughton et al. (2003) cite Phaseolus spp. as the most important legumes for direct human consumption worldwide, of which over 30% are produced in Latin America and Africa, often by small-scale and subsistence farmers. Large-scale commercial production is also important in many countries,
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M. M. LIEBENBERG AND Z. A. PRETORIUS
particularly in the United States, Canada, Brazil, and Argentina. The importance of the crop cannot be underestimated, both as a source of protein in countries where meat is an expensive and scarce commodity and as a high-fiber, low-fat, and low-sodium content ingredient of modern diets for the prevention and treatment of degenerative diseases, such as diabetes mellitus, heart disease, low blood sugar, and obesity (Hughes 1991; Vorster and Venter 1994; Holden and Haytowitz 1998). Pachico (1993) cited beans as the second most important source of dietary fiber for humans and the third most important source of calories among all agricultural products in eastern and southern Africa. One of the most widespread and important diseases of the common bean is rust, caused by the fungus Uromyces appendiculatus. Considerable research has been undertaken in order to understand the environment-hostpathogen interaction and to identify the most effective control measures. The purpose of this chapter is to provide a working reference document for researchers, in particular breeders, pathologists, and students, interested in bean rust, including those who find it necessary to take the disease into account as one aspect of a broader research field. Characteristics of the pathogen and its host, including environmental requirements, economic importance, pathogenic variation, and control are discussed. II. PATHOGEN NOMENCLATURE, MORPHOLOGY, AND LIFE CYCLE A. Nomenclature The basidiomycete Uromyces appendiculatus (Pers.:Pers.) Unger var. appendiculatus (Boerema et al. 1993) was first described in Germany in 1795 by Persoon as Uredo appendiculata phaseoli. Other synonyms are somewhat confusing due to frequent name changes. Those cited by Boerema et al. (1993) are Hypodermium appendiculatum (Pers.:Pers.) Link (1915), Puccinia phaseoli (Pers.) Rebentisch (1804), Uromyces phaseoli (Pers.) Winter (1980), and Uromyces phaseolorum [E.L.R.] Tulasne (1854). Other common names used for the disease in Africa are ‘‘roes’’ (Afrikaans: South Africa), ‘‘ferrugem (do feijoeiro)’’ (Portuguese: Angola, Mozambique), ‘‘kutu’’ (Swahili: Tanzania, Kenya, and the Democratic Republic of the Congo, ‘‘la rouille (du haricot)’’ (French-speaking countries), and ‘‘chiwau’’ (Chechewa: Malawi), which denotes the general burning or scorching effect (fire), although this name is also used for other leaf diseases, such as angular leaf spot (ALS). In Spanish-speaking parts of Latin America, rust is known as ‘‘la roya.’’
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
5
B. Morphology and Life Cycle 1. Asexual Stage. Uromyces appendiculatus, an obligate parasite, is autoecious and macrocyclic, completing its entire life cycle on the common bean (P. vulgaris) (Harter and Zaumeyer 1941). Urediniospores germinate on the surface of the leaf or other aerial part, and the germ tube, tightly appressed to the leaf surface, grows over the epidermis until it reaches a stoma. Once over the stoma, an appressorium forms, in which the physical topography of the host appears to play a key role. It is possibly triggered by an abrupt change in substrate elevation, caused by the stomal guard cell lip (Wynn 1976; Allen et al. 1991). Other signals, possibly oxygen (O2) or carbon dioxide (CO2) concentration, or a pH gradient may be involved (Von Alten 1983). An infection hypha grows into the substomatal cavity, after which the intercellular spaces are colonized, and nutrients are extracted from host mesophyll cells by means of haustoria (Wynn 1976; Mendgen 1978; Von Alten 1983). The surrounding cells are stimulated and preserved at the expense of the uninvaded tissue (Wingard 1935). Resistant accessions often react to haustorial formation with a hypersensitive reaction (HR), which involves dissolution of the contents of the infected cell, collapse of the infected cell (leading to necrosis), or collapse of the haustorium itself without visible cell damage. This usually results in the death of the fungus before spore production (Wingard 1935; Mendgen 1978). After colonization, the mycelium aggregates to form a sorus. This enlarges, and gives rise to thin-walled, single-cell echinulate urediniospores (Harter and Zaumeyer 1941). Approximately 7 to 10 days after infection, the epidermis bursts open, possibly as a result of the pressure of volatile metabolites (Last and Schein 1973), exposing the developing spores to the atmosphere. These darken from golden to cinnamon brown, forming the characteristic uredinia, or pustules, on both the adaxial and abaxial leaf surfaces, but more commonly on the abaxial. Uredinia typically range from 0.2 to 0.9 mm in diameter, but can reach 2 mm and even 4.8 mm (Yarwood 1961). On more susceptible genotypes, secondary and sometimes tertiary sori can develop in concentric circles around the primary pustule (Harter and Zaumeyer 1941), but their formation was found not to be a very consistent characteristic. The mycelial area within the leaf can reach >5 mm within 40 days, its area being greater than that of the sporulating area (Yarwood 1961). Urediniospores are released on a continuous basis and are relatively short-lived (Harter et al. 1935). Depending on the relative humidity (RH) during sporulation, a potential urediniospore production of >20,000 per pustule per day has been calculated (Aust et al. 1984). A susceptibility-temperature-density
6
M. M. LIEBENBERG AND Z. A. PRETORIUS
interaction plays an important role. Urediniospores, which are primarily wind dispersed, often in clusters (Hirst 1953; Ferrandino and Aylor 1987), can germinate as soon as they mature, completing the asexual cycle approximately every 10 to 15 days by reinfecting the host (Harter et al. 1935; Zaumeyer and Thomas 1957). 2. Sexual Stage. According to Waters (1928), environmental factors such as light intensity, temperature, and moisture, either singly or in combination, indirectly influence the life cycle of rust fungi, including U. appendiculatus. These factors affect the metabolism of the host (particularly when the host is weakened) and in this way induce the changeover from uredinial to telial production. Factors such as plant maturity, leaf age, and host response may also play a role (Stavely and Pastor-Corrales 1989). In the field, the replacement (within the same pustule) of urediniospores by dark brown teliospores occurs toward the end of the summer season on older leaves and is common in more temperate climates, such as the mid-northern states of the United States (Zaumeyer and Thomas 1957; Linde et al. 1990; Schwartz et al. 1990; McMillan et al. 2003), Australia (Ogle and Johnson 1974), and South Africa (Liebenberg, unpubl.). Most isolates collected from these areas can be induced to form teliospores in the greenhouse by manipulating host metabolism (Waters 1928; Harter et al. 1935), but teliospores will form spontaneously on leaves kept for longer periods in the greenhouse (Zaumeyer and Thomas 1957; Ballantyne 1978; Linde et al. 1990). Telia have also been observed in tropical South and Central America (J.R. Steadman, pers. commun.). Teliospores are single celled, smooth, sparsely warted or striate and thick walled, with a fragile, hyaline pedicel (Laundon and Waterston 1965). Germination of teliospores (giving rise to the basidium) requires a resting period (Zaumeyer and Thomas 1957). Karyogamy takes place in the teliospore and meiosis in the basidium, the latter giving rise to four single-celled, smooth-surfaced, hyaline basidiospores (Moore-Landecker 1982; Gold and Mendgen 1983b, 1984b). McMillan et al. (2003) concluded that conditions conducive to the emergence of volunteer bean plants were also favorable for basidiospore germination and subsequent bean plant infection. Basidiospores germinate on any aerial surface of the bean plant, forming a single germ tube that grows primarily along or toward the epidermal cell junctions. The fungus adheres to the plant surface by means of an appressorium and surrounding mucilaginous exudate. The appressorium gives rise to a penetration peg that, in contrast to the uredinial germ tube, ruptures the epidermal cell wall, eventually forming an intra- and intercellular hyphal network in the epidermis and underlying tissue; the
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
7
entire process takes up to 72 hours (Gold and Mendgen 1984a). From this network, spermogonia (pycnia), which first become visible as small chlorotic spots, 0.5 to 1.0 mm in diameter, are formed 4 to 5 days after infection (Gold and Mendgen 1984c). After 6 to 7 days, the epidermis is ruptured and spermogonia reach 3 to 5 mm in diameter. These cause localized light yellow chlorosis and malformation of the leaf, giving it a blistered appearance (Groth and Mogen 1978; Gold and Mendgen 1984c; Schwartz et al. 1990; McMillan et al. 1990). Spermatia (pycniospores) (‘‘ þ ’’ or ‘‘’’ mating type) are secreted from the spermogonia in an opaque white nectar, accompanied by receptive hyphae (Groth and Mogen 1978; Gold and Mendgen 1984c). Spermatia are ovate to elliptical, smooth walled, hyaline, and <7.6 mm long (Gold and Mendgen 1984c). Cross-fertilization with spermatia of the opposite mating type is normally performed by insects. Batra and Stavely (1993) reported that the two-spotted spider mite (Tetranychus urticae) was attracted to urediniospores on leaves and speculated that it may also play a role in spermatization. White cup-ike aecia, arranged in a circular cluster 2 to 4 mm in diameter (Schwartz et al. 1990), are formed below the spermogonia after 9 to 12 days. Should fertilization be delayed, nectar secretion continues, and a secondary ring of exudate may be formed (Andrus 1931; Groth and Mogen 1978). On leaves, spermogonia generally form on the adaxial leaf surface, and aecia on the abaxial side. On stems, petioles, and veins, the two structures are adjacent, elliptical, and <10 mm long (Andrus 1931; McMillan et al. 1990, 2003). High relative humidity is necessary for infection by basidiospores (Groth and Mogen 1978), which can occur at a very young stage, probably at or just after seedling emergence. The sexual stage has been reported on the primary leaves, petioles, stems, and the hypocotyl near or just under the soil surface (Schwartz et al. 1990; McMillan et al. 2003). However, pods can also be infected (McMillan and Schwartz 1994). Venette et al. (1978) found both spermogonia and aecia within 60 cm of the soil surface. White aeciospores infect bean plants, particularly the leaves, to form uredinia that give rise to the commonly known rust-colored, asexual urediniospores. The sexual stage has been repeatedly observed on volunteer bean plants under natural conditions in the field in Oregon (Zaumeyer and Thomas 1957), New York State (Jones 1960), North Dakota (Venette et al. 1978), Colorado (Schwartz et al. 1990), and Nebraska (Schwartz et al. 1994b) and is especially common in the spring under a young wheat, maize, or other canopy that can provide a humid microclimate suitable for spore germination, infection, and development (Schwartz et al. 1990, 1994b; McMillan et al. 2003). In Oregon, teliospores were found in large numbers on wooden poles used for staking beans in the field, and spermogonia developed on beans trained
8
M. M. LIEBENBERG AND Z. A. PRETORIUS
on these stakes in the greenhouse (Milbrath 1944). The sexual stage has also been observed outdoors in South Africa under simulated natural conditions (Rijkenberg 1994). The complete life cycle often has been induced in the greenhouse (Andrus 1931; Groth and Mogen 1978; McCain et al. 1990; Groth and Ozmon 1994; McMillan and Schwartz 1994; McMillan et al. 2003). Aecia have been reported from various other parts of the world, including Europe (Milbrath 1944; Hubbeling 1955; Guyot 1957; Wilson and Henderson 1966; Heinze 1974) and in New Zealand (Brien and Jacks 1954). It is therefore probable that the sexual stage is common in temperate climates. However, some races—for example, those occurring in areas with warmer climates such as California, Florida, and northeastern South Africa—appear to have lost the ability to form teliospores (Harter et al. 1935; Zaumeyer and Thomas 1957; Linde et al. 1990; Liebenberg 2003). Davison and Vaughan (1963b) obtained minimal germination of urediniospores stored at 3 to 4 C for 446 days and speculated that urediniospores could overwinter on bean debris and staking poles in Oregon, considering that, in the spring, early rust pustules were found on bean plants closest to stakes. Gross and Venette (2001) reported survival of urediniospores on bean leaves left outdoors over winter in North Dakota, indicating that, even in temperate climates, these could also be a source of initial inoculum in the following crop.
III. SYMPTOMS The disease can be found on all aerial parts but is most common on leaves. Initial symptoms are white to cream-colored circular specks under the epidermis (the developing sori). Rust-colored pustules develop as urediniospores break through the epidermis on both the adaxial and abaxial leaf surfaces, but are more common on the abaxial. Larger pustules often are surrounded by a chlorotic halo. A ring of secondary, and even tertiary, pustules may develop on susceptible genotypes. Circular or irregular brown or gray to black necrotic lesions, ranging from less than 0.3 mm to 3 mm or more in diameter, are also found but often are difficult to detect in the field. In some cases, necrotic lesions may contain sporulating pustules (Fromme and Wingard 1921; Harter and Zaumeyer 1941). These pustules are generally small (Fromme and Wingard 1921; Stavely 1984b; Stavely et al. 1989b) but can reach 0.8 mm or more (Liebenberg 2003). So-called green islands can form around pustules, particularly on chlorotic or senescent leaves (Wingard 1935). Green islands without
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
9
sporulating pustules have also been observed in the field and greenhouse in South Africa (Liebenberg, unpubl.). Premature chlorosis, senescence, and defoliation can also take place due to high respiration rates (Duniway and Durbin 1971b). Pustule type is a function of the race-host interaction (Harter et al. 1935; Harter and Zaumeyer 1941); consequently, where more than one race is present, more than one type can occur simultaneously on the same leaf. Pustule size, normally also a function of the race-host interaction, can be negatively affected by overcrowding resulting from large numbers of infection points and by extreme temperatures and overshadowing. Pustules on the pods, stems, and petioles, when they occur, are elongated. In some cases, pustules become black as urediniospores are replaced by the darker and more robust teliospores on older leaves near the end of the growing season (Zaumeyer and Thomas 1957). Although the uredinial stage can occur on the primary leaves of seedlings, it is generally most prolific during and after flowering (Stavely and Pastor-Corrales 1989).
IV. HOST RANGE A. Genera and Species The main host of U. appendiculatus is the common bean, Phaseolus vulgaris, but the disease has also been reported to occur on other Phaseolus spp. Fromme (1924) confirmed these Phaseolus spp. as hosts of U. appendiculatus: P. coccineus Jacq. (scarlet runner bean), P. lunatus L. (lima bean), P. polystachyus (L.) B.S.P. (year-long bean), and P. vulgaris L. (common bean), as well as the wild species P. leptostachyus Benth. (syn. P. anisotrichus Schltdl), P. coccineus L. subsp. coccineus var. coccineus (syn. P. obvallatus Schltdl.), and P. maculatus Scheele subsp. ritensis (M. E. Jones) Freytag (syn. P. retusus Benth.). It has also been reported on P. acutifolius A. Gray var. acutifolius (tepary bean), Macroptilium atropurpureum (DC) Urb. (syns. P. atropurpureus Moc and Sesse and P. dysophyllus Benth.) (siratro), and some Dolichos and Vigna spp., notably V. adenantha (G.F. Meyer) M.M.S. (syn. P. adenanthus G. Meyer) (wild pea), V. luteola (Jacq.) (hairypod cowpea), V. unguiculata (previously V. sinensis) (cowpea), and V. vexillata (L.) A. Rich (wild cowpea) (Fromme and Wingard 1921; Laundon and Waterston 1965; Stavely and Pastor-Corrales 1989) [taxons updated according to the USDA Germplasm Resources Information Network (GRIN), 2008]. Fromme (1924) distinguished true cowpea rust (Uromyces vignae Barcl.) from U. appendiculatus. This was confirmed by Harter et al. (1935) and Kim et al. (1985).
10
M. M. LIEBENBERG AND Z. A. PRETORIUS
B. Gene Pools of Phaseolus vulgaris Various studies using the phaseolin seed protein (Brown et al. 1982; Gepts and Bliss 1985, 1986; Gepts et al. 1986; Koenig et al. 1990), different allozymes (Koenig and Gepts 1989; Sprecher and Isleib 1989; Singh et al. 1991a,b), random amplified polymorphic DNA (RAPD) markers (Miklas and Kelly 1992; Skroch et al. 1992), and restriction fragment length polymorphism (RFLP) analysis (Chaco´n et al. 2005) provide strong evidence for multiple domestications of wild beans, with two major domestication centres, giving rise to two different gene pools (Andean and Middle American). Races Meso-America, Durango, and Jalisco (Singh 1989; Singh et al. 1991c) as well as race Guatemala (Chaco´n et al. 2005) originated in Central America and include small and medium seed sizes such as small black, pintos, and great northerns. Important production areas for these types are Central America and northern South America, including Brazil, Argentina, and Venezuela as well as the United States. Pintos are also popular in Lesotho and some parts of Zimbabwe. Large-seeded beans originated in the Andes and include races Nueva Granada, Peru, and Chile (Singh 1989; Singh et al. 1991c; Chaco´n et al. 2005). Main production areas include the northwestern countries of South America, such as Colombia, Peru, Ecuador, and Chile, and parts of the United States (Gepts et al. 1988; Van Schoonhoven and Voysest 1989; Voysest et al. 1993, 1994) as well as eastern and southern Africa (Gepts and Bliss 1988; Sprecher and Isleib 1989). Significant quantities of chiefly large-seeded beans are also produced in China, India, and Myanmar, and smaller quantities are produced in European countries such as Belarus, the Ukraine, and Turkey (FAO 2007). Red speckled sugar (RSS) or cranberry beans, as well as calimas (red mottled), large red, large white, and large yellow beans belong to this group (Singh 1989; Voysest et al. 1993). Although the production of small-seeded beans is increasing in many African countries due to their superior disease resistance, they have decreased in popularity in South Africa as they are now generally outyielded by newly released large-seeded cultivars (Liebenberg et al. 2008). Here the production of small-seeded beans is almost exclusively limited to small white canning beans (DPO Statistics, Sept. 2008). Co-evolution between pathogen and host for the two major P. vulgaris gene pools (Middle American and Andes) has been demonstrated for Pseudocercospora griseola (previously Phaeoisariopsis griseola) (causal agent of ALS) and Colletotrichum lindemuthianum (causal agent of anthracnose) (Pastor-Corrales 1996; Chaco´n et al. 1997) and also for the rust pathogen (Steadman 1995; Sandlin et al. 1999; Liebenberg 2003;
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
11
Pastor-Corrales and Aime 2004). In a study using rust isolates from the Americas and a differential set consisting of 30 common bean landraces of known origin, distinct specificity of Andean isolates for large-seeded (Andean) landraces was found, whereas the Middle American isolates exhibited no marked specificity and were more broadly virulent. In addition, RAPD analysis of the isolates produced banding patterns that differentiated the majority into Andean and Middle American populations (Sandlin et al. 1999). Araya and Steadman (1998) and Araya et al. (2004) also reported that their isolates clustered into three main groups, predominately Andean, predominantly Middle American, and a mixed group. The phenotypic reaction of the 1983 common bean international differential set, referred to in this review as ‘‘the 1983 differential set’’ (Table 1.1), could, in turn, be used to separate the differentials into two groups, a Middle American and Andean group, with the exception of ‘Redlands Pioneer’, an Andean-type cultivar, which fell into the Middle American group (Sandlin et al. 1999). Similar results were reported by Pastor-Corrales et al. (2005, 2008) and Jochua et al. (2008) after inoculation of the 2002 common bean international differential set, referred to in this review as ‘‘the 2002 differential set’’ (Table 1.2), with 12 and 14 Beltsville rust races and 56 Nebraskan isolates respectively. The apparently incongruent reaction of ‘Redlands Pioneer’ in all three cases is clarified by the report that the resistance gene in the predominantly Andean cultivar ‘Redlands Pioneer’ (Ur-13) is probably of Middle American origin (Liebenberg et al. 2004a, 2006a). Using both phenotypic and genotypic methods, including the alpha 1 elongation factor, PastorCorrales and Aime (2004) reported that the Middle American gene pool of U. appendiculatus was more diverse and has less host specificity than the Andean gene pool. This indicates that isolates from the Middle American gene pool may be more inclined to employ sexual outcrossing (Aime 2006). In Africa, presumably due to the predominance of largeseeded beans, the most effective sources of disease resistance and, in particular, rust resistance are of Middle American origin (Liebenberg and Vermeulen 1984; Anon. 1988; Liebenberg 1994b; Liebenberg 2003; Jochua et al. 2004).
V. DISTRIBUTION Rust is one of the most widespread diseases of common bean and has been reported from practically all production areas of the world, including many Latin American countries (Graham 1978; Van Schoonhoven
12
a
b
c
d
e
f
g
1
2
3
4
5
6
7
1
4
2
1
4
2
1
Coded Letter tripletz
No.
Designation
Golden Gate Wax
‘KW 814’
Wax (LBr)
MBr
A/MA (Sandlin et al. 1999) Gene of Andean origin?
A (Sandlin and Steadman 1994)
MA
MA/A
A/MA
MA
MA
Small white (SW)
Pinto
A/MA
Gene pooly
Medium white
Seed type
Medium brown Kentucky (MBr) Wonder (KW) 765 KW 780 Medium white (MW)
Pinto 650
California Small White (CSW) 643 (G 5693)
US#3
Accession L.L. Harter and W.J. Zaumeyer L.L. Harter and W.J. Zaumeyer
Original source
L.L. Harter and W.J. Zaumeyer
Unnamed, more than L.L. Harter and W.J. Zaumeyer one, at least one is dominant Ur-6 H.H. Fisher
Ur-4 þ
Ur-B ¼ Ur-2, and Ur-D, may have been heterozygous for Ur-Red (¼Ur-13?) (Ballantyne 1978) Not characterized L.L. Harter and W.J. Zaumeyer Not characterized L.L. Harter and W.J. Zaumeyer
Ur-US#3 tentatively named Ur-8 Not characterized (more than one)
Rust resistance genesx
Table 1.1. First International Differential Set of 20 Phaseolus vulgaris accessions for rust, decided on at the First International Rust Workshop (Stavely et al. 1983), referred to as ‘‘the 1983 differential set.’’
Fisher 1952; Sappenfield 1954; Zaumeyer 1960; Hikida 1961; Ogle and Johnson 1974. Garden bean: McClean and Myers 1990
Harter and Zaumeyer 1941; Stavely 1986; Steadman 1995; PastorCorrales 2001 Harter and Zaumeyer 1941; Kolmer and Groth 1992
Harter and Zaumeyer 1941
Harter and Zaumeyer 1941
Harter and Zaumeyer 1941; Ogle and Johnson 1974; Ballantyne 1978
Harter and Zaumeyer 1941
Pedigree and references for origin/resistance genes
13
h
i
j
k
l
8
9
10
11
12
4
2
1
4
2
Mexico 309 (G 5652)
Ecuador 299 (G 5653) Mexico 235 (G 5732)
Redlands Pioneer
Early Gallatin
Small black (SB)
Medium pink
Medium pink
Green bean (LBr)
MW
MA (Brown et al. 1982; Sandlin and Steadman 1994) MA/A (Sandlin et al. 1999). Resistance probably of MA origin
MA
A/MA (pedigree). Resistance appears to be of MA origin (Ogle and Johnson 1974; Ballantyne 1978) MA
A/MA Gene appears to be of Andean origin as the marker is in all Andean material tested (Miklas et al. 1993; Liebenberg 2003) A (Sandlin and Steadman 1994)
CIAT-Colombia
CIAT-Colombia
Ur-3 þw
Ur-5 (also in B 190)
(continued)
Stavely 1986; Singh et al. 1991a; Steadman 1995 Stavely and Grafton 1985; Stavely 1986; Steadman 1995 Stavely 1982, 1984a
Redlands Greenleaf B/Plentiful: Anon. 1967; Ballantyne 1978; Ogle and Johnson 1974; Liebenberg 2003; Liebenberg and Pretorius 2004b Liebenberg et al. 2004a, 2006a
Australia
CIAT-Colombia
Christ and Groth 1982b; Stavely 1986; Steadman 1995
J.V. Groth
Ur-3 þw
Ur-13 (Ur-C, Ur-D and Ur-Red) Ballantyne 1978
Ur-4
14
m
n
o
p
13
14
15
16
1
4
2
1
Coded Letter tripletz
No.
Accession
NEP 2 (G 4459)
Seed type
Pinto
Green bean (LBr)
SW
Actopan/Sanilac SW Selection (A S)
Olathe
Brown Beauty
(Continued)
Designation
Table 1.1.
MA
MA
MA/A (according to pedigree)
A
Gene pooly
D.R. Wood and J.G. Keenan
Ur-6 þ
B.J. Ballantyne Unknown, (two RR genes, Ur-E and Ur-F; Ur-F in common with ‘NEP 2’ [Ballantyne 1978]) Ur-3 þ w (may have B.J. Ballantyne 4 or 5 RR genes, Ur-F, Ur-I, Ur-J, and Ur-K, with suspected linkage; Ur-F in common with ‘A S 37’ (Ballantyne 1978)
B.J. Ballantyne
Original source
Ur-4
Rust resistance genesx
Derived from San Fernando through mutagenesis: McClean and Myers 1990; Ballantyne 1978; Stavely 1986; Steadman 1995
Ballantyne 1978; Stavely 1986; Steadman 1995 B23/4/DarkRedKidney/3/ UI78//UI78/4500: McClean and Myers 1990; Wood and Keenan 1982; Grafton et al. 1985; Stavely 1984a; Stavely et al. 1989b, 1994b Ballantyne 1978
Pedigree and references for origin/resistance genes
15
r
S
–
18
19
20
–
1
4
2
Later excluded: resistance the same as that of ‘KW 780’ (Stavely 1984)
One unnamed, probably more than one
MA
Mountaineer White Half Runner
Ur-3 þ w
MA
SB 51051 (? ¼ G 4489¼ Cuilapa 72, originally from Guatemala) SB Compuesto Negro Chimaltenango (CNC) R. Christen and E. Echandi
CIAT-Colombia
Ur-3 w (2 linked genes, B.J. Ballantyne designated Ur-M (¼Ur-3) and Ur-N (Ballantyne 1978)
MA
SW
Aurora
Composite of Guatemalan black beans: McClean and Myers 1990; Christen and Echandi 1967; Rasmussen et al. 2002; Wang et al. 2007
Black Turtle Soup/Cornell 49-242: McClean and Myers 1990; Ballantyne 1978; Kardin and Groth 1985; Stavely 1986; Steadman 1995 Stavely 1986; Steadman 1995
y
Limpert and M€ uller 1994. Andean (A), Middle American (MA). Unless otherwise indicated, gene pool origin is based on analysis of the seed storage protein phaseolin (Brown et al. 1982; Gepts et al. 1986; Sandlin and Steadman 1994), on allozyme analysis (nine loci) (Singh et al. 1991a), as reported in Sandlin et al. 1999, or according to pedigree (Ogle and Johnson 1974; Ballantyne 1978; or McClean and Myers 1990). x Gene symbols as proposed by Kelly et al. 1996. w The presence of the same gene (Ur-3) in Ecuador 299, Mexico 235, NEP 2, Aurora and 51051 needs verification by means of genetic studies. The precise nature of the additional resistance in tehse accessions should also be determined.
z
q
17
16
Letter
A
B
c
d
No.
A1
A2
A3
A4
8
4
2
1
PC 50
Montcalm
Redlands Pioneer
Early Gallatin
Binary system valuez Accession
Designation
Dark Red Kidney Pompadour (red mottled or Calima)
Large Brown (LBr)
Medium White
Seed type A/MA (gene appears to be of Andean origin as the marker is in all Andean material tested (Miklas et al. 1993) A (Sandlin and Steadman 1994) A/MA (according to pedigree) (Resistance appears to be of MA origin [Ogle and Johnson 1974, Ballantyne 1978, Liebenberg et al. 2006a]) A/MA (according to pedigree) A
Gene pooly
References/Comments
Ur-9, Ur-12
Uncharacterised
GN#1/Dark Red Kidney: McClean and Myers 1990 Sandlin and Steadman 1994; Voysest et al. 1993, from the Dominican Republic
Christ and Groth 1982b; Kolmer and Groth 1982; Stavely 1986; Kelly et al. 1993; Stavely et al. 1994b; Stavely and Kelly 1996; Ur-13 [according to Anon. 1967; Ogle and Ballantyne (1978): Johnson 1974; Ur-C, Ur-D and Ballantyne 1978; Ur-Red] Liebenberg 2003; Liebenberg and Pretorius 2004a,b; Liebenberg et al. 2006a
Ur-4
Rust resistance genesx
Table 1.2. Second International Differential Set of 12 Phaseolus vulgaris accessions for rust, decided on at the Third International Rust Workshop (Steadman et al. 2002a) (referred to as ‘‘the 2002 differential set’’).
17
32
1
2
4
8
f
A6
MA1 g
MA2 h
MA3 i
MA4 j
16
e
A5
Mexico 235
Mexico 309
Aurora
GN 1140
PI 260418
Golden Gate Wax
Medium pink
Small Black (SB)
Black and brown speckled on white Great Northern (MW) Small White (SW)
Wax (LBr)
MA (Brown et al. 1982, Sandlin and Steadman 1994) MA/A (Sandlin et al. 1999, (resistance probably of MA origin) MA
MA
MA
A (Sandlin and Steadman 1994) A/MA (Sandlin et al. 1999) Gene of Andean origin? A (according to origin: Bolivia)
Ur-3 þ
Ur-5
Ur-3
Ur-PI-260418, possibly two other unlinked genes Ur-7
Ur-6
Stavely and Grafton 1985; Stavely 1986 (continued)
Pinto #5/GN UI 123: McClean and Myers 1990; Augustin et al. 1972 Black Turtle Soup/Cornell 49–242: McClean and Myers 1990; Ballantyne 1978; Kardin and Groth 1985; Stavely 1986 Stavely 1982; Stavely 1984a
Stavely 1989b; from Bolivia, Pastor-Corrales 2005
Garden bean: McClean and Myers 1990
Fisher 1952
18
32
MA6 l
PI 181996
SB
Compuesto SB Negro Chimaltenango (‘CNC’)
Seed type
MA (Stavely 1990d, 1998)
MA
Gene pooly
Ur-11 þ
One unnamed, probably more than one
Rust resistance genesx
Christen and Echandi 1967; composite of Guatemalan black beans: McClean and Myers 1990; Rasmussen et al. 2002 Stavely 1990d, 1998d; Steadman 1995
References/Comments
y
Habgood 1970. Unless otherwise indicated, gene pool origin is based on analysis of the seed storage protein phaseolin (Brown et al. 1982; Gepts et al. 1986; Sandlin and Steadman 1994), on allozyme analysis (nine loci) (Singh et al. 1991a), as reported in Sandlin et al. (1999), or according to pedigree (Ogle and Johnson 1974; Ballantyne 1978; or McClean and Myers 1990). x Gene symbols as proposed by Kelly et al. 1996.
z
16
Letter
Binary system valuez Accession
MA5 k
No.
(Continued)
Designation
Table 1.2.
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
19
and Voysest 1989; Steadman 1995), the more humid parts of North America (Fromme and Wingard 1921; Netto et al. 1969; Hagedorn and Wade 1974; Groth and Scrum 1977; Graham 1978; CIAT 1983), Africa (Kaiser 1976; Howland and Macartney 1966; Allen 1995), Europe (Rodrigues 1955; Stavely and Batra 1991), Australasia (Ballantyne 1978; Ryley et al. 1990; Braithwaite et al. 1994), New Zealand (Brien and Jacks 1954), China (Wang Su et al. 1998), Asia, India, and smaller island groups (summarized in Zaumeyer and Thomas 1957; CIAT 1983 and Stavely and Pastor-Corrales 1989; Stavely and Batra 1991). It is apparently found wherever Phaseolus beans, either wild or cultivated, occur (Laundon and Waterston 1965). The first report of the fungus in South Africa was in 1909 in the Transvaal province (although it had most likely been present for many years), and it was noted over the years to be widespread and destructive (Doidge 1924; Doidge and Bottomley 1931; Doidge et al. 1953). By 1945, it had been reported in all provinces as well as in Zimbabwe and Mozambique on P. vulgaris and on P. acutifolius Gray var. latifolius Freem. (tepary bean) in the eastern Transvaal, and was cited as common and widespread on Phaseolus coccineus Linn. (locally known as large white kidney beans) (Doidge 1950). It occurs widely in Africa in at least 19 of the 20 eastern and southern African countries (Allen 1995) but regularly reaches epidemic proportions in the cooler, more humid highland areas, on the eastern escarpment, and in the islands of Madagascar and Mauritius (Howland and Macartney 1966; Kaiser 1976; Liebenberg and Deschodt 1977; Stoetzer and Waite 1984; Allen et al. 1989; Habtu 1990; Mbewe and Mulila 1990; Saumtally and Autrey 1990; Liebenberg 1994a; Wortmann and Allen 1994; Steadman et al. 2002a). According to Wortmann et al. (1998), rust is responsible for an estimated 191,400 t per annum yield loss in sub-Saharan Africa.
VI. EPIDEMIOLOGY A. Dissemination The chief dissemination method of bean rust is wind, and in particular gustiness, which enables the escape of spores from the canopy (Hirst 1953; Aylor 1990). Alternating periods of high humidity and windiness at fairly cool temperatures are, therefore, important. Although wind accounts for dissemination over long distances, other agents, such as migratory birds, animals, insects, clothing, water, vehicles, and implements, can also play a role (Nagarajan and Singh, 1990). The disease is
20
M. M. LIEBENBERG AND Z. A. PRETORIUS
not, however, seedborne (Zaumeyer and Thomas 1957). Heavy rain or overhead irrigation can retard dissemination (Chupp and Sherf 1960; McMillan 1994). Under normal circumstances, urediniospores are short lived (Harter et al. 1935), but dehydration, followed by exposure to low temperatures, is known to considerably extend their survival period (Schein and Rotem 1965). These conditions would be experienced at high altitudes during dissemination and may account for the ability of the fungus to infect isolated bean fields and the occurrence of severe epidemics in the absence of local teliospore production, as is experienced in Florida in the United States (Townsend 1939, in Zaumeyer and Thomas 1957). Wheat rust (Puccinia graminis f. sp. tritici) is known to spread in the direction of prevailing winds from Australia to New Zealand, a distance of over 2,100 km (Luig and Watson 1970). Teliospores, and to a lesser degree also urediniospores, can survive for considerable periods in bean debris (Gross and Venette 2001). In many frost-free tropical areas, especially the highlands of eastern Africa, subsistence farmers cultivate two crops of beans per year in small plots, planting at various times according to the availability of land, labor, and moisture. As a result, beans at varying stages of development are present during the greater part of the year within the same district, and bean debris is prevalent (Howland and Macartney 1966). Under these circumstances, urediniospores probably are responsible for the propagation of the fungus. B. Environmental Influences Ideal conditions for rust development are temperatures ranging from 17 to 25 C, occurring simultaneously with high RH (>95%) for at least 7 to 8 hours (dew formation is critical for infection), interspersed with dryer periods that favor dispersal (Harter et al. 1935; Hirst 1953; Mendes and Bergamin Filho 1989; Stavely 2005). Although both temperature and humidity, in particular, appear critical, it is the interaction between these two factors that is important. Due to local adaptation, genotypes originating from different climatic regions may exhibit different environmental optima. 1. Temperature. Temperature is an important factor in the development of rust. Changes of only 5 to 6 C for 4 to 8 hours can significantly influence the epidemiology of the disease. Night temperatures of 26.7 C, for instance, inhibit pustule development (Schein 1961). Although the same environmental conditions favor infection for all isolates screened at the University of Nebraska, Lincoln, isolates originating from high
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
21
altitudes—for example Ecuador—do not function at temperatures above 27 C (J.R. Steadman, person. commun.). The variation in temperatures reported to favor urediniospore germination may be due to local adaptation of the races studied. Optimum temperatures reported for germination are from 12 to 17 C (Harter et al. 1935), 10 to 25 C (Naito 1951), 12.5 to 18 C (Shands and Schein 1962), 15 to 24 C (Bell and Daly 1962), and 17.5 to 22.5 C (Imhoff et al. 1981). These discrepancies probably are due to adaptation of the fungus to local climatic conditions. Germination decreased rapidly, and germ tubes were shorter above and below the temperatures reported by Harter et al. (1935). No germination occurred at very low temperatures (below 1.8 to 4 C) or at high temperatures (above 27.5 to 35 C) (Harter et al., 1935; Bell and Daly 1962; Imhoff et al. 1981). A cold shock, however, appears to be beneficial. Schipper et al. (1969) reported 5% germination (on moist filter paper) after 6 hours, rising to <25% after 25 hours, of washed urediniospores exposed to 25 C, whereas 75% germination was obtained after 4 hours (rising to 78% after 25 hours) after exposure to 4 C for 2 hours. Temperatures favoring germination and infection differ somewhat. Optimum infection has been reported to take place at 17 C (Harter et al. 1935; Mendes and Bergamin Filho 1989) or 18 to 21 C (Shands and Schein 1962), with a sharp decrease in number of pustules per leaf at incubation temperatures of 21 to 25 C (Mendes and Bergamin Filho 1989) and no infection at 27 C or above (Harter et al. 1935). Minimum temperatures for infection may be determined by host tolerance to cold injury (Bell and Daly 1962). Von Alten (1983) reported that temperatures of 16 to 20 C favored appressorium formation whereas 24 C reduced it. According to Schein (1961), low temperatures (21.1 /15.6 C day/night) retarded pustule development and sporulation. No symptoms developed at temperatures of 32.2 /26.7 C, but the fungus was not killed. Exposure to high temperatures (>34 to 36 C) for extended periods (>60 hours) has been reported to cause death of the mycelium in the leaf (Sempio, in Zaumeyer and Thomas 1957; Groth and Mogen 1978). Farina et al. (1981) reported that heat treatment at 50 C for 20 seconds resulted in death and encasement of the fungal haustoria and hyphae but negligible damage to the host. Infection type may also be influenced by temperature; for instance, Ballantyne (1978) observed that for one particular isolate, small pustules, usually with necrosis, developed at temperatures above 25 C; but at temperatures below 20 C, larger pustules without necrosis developed. On leaves already infected for 96 to 120 hours, Schein (1961) observed the development of necrosis around pustules after 5 days exposure to temperatures of 32.2 C. The most recent
22
M. M. LIEBENBERG AND Z. A. PRETORIUS
infections were aborted, whereas older infections became static. Wei (1937), however, found that temperatures from 16 to 28 C had little effect on infection type but that low temperatures did prolong incubation period. Imhoff et al. (1981) found that the germination of spores produced at 16 and 21 C was twice that of spores produced at 24 C, and Imhoff et al. (1982) reported that sporulation from previously active pustules ceased altogether within 3 days when plants were transferred to 27 C. Schein (1961) points out that mean temperatures should not be used to characterize field or laboratory conditions, as it is the actual temperature that determines disease expression, with variation in either day or night temperatures influencing both development and sporulation; for instance, the combination of high day temperatures (32.2 C) and low night temperatures (15.6 C) greatly retarded development. Gold and Mendgen (1983a) reported that the dormancy period for teliospores lasted approximately 9 months after storage at 4 C. Germination percentage increased sharply after 36 to 42 months storage and decreased thereafter due to increased mortality. The resting period of teliospores was shortened by exposure to temperatures below freezing (Zaumeyer and Thomas 1957; Gold and Mendgen 1983a). Germination occurred between 12 to 23 C, with an optimum at 18 C, but was suppressed at 26 C, although teliospores were not killed (Gold and Mendgen 1983a). Heat treatment of teliospores at 28 to 32 C for 4 days in the dark prior to germination, followed by incubation at 21 C, increased germination percentages; however, this seriously inhibited infection of bean plants, and spores were killed by temperatures of >34 C (Gold and Mendgen 1983a). Groth and Mogen (1978) achieved spermogonium development in the greenhouse at 22 to 26 C in both sun and shade. 2. Humidity and Leaf Surface Moisture. Leaf surface moisture plays a key role in both germination and infection, and the disease causes yield loss only where sufficient humidity to promote leaf surface moisture occurs. Hydration of dry urediniospores was found to increase germination and shorten germination time (Schein 1962; Curtis 1966). Harter et al. (1935) reported that within appropriate temperature ranges, high levels of infection were obtained when plants were exposed to a RH of 96% or higher, provided free moisture was present on the leaves. However, infection levels were considerably reduced at a RH of 95%, and no infection took place at lower humidity levels. Air movement, which caused evaporation of moisture from the leaves preceding penetration, also inhibited infection. Yarwood (1961) and Imhoff et al. (1982)
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
23
observed that a greater percentage of pustules erupted under humid conditions, and more spores were produced by pustules exposed to humid conditions than those exposed to low RH. Rehydration followed by a period of high RH was also found to be a prerequisite for teliospore germination. This started 3 to 5 days after exposure to high RH (Andrus 1931; Groth and Mogen 1978; Gold and Mendgen 1983c). 3. Dew Period. Under ideal conditions of near 100% RH, Harter et al. (1935) found that at least 8-hour exposure was a prerequisite for infection by uredinospores, with an increase in the number of infections taking place after a 10-hour exposure, and an optimum of between 12 to 18 hours. Host genotype differences were also found. Mendes and Bergamin Filho (1989) reported a minimum of 4 hours of high humidity necessary for the development of pustules, and attained maximum infection (measured as the number of sporulating pustules per leaf) after 22 hours. Exposure to periods of more than 48 hours of high humidity resulted in lower levels of infection, apparently due to deterioration in the vigor of the host (Harter et al. 1935). Harter et al. (1935) concluded that the occurrence of suitable climatic conditions was far more conducive for the development of an epidemic than the presence of large amounts of inoculum. As night temperatures of between 10 to 18 C are common in many beangrowing areas, it appears that the occurrence of high humidity or free moisture on leaves (interspersed with drier, windy periods conducive to spore dispersal) is the most critical factor in the development of an epidemic. Even with the low percentage of infection taking place during 8-hour exposure to high humidity, exponential increases in the number of pustules will still occur during recurring periods of high humidity and suitable temperatures and result in the development of epidemics. 4. Light. Von Alten (1983) reported that appressorium formation was maximal under intermittent light-dark conditions but was reduced by exposure to continual light, and Harter et al. (1935) found that exposure to >48 hours of subdued light during the infection period led to reduced infection and delayed pustule development. Any factor adversely affecting the condition of the plant, including low light levels, was also detrimental to the development of the rust fungus. As was the case with temperature, Wei (1937) reported that the infection type on highly resistant and highly susceptible plants was the least affected by light intensity. Low light intensities tended to lengthen the incubation period
24
M. M. LIEBENBERG AND Z. A. PRETORIUS
and increase necrosis on susceptible hosts. Low light intensity or decreased day length can also stimulate the changeover from urediniospores to teliospores (Waters 1928). Alternating periods of darkness and light (15,000 to 26,000 lux with an optimum intensity of 17,000 lux) were reported to be a prerequisite for teliospore germination. No germination of teliospores occurred under constant light or constant darkness (Gold and Mendgen 1983c; French et al. 1993). Basidiospore release was subject to a rhythmic nocturnal periodicity (at high RH). The timing of basidiospore release was determined by the length of the photoperiod, but release was temporally inhibited by continuous light or continuous darkness (Gold and Mendgen 1983c). 5. Nutrition and Volatile Substances. Infection by urediniospores was enhanced by excess nitrogen and low levels of potassium in the soil but was not affected by levels of other nutrients within normal limits (Wei 1937). After testing various volatile chemical compounds, French et al. (1993) found that aldehydes (isobutyraldehyde, isovaleraldehyde, and furfural) and esters (methyl isobutryrate, propyl propionate, and allyl butyrate) led to a 30% increase in germination of teliospores (in alternating light and darkness) compared to no treatment. Exposure (for 8 to 19 days) of both fresh and stored spores to the volatiles released from bean seedlings increased germination rates dramatically by more than 80%. However, longer periods of exposure led to high mortality rates (Gold and Mendgen 1983c). 6. pH and Ion Concentration. Both pH and ion concentration of the medium in which the urediniospores germinate affect germination levels. A pH of 6 to 7 is optimal for germination; very low germination levels occurred below pH 5 and above pH 8 (Bell and Daly 1962). Baker et al. (1987) determined that calcium ions (Ca2 þ ) (at 0.1 to 3 mM) stimulated the germination of urediniospores. Magnesium ions (Mg2 þ ) (at 1 mM) had a slight stimulatory effect. The effect of the monovalent sodium (Na þ ) and potassium (K þ ) ions was negligible and that of manganese (Mn2 þ ) was negative at a concentration of above 200 mM. Soil pH has been reported to influence pustule diameter, with larger pustules forming on plants in low pH (5.8) potting medium compared to those in soils of pH 6.5 or pH 7.9 (Zaiter et al. 1991). This appears to result from the effect of pH on the Cl, Mn2 þ , and K þ concentrations in leaves. Pustule diameter was positively correlated with Cl (2.0 to 17.9 g kg1)
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
25
and Mn2 þ (51 to 332 mg kg1) in leaves. There was also a host genotypesoil ion interaction. C. Leaf Age Influences Tissue age strongly influenced receptivity (defined as the number of visible pustules forming per unit of applied inoculum). Smaller or undeveloped pustules were observed for very young (unfolding) leaves. Primary leaves were most receptive while rapidly expanding, with maximum receptivity was reached when leaves were approximately 20 to 40% expanded, depending on the genotype. Receptivity declined sharply after approximately 40% expansion, and older leaves generally developed smaller and fewer pustules. Similar results were obtained for second and third trifoliolate leaves, with the result that only one leaf was highly susceptible at any given time (Harter and Zaumeyer 1941; Schein 1965; Groth and Urs 1982). The duration of the susceptible period of inoculated leaves was increased (by an unspecified time) by removal of the apical meristem above the leaf. This also delayed senescence (Schein 1965). Germination rate of urediniospores was not affected by leaf age, but infection frequency on fully grown leaves was 22% that of expanding leaves. This was apparently due to inhibited appressorium formation, although the mechanism involved could not be determined. Decreased stoma density may also play a minor role (Groth and Urs 1982; Von Alten 1983). Shaik and Steadman (1989a,b) obtained a highly significant negative correlation between pustule area on a leaf and leaf age, leaf size, and plastochron index for a susceptible reaction. However, these parameters were not significantly correlated when associated with a resistant (small-pustule) reaction. Imhoff et al. (1981) determined that germination of spores from young leaves (inoculated 11 days after plant emergence) was three times that of spores produced from old leaves (inoculated 25 days after emergence). This effect on spore germination was also found when spores from young pustules were compared to spores from old pustules.
VII. ECONOMIC IMPORTANCE Losses due to rust can be dramatic. There are records of total destruction of the crop, for instance, in the San Gabriel Valley, California, in 1918 (Milbrath, in Fromme and Wingard 1921) and in parts of Colorado in 1927 (Zaumeyer and Thomas 1957). De London˜o and Anderson (in Graham 1978) reported an estimated loss of US$1 million in the Cauca
26
M. M. LIEBENBERG AND Z. A. PRETORIUS
Valley, Colombia, South America, due to bean rust. In the Americas, yield losses vary greatly across the continents; for example, <54% (<1233 kg ha1) in North Dakota (Venette and Jones 1982), 40% to 50% in Nebraska and Colorado (Steadman and Schwartz 1982), and <75% in irrigated commercial fields in Colorado (Schwartz 1984). VelezMartinez et al. (1989) reported yield losses of 75% in susceptible varieties in Puerto Rico in 1985, and Crispin and Campos (1976) named rust as one of the major diseases limiting bean production in Mexico. Venette and Jones (1982) found yield losses to be related directly to the logarithm of disease severity (measured as pustules cm2). In Nebraska, Lindgren et al. (1988) estimated that a 10% increase in rust severity brings about an 8.2% yield loss. Yield increases of <187% were obtained in Colorado (Schwartz et al. 1995) and <100% in Colombia (Panse et al. 1997) in fungicide-protected compared to unprotected beans. In Africa, serious bean yield losses are experienced on a regular basis in the more humid areas, aggravated by the fact that, in many districts, beans are present in the fields during the greater part of the year, providing a continual supply of inoculum (Howland and Macartney 1966). Almost total yield loss has been experienced in Ethiopia on susceptible cultivars (Habtu 1987b, in Habtu 1990). Omunyin et al. (1984) reported serious outbreaks of the disease in Kenya, where the damage to green beans was particularly significant. Also in Kenya, Kimani et al. (1990) cite yield losses varying between 18% to 100%, and Gridley (1990) presents similar figures for eastern African countries as a whole. For fungicide trials using susceptible commercial cultivars, fivefold yield increases above that of the unsprayed control have been recorded in Ethiopia (Habtu 1994) and up to fourfold increases in South Africa (Strauss and Killian 1996; Strauss 1997, 1999). Of the 14 economically important bean diseases in Africa, Wortmann and Allen (1994) ranked rust among the six most important for Africa as a whole and the second most important for southern Africa. Yield losses also have been reported in Queensland, Australia (Ryley et al. 1990), and in China (Wang Su et al. 1998). In parts of Turkey, where it severely affected crops, rust was reported to be the most important fungal disease (Rudolph and Baykal 1978). Yield losses appear to be primarily the result of a reduction in the available leaf area, which, according to Mersha and Hau (2008), was reduced by <46% on a susceptible cultivar as a result of relatively mild epidemics induced in growth chambers. Damage to bean crops not only causes a decrease in the number of seeds but also leads to a loss of quality and decreased seed size resulting from poor pod fill due to loss of photosynthate (Yarwood 1965; Steadman et al. 1986). Pod lesions can also blemish pods in the case of green beans
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
27
(Foster 1947). Steadman et al. (1986a) reported a highly significant correlation between rust severity and yield, total number of pods, total number of seeds and seeds per plant, and mention that early rust intensity could be used to predict yield loss. The most accurate yield loss prediction was, however, obtained when rust severity was recorded approximately 2 weeks before maturity (Lindgren and Steadman, 1992). These authors also found indications that yield losses became significant when rust infection levels reached 5% to 20%. This level was lower if other stress factors were present. Lindgren et al. (1995) reported that the relationship between rust severity and yield loss due to rust was linear and that an estimate of rust-induced yield loss (in kg ha1) for any given year could be obtained by multiplying by 19 the percentage leaf area with rust symptoms at 72 days. Lopes and Berger (2001) compared the effects of anthracnose (caused by Colletotrichum lindemuthianum) and rust on photosynthesis in bean. At all disease levels, anthracnose had a significant positive effect on the photosynthesis of the leaf area not covered by lesions. Rust, however, followed a different pattern. When rust severity was low (<30%), reduction in photosynthesis was proportional to the leaf area covered by pustules. However, when rust severity was >30%, chlorophyll content decreased markedly, and photosynthetic rate of leaves with rust severity of between 70% and 90% was near zero. The effect on yield was not measured. When comparing the effects of ALS and rust on yield loss, De Jesus et al. (2001) reported that, although in their experiments rust did not cause significant defoliation (in contrast to ALS), it did significantly decrease yield. These authors suggested that this was due to the drain on carbohydrates brought about by rust. Both of the above groups of authors observed no interaction between the two diseases studied. The strongly detrimental effect of rust appears to be due to the creation of a ‘‘pathological sink’’ operating at the expense of new tissue formation (Wittmann and Schonbeck 1995). Bassanezi et al. (2001), however, reported that the discrepancy between the visual and virtual leaf area affected by disease was greater for anthracnose and for ALS than for rust (where the virtual lesion represents the area of foliage where photosynthesis is nil). It is clear that more research is needed in this area. However, the most important aspect is the detrimental effect of rust on yield and quality, which appears to be generally more serious than for most other fungal diseases. This may also be partly due to the fact that, in Africa, rust generally appears at an earlier stage than ALS and anthracnose, already competing with the host for nutrients from the early pod-fill stage.
28
M. M. LIEBENBERG AND Z. A. PRETORIUS
Transpiration rate and average stomatal aperture of P. vulgaris are adversely affected by rust. During the presporulation stage, daylight transpiration rate of diseased leaves was significantly less than that of the control, and a linear decrease in average stomatal aperture (to a minimum of 1 mm at 65 pustules cm2) in the light was observed as infection density increased, the latter reaching a plateau at 75 pustules cm2. At maximum effect, average stomatal aperture of diseased plants was approximately 30% that of the control. This appears to be due to inhibition of stomal opening by the pathogen, which also reduced the rate of stomal opening. At the onset of sporulation, the effect was reversed due to the ruptured epidermis, and the transpiration rate of diseased leaves (under both light and dark conditions) was significantly greater than that of the control (Duniway and Durbin 1971b). When subjected to mild drought conditions [1300 ft-c (approximately 14,000 lux), 27 C, and 55% RH], diseased plants became significantly more susceptible to drought. Diseased plants wilted at soil water potentials of greater than 1 bar, whereas healthy plants wilted only when soil water potential fell below 3.4 bar. This was chiefly due to physical damage to the cuticle caused by sporulation. Water supply to leaves of diseased plants was also impaired, indicated by the reduced root to shoot ratio (Duniway and Durbin 1971a).
VIII. PATHOGENIC VARIATION The high pathogenic variation of U. appendiculatus (Harter and Zaumeyer 1941; Stavely 1984b; Stavely et al. 1989b; Linde et al. 1990; Stavely 1990a) has been a cause for concern to bean producers for many years, causing sudden and unexpected yield losses in areas where rust, although present, was not considered a problem or where resistant cultivars had been introduced (Weaver and Markus 1949; Zaumeyer 1960; Graham 1978). Watson (1970) mentions that pathogens undergoing sexual recombination on the normal host are most likely to give rise to new races. The sexual stage of U. appendiculatus is known to occur in the more temperate production areas, especially on volunteer plants growing in an ideal microclimate under the canopy of rotation crops, such as wheat. This is thought to be largely responsible for the perpetuation of the fungus from season to season (Milbrath 1944) and also for the origination of new races (Schwartz et al. 1990). Groth and Mogen (1978) successfully crossed two single pustulated derived races to obtain unequivocal crosses, demonstrating that new races can be expected to arise in this manner. Due to the great variation in
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
29
pathogenicity, regardless of geographical region or climate, it is thought that the sexual stage may also occur in subtropical environments (Stavely et al. 1989b). The area surrounding Pietermaritzburg in KwaZulu-Natal, South Africa, where the sexual stage has been reported (Rijkenberg 1994), is generally classified as subtropical, and beans are grown by small-scale farmers during most of the year. In spite of expectations to the contrary, Groth et al. (1995) found that comparable diversity existed not only in sexually reproducing populations (those that produced teliospores) but also in asexually reproducing populations (those that fail to produce teliospores). Jochua et al. (2008), using 380 isolates collected from widely diverse regions, reported that the number of unique races found was higher in fields in tropical regions than in temperate regions. It would, therefore, appear that, for the common bean, pathotype diversity may mirror the general tendency toward higher species diversity in tropical and subtropical regions and that, although sexual reproduction may occur in the full range of climatic regions, pathotype diversity is not necessarily dependent on sexual reproduction. In a study of the interaction between virulence and resistance genes, Christ and Groth (1982b) found evidence for a gene-for-gene relationship between the rust pathogen and bean host. The resistance gene Ur-8 (previously named Up1) in the accession ‘US#3’ was matched to two virulence loci (named UpA1 and UpV3) in the two isolates used, and the resistance gene Ur-4 (previously named Up2) in ‘Early Gallatin’ was matched to the virulence locus UpA2 present in both isolates. For UpA1 and UpA2 avirulence was dominant, whereas for UpV3, virulence was dominant (Christ and Groth 1982a). Considerable work has been undertaken to study the variation in the fungus over the past 60 years, and characterized races have been instrumental in the identification and tracing of resistance genes. In 2008, Alleyne et al. designed a specific primer set (ARA-2) that was able to separate rust isolates from Colorado and Nebraska, indicating that changes in the pathogen are localized. A. Standard Differentials One of the earliest differential sets of seven lines, compiled by Harter and Zaumeyer (1941), consisted of ‘US#3’, ‘Bountiful’, ‘California Small White (CSW) 643’, ‘Pinto 650’, ‘Kentucky Wonder (KW) 765’, ‘KW 780’, and ‘KW 814’. Other authors, such as Waterhouse (1954), Fisher (1952), Sappenfield (1954), Zaumeyer (1960), Hikida (1961), and Ogle and Johnson (1974), used this set and modified it with important
30
M. M. LIEBENBERG AND Z. A. PRETORIUS
local cultivars, especially ‘Golden Gate Wax’ (GGW). Differentials used by many of the early authors have been summarized by Ballantyne (1974 and 1978). During the First International Rust Workshop held in Puerto Rico in 1983, a set of 20 differentials, including 7 of the above, was proposed, (Stavely et al. 1983; Stavely 1984b) (the 1983 differential set, Table 1.1). The number was later reduced to 19 due to duplication (Stavely 1984b). Six or more host reactions to different races have been observed on these lines, making it possible to differentiate numerous races (Stavely and Steadman, 1992). This differential set has been widely used, especially in the Americas and in South Africa. In March 2002, at the Third International Rust Workshop held in South Africa, a new differential set (the 2002 differential set, Table 1.2) was proposed (Steadman et al. 2002a). This set gives wider representation to the Andean gene pool (poorly represented in the previous set), and consists of only 12 lines (six from the Andean and six from the Middle American gene pools). Duplication, especially of accessions carrying the Ur-3 and Ur-4 resistance genes, is also eliminated (Stavely 1986; Kelly et al. 1996; Steadman et al. 2002a). It was decided to employ the binary system (Habgood 1970) to denote races (modified by dividing Andean and Middle American gene pools by a hyphen). Pustule grades 1, 2, and 3 are regarded as resistant, whereas grades 4, 5, and 6 are regarded as susceptible. The probable Middle American origin of the resistance gene Ur-13 (Liebenberg et al. 2004a, 2006a), present in the predominantly Andean cultivar ‘Redlands Pioneer’ (chosen as a representative of the Andean gene pool) suggests that this set is also biased toward the Middle American gene pool (Liebenberg 2003). Since the information obtained from the discarded differentials is very useful for purposes of comparison and finer differentiation, important new races will most likely be defined on both the old and the new set as well as on locally important accessions. B. Designation of Races Ballantyne (1978) designated races by the code letters (a, b, c, etc.) of the differentials on which they are virulent. This is, however, not practical for use with more than six or seven differentials. The binary code (Habgood 1970) has also been used by the Centro Internacional de Agricultura Tropical (CIAT) for designation of ALS and anthracnose races. Although simple to use for small numbers of differentials, it has the disadvantage of becoming clumsy and less easy to interpret when large numbers of differentials are involved. Limpert and M€ uller (1994) (Table 1.3) have proposed the use of coded triplets for race designation.
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
31
This system has the advantage that the designation of each differential is immediately apparent, even to someone not familiar with the races. The system also retains its simplicity and ease of use with larger sets of differentials. For this reason, this system (indicated in square brackets after the race number) has been used in this review for races characterized with the 1983 differential set (Table 1.3). Table 1.3. Coded tripletsz (Limpert and M€ uller 1994) applied to the 1983 common bean International Differential Set for Uromyces appendiculatus. No 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 z
Cultivar US#3 California Small White (CSW) 643 Pinto 650 Kentucky Wonder (KW) 765 KW 78 KW 814 Golden Gate Wax Early Gallatin Redlands Pioneer Ecuador 299 Mexico 235 Mexico 309 Brown Beauty Olathe Actopan/Sanilac selection (A S) 37 NEP 2 Aurora 51051 Compuesto Negro Chimaltenango (CNC)
Triplet
Cultivar grouping
Triplet code
1 1 1 2 2 2 3 3 3 4 4 4 5 5 5 6 6 6 7
1.1 1.2 1.3 2.1 2.2 2.3 3.1 3.2 3.3 4.1 4.2 4.3 5.1 5.2 5.3 6.1 6.2 6.3 7.1
1 2 4 1 2 4 1 2 4 1 2 4 1 2 4 1 2 4 1
Only figures 1, 2, and 4 are used. Codes are only allocated when a cultivar is susceptible, and the codes within each triplet are summed. The differential set is divided into sets of three which are then numbered 1.1, 1.2, 1.3, 2.1, 2.2, 2.3, etc. The last triplet may be incomplete if the set does not consist of a multiple of three. Summed codes are written consecutively, for example 7,7,3,0,0,0,0 which means that the first eight accessions were susceptible and the rest resistant. A ‘‘1’’, ‘‘2’’ or ‘‘4 ‘‘ indicates that only that particular accession within the triplet is susceptible, a ‘‘3’’, that accessions one and two are susceptible, a ‘‘5’’ that accessions one and three are susceptible, a ‘‘6’’ that accessions two and three are susceptible, and a ‘‘7’’ that all three accessions in the triplet are susceptible. The susceptibility of a particular accession can be determined by examining the triplet concerned. For instance, if accession 10 is susceptible, the forth triplet will contain a ‘‘1’’ ‘‘3’’, ‘‘5’’ or ‘‘7’’. Triplets, or parts thereof, can be added if the set is extended. When doubt exists as to the correct coding (due to an intermediate reaction), the triplet code concerned is followed by the alternative code in brackets, for example 7(3),7,3,0,0,0,0 means that the susceptibility of accession number three to this race is intermediate (‘‘4,3’’ or ‘‘4’’) and that it may show a resistant reaction under slightly different conditions.
32
M. M. LIEBENBERG AND Z. A. PRETORIUS
C. Race Characterization Most of the isolates initially characterized were collected from the Americas, but some information is also available on isolates from other continents. The Harter and Zaumeyer set of seven differentials and various other smaller sets were used to characterize races in the United States (Harter and Zaumeyer 1941; Fisher 1952), Brazil (de Menezes 1952; Dias and Da Costa 1968; Netto et al. 1969; Ferraz 1969 in Coelho and Chaves 1975; Augustin and Da Costa 1971; Coelho and Chaves 1975; Carrijo et al. 1980), Colombia (Zu´n˜iga de Rodriguez and Victoria 1975), Mexico (Crispen, in Crispen and Dongo 1962; Crispen and Dongo 1962), Peru (Guerra and Dongo 1973), Costa Rica (Christen and Echandi 1967), Puerto Rico (Ruiz et al. 1982), Jamaica (Shaik 1985b), eastern Africa (Howland and Macartney 1966), Australia (Waterhouse 1954; Ogle and Johnson 1974; Ballantyne 1978), New Zealand (Yen and Brien 1960), and Europe (Portugal, Madeira and S. Tome) (Rodrigues 1955). Several authors also reported one or two new races in their areas using these differentials (Weaver and Marcus 1949; Sappenfield 1954; Zaumeyer 1960; Groth and Shrum 1977; Hikida 1961; McMillan 1972). Races reported before the mid-1970s have been summarized by Coelho and Chaves (1975) and Ballantyne (1978). Unfortunately, most, if not all, of these races are no longer available, including Beltsville races 1 to 37. It is therefore not possible to determine their relationship with current races. Using the 1983 differential set, at least 111 races have been identified at Beltsville, prefaced here by ‘‘Bel-’’ (Stavely 1984b; Stavely et al. 1989b; Abd-Alla 1996; Stavely 1996, 1999b; Pastor-Corrales 2001; Steadman et al. 2002a). Others, using the same set, have been reported from Tanzania (Mmbaga and Stavely 1988; Liebenberg 2003), Hawaii (Balcita and Hartmann 1993), Argentina (Sandlin et al. 1995), Taiwan (J. R. Stavely, person. commun. 1999), South Africa and Malawi (Bokosi et al. 1997a; Liebenberg 2003). A large number of isolates from Nebraska and Colorado have also been characterized at the University of Nebraska, for instance, Cordoba et al. (1980b) and Miles and Steadman (1989a), the Dominican Republic (Steadman et al. 1986b; Miles and Steadman 1989b), Honduras, Puerto Rico, the Dominican Republic, the United States and Tanzania (Mmbaga et al. 1996) and Mozambique (Jochua et al. 2004). Many of these races have been preserved at the USDA in Beltsville, Maryland, or at the University of Nebraska-Lincoln. Others have been characterized in Brazil (Faleiro et al. 1999b; 2001a, in Alzate-Marin et al. 2004a,b) (availability unknown) and in Bulgaria (Kiryakov 2004).
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
33
Considerable variability in the races analyzed from year to year has been reported so that an accession may be resistant during one season but be susceptible during the next (Harter and Zaumeyer 1941; Graham 1978; Pastor-Corrales et al. 2001). This finding emphasizes the necessity of repeated isolate characterization over a number of seasons before conclusions can be made about the use of resistance genes for that area. The presence of so-called unnecessary virulence has also been noted. Alexander et al. (1985) and Groth and Roelfs (1982) indicated that the virulence found in their field collections from the central United States and Mexico could not be explained by the low level of variation in resistance genes found in local cultivars. This fact implies that virulence genes that can overcome new sources of resistance may already be present in a population before the introduction of these sources. The most virulent races have been collected from places as widely separated as South Africa, Zimbabwe, Tanzania, Egypt, Hawaii, Honduras, Florida, and Taiwan (all virulent on 13 to 16 differentials), which indicates that high levels of virulence are not limited to any single region. Two races that have an unusually broad virulence are Bel58 [coded triplet 7,3,7,4,3,3,0] (Table 1.3), from the Dominican Republic, and Bel67 [5,6,7,4,5,7,1], from Florida. Bel58 is virulent on, among others, differentials carrying Ur-3, Ur-4, Ur-5, and Ur-6, although the resistance additional to Ur-3 that is present in ‘Ecuador 299’ and ‘Mexico 235’ does give protection, while race Bel67 [5,6,7,4,5,7,1,] was the first race reported to overcome the resistance of the differential ‘Compuesto Negro Chimaltenango’ (‘CNC’) (Stavely 1988b). Three races from South Africa (RSA-Ua1, -2, and -5) overcome the resistance of at least 14 differentials, including Ur-3( þ ), Ur-4( þ ) and Ur-6 (Liebenberg 2003). Races Bel65 [5,4,5,4,4,7,0] (from Puerto Rico) and Bel67 [5,6,7,4,5,7,1] are virulent on all three of the broadly resistant differentials ‘Mexico 309’, ‘Actopan/Sanilac selection (A S) 37’, and ‘51051’. Bel108 [5,0,5,4,0,0,1], from Honduras, although not as broadly virulent, and easily controlled by Ur-3, Ur-4, and Ur-6 þ (as in ‘Olathe’), is one of the few races that overcome Ur-11 þ (as found in ‘PI 181996’). It is also virulent on the broadly resistant ‘Mexico 309’ (Ur-5) and ‘CNC’. Race TZ-Ua11 from Tanzania (Liebenberg 2003) overcomes Ur-11 (as in ‘BelMiDak-RR-8’ and ‘-9’ and ‘BelMiDak-RMR-10’ and ‘-11’), but not Ur-11 þ as in ‘PI 181996’. Ur-3 and Ur-5 both control this race. Races Bel110 [7,7,7,0,3,3,0] and Bel111 [7,7,7,0(1,2,3),3,3,0] from Zimbabwe are very similar, and both are virulent on at least 13 differentials. These, as well as Bel109 [5,6,3,0,1,0,0] from Kenya, are controlled by Ur-5, Ur-11, and the resistance in ‘51051’, ‘Mexico 235’ (Ur-3 þ ), ‘Ecuador 299’
34
M. M. LIEBENBERG AND Z. A. PRETORIUS
(Ur-3 þ ), ‘A S 37’, and ‘CNC’. Ur-3 (as in ‘Aurora’, and Ur-3 þ (as in ‘NEP 2’) do not control races Bel110 and Bel111. Acevedo et al. (2005) have reported nine additional races, collected from wild beans in Honduras, which overcome Ur-11 þ . One of these (from two different samples) overcomes both Ur-3 and Ur-11. ‘Early Gallatin’ (with Ur-4), and ‘PC-50’ (with Ur-9 and Ur-12) were resistant to this race. These authors also reported that isolates that overcome Ur-11 þ had been collected from Guatemala and the Dominican Republic. Jochua et al. (2008) reported a few races from Honduras that produce a susceptible reaction on ‘PI 181996’. It was, however, still the most resistant of the new differentials to 380 isolates from the United States, Honduras, the Dominican Republic, and South Africa. Considerable variation exists between regions and in the differentials that control the races present in rust pathogen populations. However, some differentials give far broader resistance than others. Although there appears to be a considerable number of races worldwide, certain genes and gene combinations have shown wide resistance and remain useful for the control of the majority, and in some cases, all races reported to date. The range of virulence present also differs between regions. In Brazil before 1980, ‘CSW 643’ was the most resistant differential, giving a hypersensitive or resistant reaction to most races (Netto et al. and Ferraz, both in Coelho and Chaves 1975; Coelho and Chaves 1975; Carrijo et al. 1980). Of the 39 Brazilian races inoculated on the 2002 differential set (summarized in Alzate-Marin et al. 2004b), ‘Redlands Pioneer’ was resistant to all 39, ‘CSW 643’ and ‘Brown Beauty’ to 38, ‘A S 37’ to 37, and ‘CNC’ to 34 races. Souza et al. (2007) also reported ‘Mexico 235’, ‘Mexico 309’, and ‘PI 181996’ resistant to all seven races identified in Minas Gerais, Brazil, whereas ‘CNC’ and ‘Redlands Pioneer’ were each susceptible to two races. Also using the 2002 set, Paucar et al. (2006) reported that the Middle American differentials as well as ‘Redlands Pioneer’, ‘PI 260418’, and ‘Early Gallatin’ were generally resistant to eight races identified in northern Ecuador, whereas the Andean differentials ‘Montcalm’, ‘PC-50’, and ‘Golden Gate Wax’ were highly susceptible. ‘CSW 643’ and ‘KW 765’ were resistant to all Jamaican races (Shaik 1985b). However, in the United States, these two differentials were less effective (Fisher 1952; Sappenfield 1954; Hikida 1961; Harter and Zaumeyer 1941). In Puerto Rico, ‘Ecuador 299’ and ‘Mexico 309’ were highly resistant to all races (Ruiz et al. 1982), although large pustules have since been observed on ‘Mexico 309’ (Beaver et al. 2002). In Puerto Rico, many Andean-type beans have shown durable resistance, among others the new differential ‘Montcalm’, and those carrying Ur-4. However, Ur-4 has not proven as stable in the Dominican Republic (Beaver et al. 2002).
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
35
In Hawaii, small-seeded (Middle American) differentials, namely ‘Mexico 309’, ‘A S 37’, and ‘CNC’, followed by ‘NEP 2’, ‘Ecuador 299’, and ‘Mexico 235’, were the most resistant. All other differentials were susceptible, including the small-seeded ‘51051’ (Balcita and Hartmann 1993), which is resistant in many other regions (Stavely 1984b; Mmbaga and Stavely 1988). In northern Argentina, where only four races were identified from 10 sites, Middle American differentials ‘CSW 643’, ‘Mexico 235’, and ‘Mexico 309’ were the most resistant, followed by ‘CNC’, ‘Ecuador 299’, ‘KW 765’, ‘A S 37’, ‘NEP 2’, ‘51051’, and ‘Redlands Pioneer’ (Sandlin et al. 1995). Miles and Steadman (1989a,b) analyzed isolates from Nebraska, Colorado, and the Dominican Republic and found virulence on all 19 differentials, including the usually resistant Middle American lines ‘51051’ and ‘CNC’. These two differentials, together with ‘Mexico 235’ and ‘Mexico 309’ (also of Middle American origin), were, nevertheless, the most resistant in both regions. In the high plains of the United States, the Middle American differentials ‘Ecuador 299’, ‘NEP 2’, and ‘Aurora’ (all carrying Ur-3) and ‘A S 37’ are moderately resistant. Jochua et al. (2008) reported ‘Mexico 309’, ‘Mexico 235’, ‘Aurora’, ‘CNC’, and ‘PI 181996’ resistant to all isolates collected from Nebraska and Michigan. However, accessions carrying Ur-3, which have shown good resistance in Michigan for many years, have been overcome by a new race collected in the field in 2007. ‘Mexico 235’ (with Ur-3 þ ) as well as several other differentials still show good resistance to this race (Wright, et al. 2008). Large differences in the resistance of ‘PI 260418’ were reported between Nebraska, where it was resistant to all 56 of the isolates collected, and Michigan, where it was resistant to none of 70 isolates (Jochua et al. 2008). Isolates from the Dominican Republic tended to cluster with Beltsville races from the east coast of the United State and Florida, and not with those from the central plains, possibly as a result of spore translocation northward from the Caribbean. In Ecuador, ‘Mexico 309’, ‘A S 37’, ‘Olathe’, and ‘CNC’ were resistant to all 22 isolates screened and ‘51051’, ‘NEP 2’, ‘Ecuador 299’ and ‘Mexico 235’ (all with Ur-3 þ ) as well as ‘CSW 643’, ‘KW 765’, and ‘KW 780’ were susceptible to only one isolate. The most susceptible differential was ‘Brown Beauty’ with Ur-4. (Ochoa et al. 2007). ‘PI 181996’ and ‘PI 260418’ were the most resistant of the 2002 differential set to 65 isolates from the Dominican Republic (Jochua et al. 2008). Mmbaga et al. (1996) rated ‘Mexico 235’, ‘Ecuador 299’, ‘51051’, ‘NEP 2’, and ‘Aurora’ (all carrying Ur-3), ‘Mexico 309’ (Ur-5), ‘CSW 643’, ‘A S 37’, ‘Olathe’ (Ur-6 þ ), and ‘Early Gallatin’ (Ur-4) as the most informative and resistant to a large number of isolates, mainly from the United States and Central America.
36
M. M. LIEBENBERG AND Z. A. PRETORIUS
In Europe, ‘CSW 643’, ‘Redlands Pioneer’, ‘Ecuador 299’, ‘Mexico 235’, ‘Mexico 309’, ‘A S 37’, ‘NEP 2’, ‘51051’, and ‘CNC’ (all with Middle American resistance genes) have been reported resistant (J. R. Stavely, person. commun.; Kiryakov 2004). For Africa as a whole, the most resistant differentials have been ‘CNC’ (Ur-CNC þ ), ‘A S 37’, ‘Mexico 309’ (Ur-5), as well as ‘Ecuador 299’, ‘Mexico 235’, and ‘51051’ (all with Ur-3 þ ) (Mmbaga and Stavely 1988; Abd-Alla 1996; Bokosi et al. 1997a; Stavely 1996, 1999b; Liebenberg 2003; Jochua et al. 2004, 2008). However, Mmbaga et al. (1996) reported ‘CNC’ to be susceptible to a number of isolates collected from Tanzania. In strong contrast with Puerto Rico, ‘Montcalm’ and lines carrying Ur-4 are generally very susceptible, as are those with Ur-6 and Ur-8 (Liebenberg 2003). Steadman et al. (2002b) have used a mobile nursery to evaluate virulence. The nursery, consisting of 12 seedlings of relevant resistance sources, is placed in the field for 2 to 3 hours at midday, then placed in a mist chamber for 15 hours, and then in a screenhouse for a further 8 to 10 days before being rated for rust reaction. This method is especially useful for fast evaluation of the range of virulence present in an area, or where a greenhouse and/or facilities for pure isolate research is not available, and was also recommended at the Third International Bean Rust Workshop (Steadman et al. 2002a). As many African isolates do not sporulate before 10 to 13 days after inoculation, the standard 14 to 15 days may be a more suitable rating time. 1. Stability and Reliability of Race Characterization. Some variability in the reaction of differentials to a single race has been reported, especially in the resistant reaction (Harter and Zaumeyer 1941). Variations in climatic and microclimatic conditions, such as light intensity and a temperature gradient in greenhouses between outside windows and the cooling or heat source, or between seasons and geographical locations, as well as leaf age and nutrient status of the plant, can influence pustule size, type, and number. Stavely et al. (1989b), however, found that where these factors are carefully controlled, consistent results can be obtained. When a wide range of pustule sizes occurs on the same leaf, for instance, necrotic lesions, pustules less than 0.3 mm in diameter and pustules larger than 0.8 mm in diameter, this is indicative of the presence of more than one race (Stavely et al. 1989b). Harter and Zaumeyer (1941) also noted the difficulties of keeping isolates pure and of preventing cross-contamination. This is a critical factor, particularly where large numbers of isolates from different countries are inoculated, and the data are used to compare virulence
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
37
patterns in various parts of the world. Careful field observations of the rust reactions of the differentials can help to complement greenhouse experiments. Greenhouse evaluations have been used to find races that are not noticed in field evaluations due to competition with more adapted races (J. R. Steadman, pers. commun.). D. Biochemical and Molecular Variation Studies have been undertaken to determine variation in isozyme production by U. appendiculatus. Lu and Groth (1987) grouped 14 isolates into two, and possibly three, groups. Those isolates unable to form teliospores under greenhouse conditions differed considerably from the main group and from each other. Using RAPD analysis of isolates from the Americas, Sandlin et al. (1999) classified isolates into three groups, Andean, Middle American, and a smaller, intermediate group, which mirrors the gene pools of P. vulgaris. Araya et al. (2004) observed the same pattern with 90 U. appendiculatus races from centres of bean domestication in South and Central America. Braithwaite et al. (1994) reported the presence of two divergent clusters of isolates (A and B) in Australia, a third group apparently having arisen from hybridization between the two. In a second study, Mcclean et al. (1995) reported that group B, and to a lesser extent also group A, showed affinities with the American Andean-type isolates but concluded that true Middle American–type isolates may be absent from Australia. IX. MANIPULATION OF THE FUNGUS A. Purification of Isolates Single-pustule isolates can be obtained by first inoculating a dilute suspension of rust spores onto the differential set or suitable susceptible accessions. Approximately 3 to 4 mm leaf tissue containing an isolated, developing pustule, one day from opening, is then cut from a leaf using a cork borer or sharp scissors. The leaf segment is placed, abaxial side up, in a petri dish (which can contain water agar or sterile moistened filter paper) and maintained at 18 to 24 C for two to three days until the pustule is fully open. After using a stereo microscope to ensure that only one pustule is present, spores are carefully transferred, using a number 0 to 1 artist’s paintbrush, to rust-free seedlings of a susceptible accession, followed by incubation and further increase. Leaves can be premoistened with any of the suspension inoculation media mentioned below. All apparatus must be sterilized between isolations by flaming
38
M. M. LIEBENBERG AND Z. A. PRETORIUS
or dipping in ethanol and drying. If necessary, the process can be repeated until a pure isolate is obtained (Stavely 1983, 1984b; Shaik 1985c; Liebenberg 2003). B. Inoculation Although Waterhouse (1954) inoculated fully expanded primary leaves, in more recent studies (in accordance with research findings reported in the section on leaf age), it has become standard procedure to inoculate leaves between one- and two-thirds expanded (Ogle and Johnson 1974; Groth and Scrum 1977; Ballantyne 1978; Stavely 1983; Faleiro et al. 2004; Liebenberg and Pretorius 2004a). With the exception of studies of adult plant resistance, where fourth (Mmbaga and Steadman 1990, 1992a; Mmbaga et al. 1992; Bokosi et al. 1994a) or sixth (Zaiter et al. 1990b) trifoliolate leaves were used, inoculation of primary leaves has been preferred due to the small size of plants, ease of handling, and shorter growing time required (Harter and Zaumeyer 1941; Ogle and Johnson 1974; Stavely 1983). However, although Harter and Zaumeyer (1941) obtained identical results using primary and trifoliolate leaves, Mendes and Bergamin Filho (1989) observed shorter incubation and latent periods for trifoliolate leaves in the accessions studied. Hagedorn et al. (1986) successfully inoculated detached leaves, and, although less infection was observed than with whole plants, susceptibility and resistance could be adequately distinguished. A similar tendency was observed by de Souza et al. (2005), who inoculated detached leaves by immersing them in the inoculation suspension and keeping them on moist filter paper in closed petri dishes. A urediniospore concentration of 2 104 ml1 has proven adequate for race identification (Davison and Vaughan 1964; Stavely 1984b; Faleiro et al. 2004), although 2.5 104 ml1 can be used for routine screening inoculations. This ensures sufficient infection points and enables maximal development of uredinia. Concentrations of 4 104 ml1 and higher lead to overcrowding, resulting in smaller pustules and misleading results (Davison and Vaughan 1964). A very high uredinial density also causes premature defoliation (Yarwood 1961). Screening or race identification can also be done using a fixed mass of spores, either suspended (10 mg in 10 ml 0.01% Tween) (Venette et al. 1998), or applied dry (2.5 mg per leaf) by means of a settling tower (Allen 1974; Mmbaga et al. 1994). The latter is used for the study of adult plant resistance. In all cases, spore viability should be checked by spraying or spreading them on water agar (in the same concentration as on the plants) in a small petri dish.
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
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Percentage germination in randomly selected small areas can be counted the following day under a stereo microscope. Various inoculum application methods have been used. Spraying with an apparatus creating a fine mist has been found to be very effective, the most popular being low pressure ‘‘spray guns’’ designed for artist’s or spray paint application (Stavely 1983), an atomizer (Waters 1928; Faleiro et al. 2004), or a nasal pump sprayer (Gross and Venette 2002). When multiple inoculations with different races on the same leaf are required, the sprayed area can be limited by fitting a perspex extension tube over the spray head (Stavely 1983; Venette et al. 1998). This is particularly useful when testing segregating breeding material or screening germplasm. Fromme and Wingard (1921) and Harter and Zaumeyer (1941) used an atomizer or a camel’s-hair brush, but reported that dusting the leaves with dry spores was equally, or even more, effective. Waterhouse (1954) rubbed spores gently on leaves atomized with water. Schein (1964) developed an inoculator for more accurate and reproducible inoculations using spores suspended in 0.125% water agar. Spores are generally suspended in water containing a wetting agent such as Triton B1956 (Davison and Vaughan 1963) or 0.01% polyoxyethylene sorbitan monolaurate (Tween 20) (Stavely 1983; Venette et al. 1998). However, Cordoba et al. (1980a) reported a suspended mixture of spores and talc to be more effective in the greenhouse. This method also can be used for field inoculations. Carboxymethyl-cellulose (CMC) can be added to water to prevent rapid settling of spores (Davison and Vaughan 1963a). Soltrol 170 light mineral oil also has been used as a suspending agent (Statler and McVey 1987; Linde et al. 1990; Groth and Ozmon 1994; Venette et al. 1998; Rasmussen et al. 2002), although phytotoxicity and low uredinium formation has been reported for this oil (Cordoba et al. 1980a). Augustin et al. (1972) suspended spores in Freon-113, but mentioned that prolonged contact with this dispersion medium may affect viability. A pH of 6 to 7 is the most favorable for germination (Bell and Daly 1962), and the use of tap water is recommended, due to the stimulatory effect of Ca2 þ and Mg2 þ ions on U. appendiculatus (Baker et al. 1987). C. Incubation Incubation periods used vary from 16 hours (Davison and Vaughan 1963a; Stavely 1983), 24 to 48 hours (Fromme and Wingard 1921; Harter and Zaumeyer 1941; Faleiro et al. 2004) to 40 to 48 hours (Ogle and Johnson 1974). In the generally dry South African climate, incubation periods of less than 24 hours were found to be insufficient, leading to low
40
M. M. LIEBENBERG AND Z. A. PRETORIUS
uredinium density. Incubation periods of >24 hours did not significantly increase uredinium density (M. M. Liebenberg, unpubl.). Authors are in agreement that RH during incubation should be as close to saturation as possible and temperature maintained between 16 to 22 C (Stavely 1983; Mmbaga and Steadman 1992c). Low light intensity (2 105 m einstein cm2 sec1) during incubation (18 hours) favors infection, whereas high light intensity (6 hours darkness followed by 12 hours high intensity, or 18 hours high intensity) is detrimental (Augustin et al. 1972). D. Disease Reaction Ratings are generally done 14 to 15 days after inoculation (Harter and Zaumeyer 1941; Ogle and Johnson 1974; Stavely 1983), although shorter periods have been used. A number of variables, such as soil pH and leaf age, have been reported to influence uredinium size (see Section VI.B, ‘‘Environmental Influences’’), and this, in turn, can influence ratings. Various rating scales, summarized in Table 1.4, have been used for both greenhouse and field, for example, the 1 to 6 pustule size scale (Stavely et al. 1983), the modified Cobb intensity scale (Stavely 1985) and the 1 to 9 CIAT intensity scale (Van Schoonhoven and Pastor-Corrales 1987). Mmbaga et al. (1996) developed a quantitative disease score for use with statistical analysis, based on the 1 to 6 pustule size scale. Stonehouse (1994) reported that progressions of subjective classes for rating scales were exponential and for this reason based his 1 to 9 rust scale on this model. Both log and arcsine transformations were necessary to correct skewedness. Results obtained from different assessors, especially those lacking proper training and experience, were seldom comparable, and some form of calibration was needed before data from different research groups could be compared. McMillan and Schwartz (1993) investigated the feasibility of assessing rust by means of image analysis and reported promising results for simulated bean rust (the standard grading scale), covering all aspects of disease evaluation. Shaik and Steadman (1989a) stated that the spread of disease is largely determined by the number of spores produced. Although this parameter is very difficult and tedious to measure, a good estimation of spore number (for susceptibleaccessions only)canbeobtainedbymeasuringcolonysize, which includes secondary uredinia, opposed to primary uredinium size. E. Co-inoculation Effects Zaiter et al. (1990a) reported co-inoculation effects between U. appendiculatus and both Xanthomonas axonopodis pv. phaseoli (previously X. campestris), the cause of common bacterial blight (CBB) and Bean
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
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Table 1.4. Rating scales used for the evaluation of reaction to rust (causal organism Uromyces appendiculatus) on Phaseolus vulgaris. Scale
Comments
Reference
1–3 1 = Immunity 2 = Flecking without prolific spore production 3 = Susceptibility; numerous fertile pustules present
Does not allow for resistance in the presence of small, sparsely sporulating pustules
Wingard 1933
1–3 1 = Immunity (HR) 2 = Majority of pustules < 0.3 mm (R) 3 = Majority of pustules > 0.5 mm (S)
Proposed as a simplification of the Standard International 1–6 Scale (see below)
Faleiro et al. 1999
0–4 0, 1 and 2 = Resistant 3 and 4 = Susceptible
Wei 1937
0–10 0 = No reaction 1 = Hypersensitive flecking 2 = Small pustules, some spores produced 3–9 = Sporulating pustules of increasing size (<5 = Resistant; 6–10 = Susceptible)
Modified by Groth and Shrum 1977; Groth et al. 1995
Harter et al. 1935; Harter and Zaumeyer 1941
1–5 Grade 1 = Immune (no visible infection) Grade 2 = Hypersensitive (HR) (necrotic flecking without sporulation) Grade 3 = Resistant (pustules < 0.3 mm in diameter) Grade 4 = Moderately susceptible (pustules 0.3 < 0.5 mm in diameter) Grade 5 = Susceptible (pustules > 0.5 mm in diameter)
Used in the International Bean Rust Nursery (IBRN) trials (Schwartz 1980)
Davison and Vaughan 1963
(continued)
42 Table 1.4.
M. M. LIEBENBERG AND Z. A. PRETORIUS (Continued)
Scale 1–6 Scale 1 = Immune: absence of pustules or flecks 2 = Necrotic spots without sporulation (HR) 2 = <0.3 mm 2 þ = 0.3–1 mm 2 þþ = 1–3 mm 2 þþþ = >3 mm 3 = Sporulating pustules < 0.3 mm. 4 = Sporulating pustules 0.3–0.5 mm. 5 = Sporulating pustules 0.5–0.8 mm. 6 = Sporulating pustules >0.8 mm
Comments
Reference
Standard rating scale for Stavely et al. 1983; the evaluation of rust in Van Schoonhothe greenhouse and field ven and Pastoras recognised at the First Corrales 1987, International Bean Rust Scale 2 Workshop (Stavely et al. 1993); based on both pustule size and type. Both may differ on adaxial and abaxial leaf surfaces (Harter and Zaumeyer 1941) where necessary denoted by the adaxial rating, followed by the abaxial, separated by ‘‘/’’ (Stavely 1984b)
Postscripts (mostly for greenhouse use): C (or c) = Small faint chlorotic halo C þ = Large, intensely yellow chlorotic halo N = (with appropriate number of ‘ þ ’ signs) for necrosis plus sporulating pustule size (3–6) f2 = Faint ‘‘2’’; used to indicate very small, pale necrotic spots 1–7 Intensity (Severity) Scale 1 = Absence of rust 7 = Severe disease, defoliation CIAT 1–9 Intensity (Severity) Scale
Used with the above standard scale and given in parenthesis (based on percentage leaf area covered by pustules) Widely used in African countries
Galvez 1975, in Stavely et al. 1983, based on the modified Cobb scale Van Schoonhoven and PastorCorrales 1987, Scale 1
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
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common mosaic virus (BCMV). Symptoms were more severe in the presence of both rust and CBB, and different from those caused by either pathogen separately. For less susceptible accessions, bacterial lesions were confined within the rust lesions, but for susceptible accessions, bacterial necrosis covered the whole leaf. The presence of BCMV led to a decrease in uredinium size but did not change the resistant-susceptible ranking of accessions. This information has implications for simultaneous screening with these pathogens. F. Storage Low temperatures for urediniospore storage are critical, and spores exposed to room temperature can lose viability within less than 10 days (Ogle and Johnson 1974). Schein and Rotem (1965) reported that germination after storage was inversely proportional to both storage temperature and humidity. Differences between reports of survival time at comparable temperatures can possibly be attributed to differences in prestorage dehydration and poststorage rehydration. Dehydration of spores for approximately 48 hours over a drying agent, such as anhydrous calcium sulphate, at 10 C (Groth and Ozmon 1994) is necessary to ensure longevity. Rehydration of stored urediniospores for <96 hours by flotation over distilled water or exposure to high RH was found to increase germination from 40% to >70% after storage at 60 C for 670 days (Schein 1962; Schein and Rotem 1965). Hydrated spores germinated within 6 hour (80% germination), whereas for nonhydrated spores, germination was <30% after 6 hours and 50% after 24 hours (Curtis 1966). Syamananda and Staples (1961) hydrated spores for 2 hours at 20 C by flotation and achieved 96% germination after removing the liquid by filtration and suspending the spores in 0.01% Tween 20. Short-term storage is possible between 0 and 10 C, for instance, on dried leaves for <6 months (185 days) and for 123 days in gelatine capsules at 5.5 C (Schein and Rotem 1965; Stavely 1983). Harter et al. (1935) reported that viability of urediniospores declined when stored at 9 C for 36 weeks (252 days), with no infection occurring after 38 weeks (266 days). Temperatures below freezing are preferable; Harter and Zaumeyer (1941) stored urediniospores in glass vials at 18 to 20 C for more than two years. Davison and Vaughan (1963b) obtained 16% germination and good infection after storage for >600 days at 18 C but reported minimal germination after 446 days at 3 to 4 C. Storage at ultra-low temperatures of 60 C and lower prolongs the life of spores. Schein (1962) reported urediniospores stored at 23 , 13 , and 16 C dead after 30 to 150 days, whereas 40% of those stored at 60 C
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M. M. LIEBENBERG AND Z. A. PRETORIUS
survived for 670 days. This percentage was increased to 70% after hydration for 96 hours. Infectivity of germinated spores did not appear to be affected. For long-term storage, liquid nitrogen is recommended (Loegering et al. 1961, 1966; Cunningham 1973). Teliospores were reported to be viable at least 207 days after storage at 9 C (Harter et al. 1935). Gold and Mendgen (1983a) stored teliospores at approximately 4 C (70% RH) in the dark. After a dormancy period of approximately 9 months, germination percentage increased up to a maximum of 36 to 42 months.
X. DISEASE MANAGEMENT Schwartz and Peairs (1999) stress the value of adequate technology transfer as well as the use of accurate prediction models, based on effective scouting, tracking, and prediction in integrated management of diseases such as rust. Multiple logistic regression models have been developed to quantify the probability of the sexual and asexual stages under different weather conditions on the high plains of the United States (Schwartz and Gent 2004; see also www.colostate.edu/programs/ pestalert). A. Fungicides The effectiveness of fungicides to reduce yield losses due to rust on common bean has been well studied and documented (Table 1.5). However, changes in fungicide registrations in many countries, especially the United States, occur every year. Thus, producers need to keep up to date on fungicides registered for bean rust. The recent outbreak of soybean rust in southern Africa as well as North and South America has promoted new fungicide availability for common bean and other hosts. Using a network of electronic weather stations, Schwartz et al. (1995) developed an early warning system employing information from a model based on rust levels during the previous season, volunteer bean infection, humidity and temperature, and growth stage. This system enables farmers, alerted by means of weekly communications, to employ timely (and avoid unnecessary) spraying (Schwartz et al. 1995, 1998). Gent et al. (2003) reported that organosilicone-based adjuvants improved fungicide leaf coverage by 26% to 38% above that achieved using a latex spreader-sticker. The addition of certain commercial adjuvants (which improved coverage and/or azoxystrobin absorbtion) to maneb
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
45
Table 1.5. Reports of use of fungicides for control of bean rust (caused by Uromyces appendiculatus), grouped according to active ingredient, as classified by the Fungicide Resistance Action Committee (FRAC) (http://www.frac.info/frac/ publication/anhang/FRAC_Code_List_2007_web.pdf, accessed October 2008). Active ingredient (Risk level for development of resistance)
Application timing and results
References
Protectants (contact fungicides, multisite activity fungicides) General
1–3 sprays of protectant fungicides, increased yields by 65–187%
Schwartz et al. 1995
Good control when applied ‘‘at frequent intervals’’ as a dust or spray before rust is present Leaf scorching caused by sulfur, which may have been responsible for yield depression Weekly applications of sulfur increased marketable yield of green beans in Florida (differences generally not significant) and significantly reduced the number of pustules
Zaumeyer and Thomas 1957
Inorganics (Low risk) Sulfur and lime-sulfur
Lindgren and Steadman 1982 Pohronezny et al. 1987
Chloronitrile (Low risk) Chlorothalonil
Increased yield Multiple (3–4) sprays starting a first sign of rust increased yield and seed size Weekly applications of chlorothalonil increased marketable yield of green beans in Florida and reduced number of rust pustules 3 applications increased yield by 142% and improved quality. Moderate yield increases were obtained after one or two applications
Mullins and Hilty 1975 Steadman and Lindgren 1983 Pohronezny et al. 1987
Schwartz et al. 1994a
Dithiocarbamates and related fungicides (Low risk) Maneb
Multiple (3–4) sprays starting at first sign of rust significantly increased yield and seed size 1 application significantly improved yield by 100–150% Weekly applications increased marketable yield of green beans in Florida, and reduced number of rust pustules Effective in trials in Colorado
Steadman and Lindgren 1983 Steadman et al. 1986a Pohronezny et al. 1987
Steadman 1995 (continued)
46 Table 1.5.
M. M. LIEBENBERG AND Z. A. PRETORIUS (Continued)
Active ingredient (Risk level for development of resistance)
Application timing and results
Mancozeb
Good control, more than doubled yields Monetary returns on spraying every 14 d more than double those spraying every 7 d, although 7-d treatments tended to be more effective Four applications starting at first signs of rust, increased yield by 71% Yield doubled using 2 sprays and a 3-fold increase using 4 sprays in 1985 in southern Queensland, Australia Effective in the USA but no longer registered in the USA for use on beans Significantly increased yield (<30%) when applied to a susceptible cultivar under high disease pressure in South Africa from 1995 to 1999 Metiram Good control, more than doubling yields Zinc-maneb Yields of susceptible cultivars mixture doubled under high disease pressure with 4 applications applied at 10-d intervals, starting 15 d after planting Formaldehyde-based More than 3-fold yield increase contact chemical
References Gonzalez et al. 1977 Lindgren and Steadman (1985)
Steadman et al. 1986a Ryley et al. 1990
Steadman 1995
Strauss and Killian 1996; Strauss 1997, 1999 Gonzalez et al. 1977 Simbwa-Bunnya 1972
McMillan 1994
Other multisite activity fungicides Captafol (A phthalimide) (Low risk)
Good control, more than doubling yields
Gonzalez et al. 1977
Systemic fungicides Benzimidazoles (High risk) Benomyl
Thiophanate methyl
No effect Gonzalez et al. 1977 Applied alternatively with Velez-Martinez oxycarboxin at weekly intervals, et al. 1989 starting before flowering, increased yield by 64 to 75% for susceptible cultivars in Puerto Rico, but rust infection still reached high levels on susceptible cultivars. Efficacy may have been chiefly due to oxycarboxin Most effective of fungicides tested Tanaka and Netto 1982
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
47
Table 1.5. (Continued)
Active ingredient (Risk level for development of resistance)
Application timing and results
References
Triazoles (Moderate risk) Difenoconazole
Cyproconazole
Flusilazole and flusilazole þ carbendazim
Propiconazol
Tebuconazole
Trizdimefon (triadimefon)
Applied at 14-d intervals from 6 weeks after planting, excellent control on a susceptible cultivar under high rust pressure in South Africa increased yield up to more than 4 that of control from 1995 to 1999 Applied at 14-d intervals from 6 weeks after planting, excellent control on a susceptible cultivar under high rust pressure in South Africa from 1995 to 1999, increased yield up to more than 4 that of control Applied at 14-d intervals from 6 weeks after planting, excellent control on a susceptible cultivar under high rust pressure in South Africa from 1995 to 1999, maximum yield increased up to 3 that of control Applied at 14-d intervals, insignificant yield gain, probably due to crop injury Effective when applied at 14-d intervals the next season Reduced infection efficiency comparable to non–race-specific resistance and a 3-fold yield increase in Colorado in 1888 Effective when applied at the first sign of disease in trials in Colorado Applied at 14-d intervals from 6 weeks after planting, excellent control on susceptible cultivar under high rust pressure in South Africa from 1995 to 1999, increased yield up to 3 than of control Applied at 7-d intervals, insignificant yield gain, probably due to crop injury Significantly improved yield by 100-150% applied at 14-d intervals
Strauss and Killian 1996; Strauss 1997, 1999
Strauss and Killian 1996; Strauss 1997, 1999
Strauss and Killian 1996; Strauss 1997, 1999
Mullins and Hilty 1985
Mullins and Hilty 1986 Hill et al. 1990
Steadman 1995
Strauss and Killian 1996; Strauss 1997, 1999
Mullins and Hilty 1985
Steadman et al. 1986a (continued)
48 Table 1.5.
M. M. LIEBENBERG AND Z. A. PRETORIUS (Continued)
Active ingredient (Risk level for development of resistance) Bitertanol
Hexaconazole
Application timing and results Effective Significantly improved yield by 100–150% applied at 7- and 14-d intervals Weekly applications, started after rust was observed, increased marketable yield of green beans and controlled number of rust pustules in Florida More than 100% yield increase with 4 applications in Mauritius, best of 7 fungicides tested Good results in Cuba, applied at 14-d intervals Yield increased up to 3 that of control, when applied to a susceptible cultivar under high rust pressure in South Africa from 1995 to 1999 (applied at 14-d intervals) starting 6 weeks after planting Good results in Cuba, applied at 14-d intervals
References Mullins and Hilty 1986 Steadman et al. 1986a
Pohronezny et al. 1987
Saumtally and Autrey 1990 Steadman 1995 Strauss and Killian 1996; Strauss 1997, 1999
Steadman 1995
Carboxamides (Moderate risk) Oxycarboxin
Good control, more than doubled yields Applied alternatively with benomyl at weekly intervals, starting before flowering, increase yield 64–75% for susceptible cultivars in Puerto Rico in 1985, rust infection still reached high levels on susceptible cultivars Significantly increased yield in southern Queensland, Australia but only when rust pressure was not high (in 1986) Significant yield improvement (up to 5 fold) in Ethiopia on a susceptible cultivar Good results in Cuba, applied at 14-d intervals Applied at 14-d intervals from 6 weeks after planting, increased yield up to 86% on susceptible cultivar under high rust pressure in South Africa from 1995 to 1999
Gonzalez et al. 1977 Velez-Martinez et al. 1989
Ryley et al. 1990
Habtu 1994
Steadman 1995 Strauss and Killian 1996; Strauss 1997, 1999
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
49
Table 1.5. (Continued)
Active ingredient (Risk level for development of resistance)
Application timing and results
References
QoI-fungicides (Quinone outside Inhibitors) (High risk) Azoxystrobin
Available leaf area increased <48.5% with 1 application of fungicide during artificially induced epidemics
Mersha and Hau (2008)
Effective protection, effect on yield was not measured
Rajam et al. 1986
Other a-Difluoromethylornithine (DFMO) (No risk level given)
lowered rust incidence up to 62%. However, the effect on yield was not significant. Use of these compounds can enable lower application volumes, reduced rates, and/or longer intervals between treatments. The use of food additives as an alternative control measure for U. appendiculatus was investigated by Arslan et al. (2006). Potassium acetate, potassium benzoate, sodium acetate, and sodium citrate significantly reduced disease incidence on potted seedlings, without injury to bean leaves. Disadvantages of fungicides and other chemicals include the increase in production costs, fairly widespread lack of application technology, expertise, and correct timing of application, as well as lack of availability, particularly in Africa. These problems render fungicides generally unpractical for use by subsistence farmers. Potential phytotoxicity due to using incorrect rates and possible detrimental effects of the chemicals on the environment are further negative factors that make nonessential use unadvisable. The potential use of fungicides is curtailed in some parts of the world by delay in or lack of registration (Steadman 1995), bans on certain chemicals (e.g., mancozeb in the United States; Stavely and Steadman 1992), prohibition of fungicide application within a certain period before harvesting to meet residue limits, the presence of chemical residues (Pohronezny et al. 1987) (particularly applicable to green beans), and limitations on use when beans are followed by nonregistered rotation crops (Stavely and Steadman 1992). The development of fungicide resistance may limit the long-term usefulness of some fungicides, and overuse, especially prevalent in some snap bean production areas, is a threat to their stabiblity. Risk levels for the various classes are indicated in Table 1.5.
50
M. M. LIEBENBERG AND Z. A. PRETORIUS
B. Resistance Breeding The incorporation of multiple resistance genes into locally adapted cultivars remains the most cost effective control measure for rust (Coyne and Schuster 1975; Stavely and Kelly 1996; Liebenberg et al. 2005). However, many cultivars are susceptible, and the disease remains a problem where the environment is favorable. Most United States varieties are susceptible, as are most in Latin America (J. R. Steadman, person. commun.). In some cases, cultivars lose their resistance when new races appear. 1. Race-Specific Resistance Conferred by Major Genes. There are numerous reports on the inheritance of rust resistance, and it is generally accepted that resistance to rust is controlled by one or more major, dominant genes (Zaumeyer and Harter 1941; Ballantyne 1978; De Carvalho et al. 1978; Meiners 1981; Kolmer and Groth 1982; Kardin and Groth 1985; Stavely 1986; Webster and Ainsworth 1988; Stavely and Pastor-Corrales 1989; Bokosi et al. 1994a; Sayler et al. 1995; Steadman 1995; Gonzalez-Gracia and Grafton 1996; Stavely and Kelly 1996; Alzate-Marin et al. 2004a; Mutunga et al. 2002; Liebenberg and Pretorius 2004a; Pastor-Corrales 2005). However, recessive genes have been reported (Finke et al. 1986; Zaiter et al. 1989; Sayler et al. 1995), including a (mutant of Crg) (Complements resistance gene). Crg is necessary for the expression of rust resistance gene Ur-3 (Kalavacharia et al. 2000). Available Rust Resistance (Ur) Genes. Various named and some as-yetunnamed rust resistance genes are known, and many have been used in resistance breeding (Kelly et al. 1996; Pastor-Corrales et al. 2001; Hosfield et al. 2003; Brick et al. 2005; Liebenberg et al. 2005) (Table 1.6). Ur-3 and Ur-11 (the latter previously known as Ur-32) were thought to be alleles (Kelly et al. 1996) but have since been reported to be linked in repulsion (Stavely 1998). Recombination of these genes was achieved, and they are now linked in coupling in the breeding lines ‘BelDakMiRMR-14’ to ‘-23’ and in ‘BelMiNeb-RMR-6’ to ‘-13’ (Stavely 1998; Stavely et al. 1998; 1999a,b; Pastor-Corrales 2003). The effectiveness of single major genes for the long-term management of plant diseases is questionable; however, single resistance genes have been effective for some diseases for a number of years in some parts of the world (van der Plank 1968). For P. vulgaris, the resistance gene Ur-3 has, for example, given sufficient control in North Dakota and Minnesota since at least 1977 (Groth and Shrum 1977; Stavely et al. 1999a; Gross and Venette 2002), in spite of the fact that many races virulent on Ur-3 have been collected in North America (Stavely 1999a).
51
Ur-E Single dominant. Allele or closely linked to Ur-2 Ur-M Tightly (probably ¼ linked Ur-I) gene complex or single dominant gene
As above, with various (different) additions
Ur-22
Ur-3 þ
Ur-3
Single dominant
Ur-2
Ur-B
Ur-A
Single dominant
Ur-1
Synonym
Type
MA
MA
MA
MA
MA
Probable gene pooly
‘Kodiak’ ‘Merlot’ ‘Grand Mesa’ ‘Teebus-RR 1’
‘BelJersey-RR-1’
Mexico 235 (medium ‘‘0’’ < ‘‘6,5’’; most frequent: ‘‘2’’ pink), also, with or ‘‘2,3’’ different additional genes in NEP 2 (small white), Ecuador 299 (medium pink), and 51051 (small black)
–
–
‘‘2’’–‘‘3’’; probably < ‘‘6’’ with other races
‘‘2’’–‘‘3’’; with Beltsville races < ‘‘5,6’’; most frequent: ‘‘2,3’’
–
Example of use
‘‘4’’ < ‘‘5’’; probably < ‘‘6’’ with other races
Range of infection types obtainedx
‘‘f2’’ < ‘‘6,5’’, wide variation
Gallaroy Genotype A and B (no longer traceable due to loss of isolates) Gallaroy Genotype B (no longer traceable due to loss of isolates) Actopan/Sanilac Selection (A S) 37) (no longer traceable due to loss of isolates) Aurora
Source
(continued)
Ballantyne 1978; Kardin and Groth 1985; Stavely 1986; Stavely et al. 1989; Kelly et al. 1996, Anon 2002; Hosfield et al. 2003; Brick et al. 2005; Liebenberg et al. 2005 Stavely 1984; Stavely and Grafton 1985; Stavely 1986; Kelly et al. 1996; Stavely et al. 1989
Ballantyne 1978
Ballantyne 1978
Ballantyne 1978
References
Numbered rust resistance and related genes in Phaseolus vulgaris, and some additional as yet unnamed resistance genes
Genez
Table 1.6.
52
Series of single dominant genes tightly linked in coupling (‘‘gene block’’)
Single dominant
Ur-5
Ur-6
Ura, Ur-G
‘‘B-190’’
– Gene necessary for the expression of Ur-3 Single Ur-C?, Up2 dominant
Crg-
Ur-4
Type
Genez
Synonym
(Continued)
Table 1.6.
Sierra
Source –
Range of infection types obtainedx
A/MA (gene probably of Andean origin)
Golden Gate Wax (A/MA) (LBr), Olathe (MA) (Pinto)
‘‘0’’ or ‘‘f2’’ < ‘‘6,5’’; most frequent: ‘‘4,5’’ or ‘‘5,6’’
Early Gallatin A/MA gene (medium white) appears to be Ur-4 is also of Andean reported to be in origin as the ‘Brown Beauty’ marker is in and ‘KW 780’, all Andean the latter with material additional tested (Miklas resistance et al. 1993; Liebenberg 2003) ‘‘0’’ < ‘‘5,6’’; most Mexico 309 MA/A (gene frequent: ‘‘2,3’’ (MA/A) (small block black) (via ‘B-190) probably of MA origin)
MA? (Kalavacharla et al. 2000)
Probable gene pooly
Ballantyne 1978 (Ur-C) in Brown Beauty; Christ and Groth 1982b; Kolmer and Groth 1982; Stavely 1986, Kelly et al. 1993, 1996; Stavely and Kelly 1996; Stavely et al. 1994
‘BelMiDak-RR 2’ to ‘-12’
Ech avez et al. 1982; ‘B–190’, ‘BelNebStavely 1982, 1984a; RR-1’, Freytag et al. 1985; ‘L226-10’ and Stavely et al. 1989a; ‘L227-1’, ‘TeebusKelly et al. 1996; RCR 2’ Miklas et al. 1998; Alzate-Marin et al. 2004a; Anon. 2005; Liebenberg et al. 2005; de Souza et al. 2006, 2007 ‘BelDakMi–RMRGrafton et al. 1985; 14’ –to ‘–18’ Stavely and Kelly 1996; Kelly et al. 1996; Stavely et al. 1998, 1999a
Kalavacharla et al. 2000
References
–
Example of use
53
RB11
Up1
Urp
Single dominant
Ur-7
Single Ur-US#3 dominant (tentatively Ur-8)
Ur-9
URPRI, Single Ur-Resisto, tentatively dominant also Ur-10 (slow referred to rusting) as Ur-10 Ur-32 Ur-11 Series of tightly linked dominant genes (gene block)
Single dominant
Ura þ Urc
Ur-6 þ
MA (Stavely 1990d, 1998)
PI 181996 (small black), PI 190078 (small black)
‘BelNeb-RR-1’
‘BelDakMi RR-1,’ ‘BelDak-RR-2’, ‘BelNeb-RR-1’
0.49–0.7; selected for ‘‘small pustule resistance’’ (not widely tested) ‘BelMiDak RR-8’ to Generally < ‘‘3’’, ‘-12’, ‘BelDakMialthough several RMR-14’, races do overcome ‘Sederberg’ it, for example Bel108 and Ua-TZ11, see also Acevedo et al. (2005)
‘‘4,3’’ < ‘‘6’’, probably wider, not tested with most races
‘‘0’’ or ‘‘f2’’ < ‘‘6,5’’, Olathe (MA) wide variation Sandlin and Steadman 1994) (Pinto) (reported to contain at least three closely linked RR genes (Stavely 1984a) GN 1140 (Great ‘‘2 þ ,3,4’’ < ‘‘6,5’’, not Northern) tested with most races US#3 (large white) ‘‘0’’–‘‘6,’’5’’; most frequent: ‘‘6,5’’
PC 50 (‘Pompadour A (Finke et al. Checa’) (red 1986; Kelly mottled) et al. 1996; Sandlin and Steadman 1994) A (Webster Resisto, Cape (green beans) and Ainsworth 1988)
MA/A
MA
A (in MA background) (Kelly et al 1996)
Stavely 1990d, 1998; Stavely et al. 1994a,b; Kelly et al. 1996; Stavely and Kelly 1996; Stavely et al. 1998; Alzate-Marin et al. 2004a,b; Anon. 2005; Liebenberg et al. 2006b (continued)
Webster and Ainsworth 1988; Kelly et al. 1996
Augustin et al. 1972; Stavely et al. 1989a; Kelly et al. 1996 Christ and Groth 1982b; Kolmer and Groth 1982; Grafton et al. 1985; Kelly et al. 1996 Finke et al. 1986; Kelly et al. 1996; Jung et al. 1998; Park et al. 1999; Saladin et al. 2000
Grafton et al. 1985; Stavely 1984a; Stavely and Grafton 1989; Stavely et al. 1989a,b; 1994b; Kelly et al. 1996
54 ‘‘0’’–‘‘6’’; most Kranskop (RSS) frequent ‘‘3’’–‘‘5’’ via Redlands Greenleaf C. May originate from ‘CSW 643’ (which may have been heterozygous for Ur-Red (Ballantyne 1978) PI 151385 (Capio de Enredadera) (large tan with brown markings) ‘PI 151395’ (Guecito) (small white)
MA (Liebenberg 2003; Liebenberg and Pretorius 2004a)
A? (Stavely 1988b)
MA? (Stavely 1988b)
Single dominant?
Single dominant?
‘‘PI 151385’’ (may be Ur-11)
‘‘PI 151395’’ (may be Ur-11)
Ur-13
PC-50
A
– Single dominant gene for adult plant resistance, expressed at the 4th trifoliate stage Single Possibly Ur-Red dominant (Ballantyne 1978)
For adult plant resistance, pustule on adult leaves smaller than on primary leaves, not widely tested
Resistant to Race Ua-TZ11
Ur-12
PI 181996 (small black), PI 190078 (small black)
MA (Stavely 1990d, 1998)
Range of infection types obtainedx
As above but superior to Ur-11
Source
Ur-11 þ
Probable gene pooly
Type
Genez
Synonym
(Continued)
Table 1.6.
Jung et al. 1998
Liebenberg. 2003; Liebenberg and Pretorius 2005; Liebenberg et al. 2005
References
‘BelFla-RR-1’ to ‘-3’
‘BelFla-RR-4’
Stavely and McMillan 1991
Stavely and McMillan 1991
Many South African Liebenberg 2003, Liebenberg and RSS cultivars, Pretorius 2004a,b; some ‘Redlands’ Liebenberg et al. cultivars 2006a,b
Resistance additional to Ur-11 is generally not transferred
Example of use
55
Single dominant
Single dominant
Ur-Dorado108
Ur-Dorado53
MA (Miklas et al. 2000)
MA (Miklas et al. 2000)
MA (Corr^ea et al. 2000)
MA (Jung et al. 1996)
Dorado (DOR 364) resistant to races Bel-53 þ 54
Dorado (DOR 364) (resistant to race Bel 108)
Ouro Negro (small black) derived from the line ‘Honduras-35’
BAC-6
Compuesto Negro Chimaltenango (‘CNC’) KW 814
MA
MA
PI 260418 (large black and brown speckled on white)
A (PastorCorrales 2002)
2,3–5, not widely tested
1–5, not widely tested
‘‘0’’ < ‘‘6,5’’; wide variation Small pustules obtained with race D85C-1, not widely tested Not widely tested
‘‘0’’ < ‘‘5,6,4’’; most frequent: ‘‘2,3’’
Complements Ur-11, giving resistance to race Bel 108
Widely used in Central Brazil
‘BelDak-RR-2’
Miklas et al. 2000, 2002
Corr^ ea et al. 2000; Faleiro et al. 2001; Miklas 2002; Alzate-Marin et al. 2002; 2004a; de Souza et al. 2007 Miklas et al. 2000, 2002
Jung et al. 1996
Stavely and Grafton 1989; Stavely 1994b; Rasmussen et al. 2002 Kolmer and Groth 1982
Stavely 1989b; PastorCorrales 2002, 2005
Gene symbols as proposed by Kelly et al. 1996. The reader is also referred to the BIC Web site list of genes: www.css.msu.edu/bic/PDF/Bean% 20Genes%20List%202008.pdf. y Andean (A), Middle American (MA). Unless otherwise indicated, gene pool origin is based on analysis of the seed storage protein phaseolin (Brown et al. 1982; Gepts et al. 1986;Sandlin and Steadman 1994), on allozyme analysis (nine loci) (Singh et al. 1991), as reported in Sandlin et al. 1999 or according to pedigree (Ogle and Johnson 1974; Ballantyne 1978; or McClean and Myers 1990). x See 1 to 6 scale, Table 1.4.
z
–
–
–
Major dominant
Ur-OuroNegro
Ur-BAC 6
Ur-814
Ur-CNC
Single dominant, possibly two other unlinked More than one, dominant Single dominant Single No allele tests dominant reported
‘‘PI 260418’’
56
M. M. LIEBENBERG AND Z. A. PRETORIUS
Gene stacking (or pyramiding) has been proposed as a more durable solution (Coyne and Schuster 1975; Stavely 1988a; Singh 1999). Many accessions, in particular the more resistant differentials, are known to contain at least two Ur genes. Stavely and Grafton (1985) reported that the resistance in the differential ‘Mexico 235’ is due to at least two, and possibly three, dominant genes or tightly linked series of genes. Kardin and Groth (1985) found indications that the old differential ‘Aurora’ contains at least two independent major dominant rust resistance genes, and Grafton et al. (1985) reported the presence of two genes in ‘Aurora’, one of which (Urc) appeared similar to a gene found in ‘Olathe’. ‘PC-50’ has a gene (Ur-9) expressed in the primary leaf stage and one (Ur-12) expressed at a later stage (Bokosi et al. 1996; Jung et al. 1998). The differential ‘CNC’ is resistant to many races (Stavely and Meiners 1981; Stavely 1988b, 1993, 1994; Stavely et al. 1994b, 1997; PastorCorrales 2001, 2002; Liebenberg 2003) and probably contains two or more resistance genes, one of which has been studied by Rasmussen et al. (2002). Some genes constitute a complex locus of tightly linked genes that is usually inherited as a unit (described as a gene block), such as Ur-5 (Stavely 1982) and Ur-11 (Stavely 1990d). Two, three, and as many as four resistance genes have been combined in various Beltsville lines; for example, Ur-3, Ur-4, Ur-6, and Ur-11 are stacked in ‘BelDakMi-RMR-18’ to ‘-23’. In addition, many of these releases combine rust resistance with resistance to the viral diseases BCM and BCMN, imparted by the I-gene, bc-12, and/or bc-3 (Stavely et al. 1998, 1999a; Pastor-Corrales 2003). Rust-resistant lines released in the United States between 1988 and 2003 are summarized in PastorCorrales (2003). Ur-3 and Ur-6 (together with the I-gene and bc-12 for resistance to BCMV and BCMNV) have also been stacked in the pinto cultivar ‘Kodiak’, released in the United States (Kelly et al., 1999). Ur-11 and Ur-13, together with the I-gene and resistance to ALS have been combined in the South African cultivar ‘Sederberg’ (Anon 2006). The BIOAGRO laboratory in Vic ¸osa, Brazil, is also using marker-assisted selection (MAS) to stack rust and other resistance genes. The rapidly increasing number of functional molecular markers linked to rust resistance genes will undoubtedly facilitate gene stacking. Certain gene combinations, such as resistance gene(s) from ‘CNC’ (UrCNC þ ) and ‘Mexico 235’ (Ur-3 þ ) [or ‘Olathe’ (Ur-6 þ )], or from ‘Mexico 235’ (Ur-3 þ ) and ‘Early Gallatin’ (Ur-4) [or ‘Olathe’ (Ur-6 þ )], have been particularly successful in the achievement of broad resistance in the United States (Stavely et al. 1992). Pastor-Corrales (2001) points out that the combined resistances from ‘CNC’ and ‘Ecuador 299’ gives control of all 94 races then available in Beltsville, with the exception of race 85.
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
57
This race is controlled by differentials carrying Ur-4, Ur-6, and Ur-11, and by ‘NEP 2’, ‘KW 814’, and ‘US#3’. Furthermore, the combination of Ur-3 or Ur-4 with Ur-11 gives protection to all rust races then available in Beltsville (Pastor-Corrales 2002). Other Sources of Race-Specific Resistance. The broadest resistance to Beltsville races is found in Plant Introduction (PI) numbers ‘151385’ (large tan with brown markings), ‘151388’ (medium light tan with dark ringlike markings, from Colombia), ‘151395’ (small white), ‘151396’, ‘181996’ (small black, from Guatemala), ‘190078’ (small black), ‘260418’ (large black and brown mottled on white), ‘310962’, and an additional 29 PIs. Only ‘PI 260418’ and ‘PI 310962’ gave resistance to all 87 races known by 1997, whereas the remaining 35 PIs were susceptible only to race Bel108 (Stavely 1989b, 1990b,c, 1995, 1997; Stavely et al. 1994b, 1997). ‘PI 260418’ has since been reported susceptible to race Bel84 from Colorado (Pastor-Corrales 2005, 2008). It is moderately susceptible to the South African races RSA-Ua6, -9 and -10 and moderately susceptible in the field in South Africa (Liebenberg 2003). Jochua et al. (2008) reported ‘PI 260418’ resistant to the majority of isolates collected in Michigan, Yuscaran (Honduras), and the Dominican Republic but susceptible to more than 60% of those collected from Nebraska, Tatumbla (Honduras), and South Africa. ‘PI 260418’ has been reported to have between one and three rust resistance genes (Pastor-Corrales 2005). CIAT accession ‘G 2333’, a Mexican landrace possessing three resistance genes for anthracnose (Young et al. 1998), was reported resistant to all rust isolates tested in Ecuador (Ochoa et al. 2007), and resistance to all Brazilian rust races tested was found in ‘Ouro Negro’ (Corr^ ea et al. 2000; Faleiro et al. 2001). The latter also contains the Co-10 gene for anthracnose resistance (Alzate-Marin et al. 2001a; Ragagnin et al. 2003). Accessions that have been reported to be very resistant to rust in Africa are ‘BelNeb-RR-1’ (Ur-5, Ur-6 and Ur-7), ‘PI 181996’ (Ur-11 þ ) and the CIAT carioca line ‘A 286’, which has been released in South Africa as ‘Mkuzi’, and in Malawi as ‘Kambidzi’ (resistance genes unknown) (Liebenberg et al. 2005). These two cultivars are particularly popular for subsistence farming due to their multiple disease resistance and high yield. However, ‘Mkuzi’ has not been accepted in commercial markets in South Africa. Differentials containing the resistance genes Ur-3, Ur-5 and Ur-11 were resistant to 69 isolates collected in Mozambique (Jochua et al., 2004). The differentials ‘Mexico 309’ (Ur-5), ‘A S 37’, ‘51051’ and ‘CNC’, as well as the CIAT lines ‘G 5698’ and ‘Mexico 54’ were also reported to show useful rust resistance (Liebenberg 1998).
58
M. M. LIEBENBERG AND Z. A. PRETORIUS
2. Race-Nonspecific Resistance. The confusion over and variety of terminology in connection with various types of resistance has been discussed by Nelson (1978) and Zadoks (2002). Terms that have been used to describe ‘‘horizontal’’ resistance sensu van der Plank, include polygenic, race-nonspecific, generalized, durable, rate-reducing, partial, small pustule, adult plant, minor gene, residual, additive, and field as well as slow rusting, tolerance, and (conferred by) Quantitative Trait Loci (QTL) (van der Plank 1968, 1969, 1982; Watson 1970; Nelson 1978; Skovmand et al. 1978; Parlevliet 1979; Webster and Ainsworth 1988; Zadoks 2002). The dilemma is further increased when a particular case of race-nonspecific resistance is found to be nondurable, when a particular race-specific (vertical) resistance gene proves to be durable, and when a type of resistance thought to be race-nonspecific is found to be racespecific, as was, for instance, reported by Lee and Shaner (1982) for slow rusting in wheat. In any discussion of resistance, the important role played by genotypeenvironment interaction in the manifestation of rust symptoms must be taken into account (Browder 1985). It is also becoming increasingly clear that the nature of host-pathogen interactions in relation to durable resistance are particularly diverse (Johnson 1984). As van der Plank (1968, 1982), Parlevliet (1976), and Nelson (1978) have pointed out, the distinction between vertical and horizontal resistance is not clear, and in many cases the two may be associated. For this reason, many of the above terms cannot be categorized. Van der Plank (1982) further draws attention to the fact that much so-called polygenic resistance is, in fact oligogenic, and concludes that ‘‘polygenic inheritance would be a burden on the plant breeder,’’ most of whom prefer to strive for ‘‘additive variance in a system of oligogenic inheritance’’ (p. 138). Adult plant resistance (APR) has been reported for bean rust and was thought to be race-nonspecific and related to leaf pubescence (Shaik 1985a; Steadman and Shaik 1988; Shaik and Steadman 1988, 1989b; Zaiter et al. 1990b; Mmbaga and Steadman 1990, 1992a,b,c; Mmbaga et al. 1994; Sevillano et al. 1997). However, APR was later found not to be associated with pubescence (the gene for pubescence and that for APR were located on different chromosomes), and not to be racenonspecific (Bokosi et al. 1994a; Sandlin and Steadman 1994; Jung et al. 1996, 1998). This finding is in agreement with various findings for APR in cereals, summarized in van der Plank (1982). APR in beans is fully expressed above the third trifoliolate stage and was reported to be controlled by a different gene from that controlling specific resistance on the primary leaves (Bokosi et al. 1994a,b; Jung et al. 1998). Accessions reported to show APR in the field and/or to multiple isolates include
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
59
‘Pompadour Checa 83–30’, ‘Alubia 33–1’ (and other ‘Alubia’ selections), ‘Jose Beta’, ‘Diacol Calima’, ‘Kabanima’, and ‘Jamaica Red’ (Mmbaga and Steadman 1990, 1992a; Zaiter et al. 1990b), ‘Nasaka’ (a Malawian landrace selection) (Bokosi et al. 1994b, 1997b), ‘PC 50’ (Sandlin and Steadman 1994), ‘BAT 93’, ‘BAT 308’ and ‘EMP 81’ (Beebe and PastorCorrales1991) as well as ‘INIAP-414’ (Ochoa et al. 2007). The CIAT line ‘CAL 143’ (registered in Malawi as ‘Napilira’) is rust tolerant in the field in South Africa and exhibits APR (in the form of reduced pustule size) to at least one race in the greenhouse (M. M. Liebenberg, unpubl.). It has also been reported resistant in Ecuador (Murillo I et al. 2006). Partial or rate-reducing resistance, defined as any combination of reduced infection efficiency, lengthened latent period, reduced sporulation capacity, shorter infectious period, and reduced pustule size (Watson 1970; Parlevliet 1979; Niks and Rubiales 2002), is widely recommended to combat disease. Parlevliet (1975), for instance, reported large differences in latent period for wheat rust on wheat, especially at flag leaf stage. Various other aspects of rate-reducing resistance, including slow rusting, reduced sporulation, and early telia formation, have been investigated for possible use in bean breeding (Ballantyne 1978; Schwartz and Temple 1978), but very little has been reported on the success of such strategies. Meiners et al. (1975a,b) reported that slow rusting was common among green (snap) beans,and that dry bean accessions ‘Swedish Brown’ and ‘US#5 Pinto’ were slow rusting. Ballantyne (1978) observed slow rusting, which appeared to be relatively simply inherited, in cultivars ‘Apollo’ and ‘California White Kidney’. Statler and McVey (1987) studied differences in latent period, infection density, early and late fungal colony abortion, uredinial size, and uredinia per square centimeter on primary leaves of resistant and susceptible P. vulgaris accessions. Significant differences were obtained for all parameters except latent period. Aust et al. (1984), using a field collection of rust from Brazil, determined that the lines ‘Carioca’/‘C-224’ and ‘Roxo’/‘C-743’ produced approximately one-third less spores than the susceptible ‘Rosinha-G-2’/‘C-21’. Edington et al. (1994a,b) found partial resistance to be highly heritable and additive and developed 45 promising large-seeded bean lines. Habtu (1994) reported significant differences between accessions for five components, of which the most important were latent period, infection efficiency, and pustule size. Small pustule size is generally thought to be an indication of a more stable, polygenic, non–race-specific resistance (Parlevliet 1994; Niks and Rubiales 2002). In a study of six accessions exhibiting large pustules and four exhibiting small pustules, Pastor-Corrales and Correa (1983)
60
M. M. LIEBENBERG AND Z. A. PRETORIUS
found pustule size to be more important than rust severity in determining yield differences. Aust et al. (1984) also found that accessions exhibiting small pustules produced two-thirds the number of spores of a susceptible accession. Although this type of resistance is undoubtedly important, many races that overcome genes, or gene blocks (such as Ur-5, Ur-11 and the resistance gene[s] in ‘CNC’) (all of which condition a small pustule reaction to many races) have been characterized (Stavely 1989b, 1990d; Stavely et al. 1997; Sandlin et al. 1999). Thus, this type of resistance, which is monogenetically (or relatively simply) controlled, is not necessarily stable in P. vulgaris (Stavely 1984a). Webster and Ainsworth (1988) reported that cultivars ‘Resisto’ and ‘Cape’ possessed ‘‘small pustule resistance,’’ conditioned by a single dominant gene (common to both cultivars). Jung et al. (1996) studied ‘‘small pustule resistance’’ in ‘BAC 6’ and obtained a resistant:susceptible 1:1 segregation (indicative of dominance) for the recombinant inbred line (RIL) in the F7 generation. In addition, Shaik and Steadman (1989a) cautioned that leaf development stages at the time of inoculation can cause considerable variation in uredinial size and recommended that a range of developmental stages should be included when this parameter is studied. They also concluded that secondary uredinial size may be a more reliable measure of adult plant resistance. Allen et al. (1991) mention that the uniform response of races from diverse geographical locations to signal height for appressorium formation creates the possibility of breeding for stomatal lip heights that do not induce appressorium formation: a truly race-nonspecific form of resistance. However, no variations in lip height was found when numerous bean lines were measured. Johnson (1981, 1984, 1992) defines durable resistance as ‘‘resistance that remains effective during its prolonged and widespread use in an environment favorable to the disease,’’ adding that it does not provide any explanation of the genetics, resistance mechanism, or the nature of its specificity. He also concludes that the diversity of host-pathogen interactions defies explanation by a single model. When the goal is durable resistance, the distinction between vertical and horizontal resistance is immaterial. It is, however, difficult to design a strategy for the achievement of durable resistance, in that the outcome can be measured only in retrospect. Durable resistance is also not necessarily permanent. Widespread and prolonged testing prior to release of a cultivar may also considerably reduce its durability in the hands of the farmer. Johnson (1981) points out that durable resistance in cultivars possessing vertical resistance may be due at least partly to the presence of
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
61
additional genes and that ‘‘it is difficult to be sure that the entire resistance genotype of a cultivar has been described.’’ Neither the nature of inheritance nor the various forms of resistance influence their importance in integrated disease management, neither do they exclude the use of any resistance, including vertical, from useful deployment. The use of all resistance components is recommended, even where differences are relatively small (Van der Plank 1968; Coyne and Schuster 1975; Zadoks 2002). Effective control should include all integrated disease management strategies (Watson 1970; Zadoks 2002) that could prolong the efficacy of vertical genes (Person et al. 1976). Complete control of disease under all circumstances is difficult to attain and probably unnecessary, but factors restricting the amount of inoculum present often can limit severe damage to exceptional seasons with favorable disease conditions. 3. Marker-Assisted Breeding. Phenotypic markers have been used extensively in the mapping of genes of P. vulgaris (Bassett 1988, 1991); for example, the ‘XAN 159’ source of CBB resistance is known to be linked to purple flower color and black seed coat (Jung et al. 1997). However, to date, the only phenotypic traits available for rust resistance are host reactions to characterized rust races (discussed under ‘‘Pathogenic Variation’’). Ballantyne (1978) studied the possible relationship between rust resistance and growth habit, seed coat color, and stem pigment color for various crosses but found no evidence of linkage with resistance. Jung et al. (1996, 1998) also found no linkage between abaxial leaf pubescence and rust resistance. Biochemical markers such as isozymes and proteins have been useful in tracing the origins of bean cultivars (Gepts et al. 1986), but for gene mapping (Gepts 1999; Gepts et al. 1993), cultivar fingerprinting (Stockton et al. 1992; C.M.S. Mienie, person. commun. 2003; Faleiro et al. 2004) and resistance breeding (Miklas 2002; Ragagnin et al. 2003; Faleiro et al. 2004), recent attention has been given to polymorphic-rich markers using nucleic acids (usually DNA). Initial studies used restriction fragment length polymorphisms (RFLPs) (Nodari et al. 1992), but, due to the time consumed by this method, the large amount of DNA required, and the dangers of radioactivity, it quickly gave way to polymerase chain reaction (PCR)based markers such as RAPD markers (Williams et al. 1990; Miklas and Kelly 1992; McClean et al. 1994; Johnson et al. 1995; Jung et al. 1996, 1998; Faleiro et al. 2004; Park et al. 2004b), amplified fragment length polymorphisms (AFLPs) (Vos et al. 1995; Beebe et al. 1998; Rasmussen et al. 2002; Liebenberg 2003), derived sequence characterized amplified
62
M. M. LIEBENBERG AND Z. A. PRETORIUS
region (SCAR) markers (Park et al. 2004b,c, 2008; Mienie et al. 2005), microsatellites (simple sequence repeats [SSRs]) (Yu et al. 2000; Blair et al. 2003; Pastor-Corrales et al. 2008), and targeted region amplified polymorphism (TRAP) markers (Wright et al. 2008). There are several genetic maps on which many of the rust resistance genes have been mapped; for instance, Gepts et al. (1993); Nodari et al. (1993); McClean et al. (1994) (Ur-6); Jung et al. (1996) (Ur-BAC6); Freyre et al. 1998 (Bean Core Map); Jung et al. (1998) (Ur-9 and Ur-12); Miklas et al. (1998) (Ur-5); Miklas et al. (2000) (Ur-Dorado-53, Ur-Dorado-108, Ur-5 marker); Miklas et al. (2002) (Ur-3, Ur-4, Ur-5, Ur-9, Ur-11, Ur-12, Ur-Dorado-53, Ur-Dorado-108, Ur-Ouro-Negro, Ur-BAC 6); Faleiro et al. (2003) (Ur-Ouro-Negro), Mienie et al. (2005) (Ur-13); and Pastor-Corrales et al. (2008) (Ur-PI260). The Bean Core (‘BAT 93’/‘Jalo EEP 558’) map has been expanded to accommodate most of these, and other, genes (Miklas et al. 2006). Chromosome numbers, allocated in 2003 by Pedrosa et al. (2003), have been changed to correspond with those used for the Core Map linkage groups by Freyre et al. (1998), Pedrosa-Harand et al. (2006), and Pedrosa et al. (2008). Conflicting chromosome numbers may, therefore, occur between publications of before and after 2006. From the Comprehensive Map (Miklas et al. 2006; www.css.msu.edu/ bic/PDF/Bean%20Core%20map%202007.pdf), it is apparent that the rust resistance genes of Middle American origin tend to cluster into two main groups and are also associated with anthracnose resistance genes of Middle American origin. On chromosome 4, the Ur-5, Ur-Dorado-108, and Ur-Ouro-Negro resistance genes, and the Co-3, Co-9, Co-y, and Co-z genes for anthracnose resistance cluster together. This group also contains QTL for bean golden mosaic virus (BGMV), halo blight, anthracnose, and ashy stem blight. On chromosome 11, Ur-11, Ur-3, and Ur-Dorado-53, the Co-2 gene for anthracnose resistance, as well as QTL for common bacterial blight and anthracnose, cluster together. Chromosome 11 also contains Ur-BAC 6 and Ur-6 (Miklas et al. 2002; Kelly et al. 2003). The tight clustering of Ur-11 and Ur-3 confirms the observation of Stavely (1998) that these genes were linked in repulsion. The Andean gene Ur-9, however, is associated with the Co-I, Co-x, and Co-w genes for anthracnose resistance on chromosome 1 (Kelly et al. 2003). Other as-yet unmapped genes may be associated with existing clusters, and more clusters on other chromosomes may become apparent as more genes are mapped. PCR-based techniques are becoming increasingly popular, but their full potential remains to be realized. For breeding purposes, where gene stacking is involved, reliability is important, especially for the inclusion
1. COMMON BEAN RUST: PATHOLOGY AND CONTROL
63
or retention of hypostatic genes as a protective measure for epistatic genes in breeding material. These markers are useful when informative races (by means of which their presence can be detected) are not available, where pathogen inoculations are impractical or containment for foreign races is not available, when screening for multiple disease resistance (to avoid repeated inoculations, frequent handling, risk of damage and stress), or where interaction between diseases occurs. The use of PCR-based markers has been restricted chiefly by lack of reliability over different genetic backgrounds and between labs, or low linkage (summarized in Miklas 2002). For instance, the RAPD (repulsion) marker OAE19890 (Johnson et al. 1995) is present in at least six lines with Ur-11 and absent from less than six lines without Ur-11. However, this marker has been used with success by de Oliveira et al. (2002), using ‘BelMiDak-RR-3’ as the donor of Ur-11. The SCAR marker, developed from the above, sAE19890 (de Queiroz et al. 2004), has also been successfully used for MAS in Brazil. This marker has been reported to be in several accessions containing Ur-3 (‘NEP 2’, ‘51051’, ‘Aurora’, and ‘Helderberg’), as well as in several ‘‘Bel’’ lines containing the Ur-3 þ Ur-11 genes in coupling phase linkage (‘BelDakMi-RMR-14’,’-16’, ‘-18’, ‘-21’, and ‘-23’ and ‘BelMiNeb-RMR-7’, to ‘-10’, ‘-12’, and ‘-13’) (Liebenberg et al. 2008). This marker may be useful for MAS of Ur-3 þ Ur-11 in coupling, provided that other flanking markers can be identified. The RAPD marker OAC20490 for Ur-11 (Johnson et al. 1995) is present in ‘PI 181996’ as well as in those lines for which ‘PI 181996’ was the source of Ur-11, but a similar band occurs in many Middle American lines that do not contain Ur-11. It was absent from most of the Andean accessions tested, indicating that it may be more useful in this background (Johnson et al. 1995). However, Liebenberg (2003) reported inconsistent results in the application of this marker. The RAPD marker OA141100 for Ur-4 (Miklas et al. 1993) also has limitations. It was present in all Andean material tested by the above authors and is therefore suitable only for use in a Middle American background. This marker has been used in tracing Ur-4 in the presence of Ur-11 in the ‘BelMiDak-RR’ lines (Kelly et al. 1993; Stavely et al. 1994a) and for confirming homozygosity in the ‘BelMiNeb RMR-6’ and ‘-7’ lines (Stavely et al. 1999). OA141100, or the codominant SCAR marker Ur-4-SA1079/800 (Mienie et al. 2004) developed from it, may be useful for the transference of Ur-4 from ‘KW 780’ (where this marker appears to be linked in repulsion with Ur-4) into large-seeded materials that contain the marker but lack Ur-4 (Liebenberg et al. 2004b). Markers were also used to confirm the presence of Ur-3 and the I-gene in ‘BelDakMi-RMR-14’ (Stavely et al. 1998) and ‘BelDakMi-RMR-15’ to ‘-18’
64
M. M. LIEBENBERG AND Z. A. PRETORIUS
(Stavely et al. 1999a), and facilitated selection for resistance to BCMV, BCMNV (I and bc-3 genes), and BGMV (bgm-I gene) for various other rust resistant ‘‘Bel’’ lines developed in the United States (Stavely et al. 1997). MAS is also being used with success to detect the rust resistance of ‘Ouro Negro’ in lines with multiple disease resistance and to facilitate the recovery of resistant progeny closest to the background of the recurrent parent (Corr^ ea et al. 2000; Faleiro et al. 2004; Ragagnin et al. 2003). AlzateMarin et al. (2001) used existing RAPD markers for Ur-3, Ur-7, Ur-9, and Ur-Ouro-Negro (¼ Ur-Honduras-35, to screen breeding material from Minas Gerais, Brazil. Liebenberg et al. (2006b) used SCAR markers to trace Ur-13 in the presence of the epistatic Ur-11 and to trace Ur-5 in breeding lines. The SQ4 marker, linked to the Co-2 gene (conferring anthracnose resistance) on chromosome 11, appears to be linked to the Ur-11 gene (Awale et al. 2008; Liebenberg et al. 2009), and it is possible that markers for other diseases may be used to supplement rust gene markers, particularly within resistance gene clusters, such as those on chromosomes 11, 1, and 4. Currently only marker O131350, linked at 34.6 cM, is available for APR (Ur-12 in ‘PC 50’), but a more tightly linked marker is needed for effective use (Jung et al. 1998). Important molecular markers for known rust resistance genes have been summarized in Table 1.7. Sequences of available SCAR markers can be obtained from www.css.msu.edu/bic/PDF/SCAR%20Markers% 202007.pdf. It is important that all markers be validated for use with local breeding material and in the laboratories concerned, before widescale application is attempted. C. Biological Control and Induced (Acquired) Resistance Very little work has been undertaken in the field of biological control and induced (acquired) resistance. The bacteria Bacillus subtilis (Baker et al. 1983, 1985) and fungus Verticillium lecanii (Allen 1982) have been identified as biological control agents for U. appendiculatus. Wittmann and Sch€ onbeck (1995) observed a reduction of pathological sink activity and a corresponding increase in the sink activity of the youngest leaf after application of the inducer ‘‘B 50’’, a filtrate of a Bacillus subtilis strain. Yuen et al. (2001) evaluated >100 strains of bacteria against rust under greenhouse conditions and reported that the application of cultures of one strain each of Pantoea agglomerans and Stenotrophomonas maltophilia led to reduced rust severity comparable to that of a contact fungicide, and concluded that there was potential for the biological control of rust.
65
MA
MA
A
MA
Gene
Ur-3
Crg-
Ur-4
Ur-5 RAPD OI19460 SCAR SI19
B-190 (BBL47 6// Green Giant 447/B-190 & Slenderette 5/ 3/Eagle//Green Giant 447/B-190) Coupling
Coupling
RAPD OA141100 SCAR OA14
Early Gallatin C 20/Early Gallatin
Coupling
Phase
Coupling
SCAR SK14620
Genetic marker
RAPD
Sierra
Kodiak (originally from NEP 2) near isogenic lines 90T-4042R and 90T-4042S
Accession/ Cross used for identification
No recombinants
No recombinants
?
Not complete agreement with inoculations
Linkage distance (cM)
Genetic markersz available for rust resistance genes in Phaseolus vulgaris.
Probable gene pooly
Table 1.7.
False positives for some accessions
Only MA gene pool
–
Limited application
Limitations
4
(continued)
Haley et al. 1993; Melotto and Kelly 1998; Miklas et al. 1998, 2002
Nemchinova and Stavely 1999; Haley et al. 1994 (RAPD OK14620), Miklas et al. 2002; Kelly et al. 2003 8 Kalavacharla et al. 2000; Miklas et al. 2002 6 (previously Miklas et al. B4) 1993; Miklas 2002; Kelly et al. 2003; Mienie et al. 2004
11
Chromosome numberx References
66
A
A
A
MA
MA
MA
Gene
Ur-6
Ur-6
Ur-6
Ur-7
Ur-7
Ur-7
(Continued)
Probable gene pooly
Table 1.7.
GN 1140(Great Northern) GN 1140/GN Nebr.#1
GN 1140 (Great Northern) GN 1140/GN Nebr.#1
Olathe Olathe/ GN Nebr. #1 sel.27 GN 1140 (Great Northern)/ GN 1140/GN Nebr.#1
Olathe Olathe/ GN Nebr. #1 sel.27
Olathe Sierra/ Olathe
Accession/ Cross used for identification
7.7
Repulsion
RAPD OAI121000
OAD12550 SCA SOAD12537 OAF17900 RAPD OAB16850 OAD9550
Coupling
Coupling
2.4
2.2
No recombinants
1.3 2.0
Coupling
RAPD OBC06300 ( þ SCAR) and RAPD OAG15300 (flanking) RAPD OAY15200
Coupling
10.4
Coupling
RAPD OV12950
RAPD OAA11500
Linkage distance (cM)
Phase
Genetic marker
–
–
SOAD12.537 is in several lines with Ur-6, e.g., ‘BelDak-RR1’ & ‘-2’ and ‘CO12783’
–
–
–
Limitations
11
Park et al. 2003
Park et al. 2003
Park et al. 2003, 2008
11
11
Park et al. 2004b
McClean et al. 1994; Kelly et al. 1996 Park et al. 2004a,b,c
11
11
11
Chromosome numberx References
67
MA
A
A
MA
MA
MA
A
Ur-7
Ur-9
Ur-9
Ur-11
Ur-11
Ur-11
Ur-12
PC-50 PC-50/XAN 159)
BelMiNebRR-1 & -3 Susceptible GN/BelMiNeb RR-1)
PI 181996 NX-040 4/ PI 181996
GN 1140 (Great Northern) GN 1140/GN Nebr.#1 Pompadour Checa (PC-50) (Calima) PC-50/XAN 159) PC-50 PC-50/ Chichara PI 181996/PI 181996
Repulsion
Coupling
Coupling
RAPD OAE19890 SCAR: sAE19890
RAPD GT02450
RAPD O131350
Coupling
Coupling
Coupling
RAPD J131100
RAPD A041050 RAPD OAC20490
Repulsion
RAPD OAB18650
34.6
Not complete agreement with inoculations
Not in ‘PI 181996’ (source)
Limited application may be useful as a coupling marker for Ur-(3 þ 11)
Limited application
63
1.0 (de Oliveira et al. 2002)
–
–
–
8.6
5.0
7.6–8.2
7
11
11
11
1
1
11
(continued)
Jung et al. 1998
Park et al. 1999 Johnson et al. 1995; Kelly et al. 2003 Johnson et al. 1995; de Oliveira et al. 2002; Kelly et al. 2003 de Queiroz et al. 2004 Liebenberg et al. 2008 Boone et al. 1999
Jung et al. 1998
Park et al. 2003
68
MA
MA (Jung et al. 1996) MA
Ur-13
‘‘CNC’’
Ur-BAC 6
Ur-OuroNegro
MA
Gene
(Continued)
Probable gene pooly
Table 1.7.
Ouro Negro Pinto 111/ Ouro Negro)
CNC CNC/ Othello BAC-6
Kranskop Bonus(SA)/ Kranskop)
Accession/ Cross used for identification
AFLP/SCAR in progress Flanking RAPD AJ16250 H191050 RAPD OX11630, RAPD OF101,050/ SCAR SF10, Flanking markers
SCARs SEAACCMAC C430/405 SEACAMCTT310/288 SEAAGMCGT430 HhaI220/186
Genetic marker
Coupling Coupling
Coupling
Coupling
12.5 14.6 5.8 7.7
–
Linkage distance (cM)
Co-dominant 1.6 9.3 16.1
Phase
Not widely tested
Not widely tested
–
–
Limitations
4
11
–
8
Ragagnin et al. 1998 in Corr^ ea et al. 2000; Faleiro et al. 2000; Miklas et al. 2002; Ragagnin et al. 2003; Kelly et al. 2003
Liebenberg 2003; Liebenberg and Pretorius 2004a,b, Mienie et al. 2005; Liebenberg et al. 2006a Rasmussen et al. 2002 Jung et al. 1996
Chromosome numberx References
69
MA
MA
A
Ur-Dorado108
Ur-Dorado53
UrPI260418
Dorado (DOR 364) (resistant to race Bel 108) Dorado (DOR 364) (resistant to race Bel-53) PI 260418 (large black and brown speckled on white)
Ouro Negro Pinto 111/ Ouro Negro Coupling
Coupling
Coupling
Coupling
Flanking SCARs: OPF101.072 (A8) OPBA8530 (BA8)
RAPD
RAPD
SSR
20
9.6 from Co-2 marker locus
11.3 from Ur-5 marker locus
6.0 4.3
1
11
4
–
–
4
Not widely tested
Pastor-Corrales et al. 2008
Miklas et al. 2000, 2002
Corr^ ea et al. 2000; Faleiro et al. 2001; Miklas 2002; Alzate-Marin et al. 2004a Miklas et al. 2000, 2002
z The reader is also referred to Miklas et al. (2006) and the list of SCAR markers at: www.css.msu.edu/bic/PDF/SCAR%20Markers%202008. pdf. y Andean (A), Middle American (MA). x Chromosome numbers, equivalent to the ‘‘B’’ linkage group numbers used for the ‘Bat 93’/’Jalo EEP 558’ Core Map, are according to PedrosaHarand et al. (2008).
MA
U-OuroNegro
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Siegrist et al. (1997) observed systemic acquired resistance to rust 4 days after sprayed application of benzo[1,2,3] thiadiazole-7-carbothioic acid-S-methyl ester (BTH). This was confirmed by Iriti and Faoro (2003), who obtained complete control after a single dose of BTH applied 7 days before inoculation. They attributed the resistance to cell wall strengthening induced by enhanced acid perioxidase activity resulting from increased hydrogen peroxide (H2O2) levels in the plant. Tyihak et al. (1989) reported that the amino acid derivative Ne-trimethyl-L-lysine induced resistance to rust in the cultivar ‘Saxa’. The 6- to 8-day interval between inducer treatment and inoculation with rust was critical. Unfortunately, with this type of response, field application of inducers (where a continual supply of inoculum is present) is not practical. Ebrahim-Nesbat et al. (1982) infiltrated bean leaves with a glucans-rich elicitor, obtained from germinated urediniospores. The resulting accumulation of phytoalexins prevented haustorium formation. Allen (1975) and Johnson and Allen (1975) succeeded in inducing resistance to rust by means of pre-inoculation with either maize rust or a weakly virulent race of U. appendiculatus. Researchers at CIAT also succeeded in inducing resistance to one rust race by pre-inoculation with another race, avirulent on that accession. Although the protection was not translocated to uninoculated leaves, significant differences were obtained in field trials between unprotected and protected plots (CIAT 1987). Induced resistance may have future applications, particularly for intercropping and the use of multilines, but does not yet appear to have found a practical application. Assante et al. (2004) reported effective parasitism of urediniospores of U. appendiculatus by the mycoparasite Cladosporium tenuissimum but stressed the importance of environmental factors. Complete control of the disease was obtained by means of applications of C. tenuissimum culture filtrates but not by conidial suspensions. According to Nasini et al. (2004), secondary metabolites produced by this hyperparasitic fungus (cladosporols 1 to 5) are responsible for the inhibition of urediniospore germination. D. Cultural Practices 1. Cultivar Mixtures and Multilines. The use of seed mixtures and multilines, which incorporate an array of race-specific resistance, has been proposed as a rust control strategy. This method possibly discourages the development of new races and lowers the amount of inoculum present (Browning and Frey 1969; Coyne and Schuster 1975; Smithson and Lenn e 1996; Pink 2002). Mixtures of bean cultivars
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or landraces are commonly planted by small-scale farmers in Africa. Such mixtures can contain from two to 30 components, with three usually comprising 50 to 90% of the whole (Mohamed and Teri 1989; Mbewe and Mulila 1990; Trutmann et al. 1993; Smithson and Lenn e 1996). Mixtures have been reported to have a suppressive effect on disease incidence (Van Rheenen et al. 1981) and to be employed by farmers in a disease management program, even where very little knowledge of the causes of disease exists (Mohamed and Teri 1989; Trutmann et al. 1993). Habtu (1994) reported that radial expansion of the disease from inoculation points was only 3 cm per day in a mixture containing 20% susceptible plants, as compared to a 16 cm per day in plots containing susceptible plants only. Panse et al. (1997) obtained slight increases in yield using various mixture combinations. Other authors, however, reported an inconsistent effect of mixtures on rust as compared to monoculture (Van Rheenen et al. 1981; Aylor 1988), although the general tendency does appear to be a lessening of the amount of disease. The advantages of the use of multilines have been summarized in Browning and Frey (1969) and Coyne and Schuster (1975). The additional inputs required for seed maintenance of both multilines and mixtures, together with the strict requirements for uniformity in commercial markets, limits the widescale use of both methods in commercial systems (Smithson and Lenn e 1996; Steadman et al. 2002a). Nevertheless, where small-scale farmers are concerned, there may be opportunities for the expansion of this strategy. Smithson and Lenn e (1996) suggest carefully controlled selection of mixture components similar to that proposed for multilines, combined with evaluation of farmer mixtures and possible improvements by backcrossing resistance into a common background. 2. Intercropping and Multiple Cropping. Intercropping of beans with nonhost crops, such as maize, is popular in many parts of Africa (Simbwa-Bunnya 1972; Van Rheenen et al. 1981; Mbewe and Mulila 1990; Fininsa and Yuen 2001) as well as in Latin America (Woolley and Davis 1991). In some circumstances, maize in particular may decrease rust levels, possibly due to the provision of a physical barrier influencing factors such as spore dispersal and temperature (Msuku and Edje 1982; Sengooba 1990; Boudreau and Mundt 1992; Fininsa 1996). However, ambiguous results have also been obtained (Van Rheenen et al. 1981; Boudreau and Mundt 1992) and in some studies, such as reported by Diaz (1981), an increase in rust incidence was observed for beans in association with maize. These differences may be due to variation
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in topography, wind patterns, and other local factors influencing microclimate and spore dispersal. In a study using computer-simulated epidemics where many variables could be manipulated, multilines and intercropping were demonstrated to decrease the amount of disease (Mundt and Leonard 1986). 3. Sanitation. Reduction of the number of volunteer bean plants, including those within rotation crops or weed canopies, thorough harvesting of bean seed, weeding, and the use of herbicides is recommended to remove potential hosts for the establishment of the sexual stages of the pathogen in temperate climates and to prevent early buildup of inoculum. Tillage practices are also important to avoid potential hosts for the sexual stage, and include deep plowing to incorporate bean debris into the soil. Bean plants that germinated through bean debris were reported to have a higher incidence of aecial infection than those that germinated through a clean surface, indicating that minimum tillage practices encourage the development of the sexual stage in bean rust. Effective weed control and wider spacing can also minimize the formation of a dense canopy, which creates a humid microclimate conducive to rust (McMillan and Schwartz 1994; McDonald and Linde 2002; McMillan et al. 2003). 4. Crop Rotation. Rotation of two or more years between bean crops is widely recommended, especially in areas where the sexual stage is known to occur (McMillan et al. 2003). To be effective, this crop rotation must be combined with good sanitation practices, which have the additional advantage of also reducing bacterial and other fungal diseases. 5. Planting Time. Conducive conditions during the most vulnerable stages of the host can be avoided by judicious selection of planting date (Steadman 1995). This method is widely practiced by small-scale farmers in Africa (Mohamed and Teri 1989). 6. Overhead Irrigation. McMillan (1994) obtained a significant decrease in rust severity accompanied by a fourfold yield increase by applying overhead irrigation four times per week. This created the effect of intermittent heavy rain, which presumably washed the spores off the leaves and into the soil, thus preventing spore dissemination by wind (Chupp and Sherf 1960). However, this practice may promote other diseases and may not be practical for bean crops.
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XI. CONCLUSIONS It appears that there is adequate knowledge of the basic climatic conditions conducive to the development and sporulation of U. appendiculatus, and techniques for its inoculation and maintenance have been established. There are also many available sources of vertical resistance within P. vulgaris, some of them as yet poorly characterized and utilized, although new sources, particularly within the Andean gene pool, will be useful, especially where a wide range of virulence occurs. There is, however, a need for effective sources of true oligogenic, race-nonspecific forms of resistance. Although the phenomenon of horizontal or field resistance has received attention, the need for the understanding and application of this resistance type in breeding is challenging. The psychological effect of diseased beans on farmers undoubtedly has an influence on their choice of planting material, but the final determining factors must be yield and quality, and field resistance is perhaps best measured in these terms. We would benefit from an understanding of the mechanisms responsible for stable yield in cultivars in spite of significant amounts of rust. Perhaps researchers should study ‘‘durable yield’’ instead of ‘‘durable resistance’’. In Africa, where population growth often exceeds food production, and soils are rapidly becoming depleted of nutrients, reliable yield under natural conditions, without the intervention of fungicides, is of paramount importance. The techniques used to study the mechanisms of durable resistance are often difficult to use, and new methods that enable quick and easy screening are needed. Less than two decades ago, the use of molecular markers for disease resistance breeding was uncommon, not only for bean rust but also for other diseases and other crops. Since then, and especially during the past few years, striking and almost exponential progress has taken place. This technique is a very useful tool in the hands of a competent breeder and will certainly become more important in the future. However, there is a danger that marker-assisted selection may become marker selection, with fieldwork taking second place. Once again, the real measure of success is yield and quality under field conditions. Marker and greenhouse screening do not provide an easy way out, and they must remain a tool and not the aim of any breeding program. As molecular techniques become standardized, screening of large quantities of material is now possible in the larger laboratories, especially those associated with private breeding companies. This enables breeders to retain large numbers of marker-carrying plants, which they must then screen and select in conventional field trials. Screening with the most suitable pathogens
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also cannot be eliminated. Before MAS can be applied, markers need to be tested in local genetic backgrounds and matched with the reaction to suitable local races in the greenhouse. Periodic greenhouse screening must also complement MAS. For this reason, race characterization must continue, albeit directed at important races that can distinguish the genes being utilized and races that overcome sources of resistance. With this in mind, a serious attempt should be made to characterize more races from Africa, where beans are extremely important. Characterization of races from other important bean-producing countries, such as China, is also needed. Results from the New World, although valuable to the international community for identification of promising sources of resistance, are not sufficient. There is also ample evidence that African races can exhibit a high degree of virulence and that some may be unique to Africa. These races may, in turn, be of value to breeding programs on other continents. However, care should be taken that race characterization does not become a purely academic exercise. In South Africa, some progress has been made in broadening the genetic base of rust resistance (Liebenberg et al. 2005), which in the past was limited by reliance on closely related, well-adapted resistance sources. Probably due to the strong preference for large-seeded beans in the past, Andean-specific races are more prevalent, and small-seeded beans provide the most effective sources of resistance. However, the increasing popularity of small-seeded beans in the continent (due to their superior disease resistance and yielding ability) as well as the increasing reliance on beans as a source of protein may, with time, lead to increasing prevalence of races that overcome Middle American resistance sources. This has been the case for ALS. Previously, races of P. griseola attacking small-seeded beans were practically unknown, but in recent years, Middle American–type races (distinguishable from the general Andean type on a molecular level and according to host reaction) have been increasingly observed on small-seeded beans in several African countries, such as Malawi, South Africa, and Kenya (Boshoff et al. 1996; Liebenberg 1998; Wagara et al. 2004). It is, therefore, becoming increasingly important to include resistance genes from both gene pools, as has been a priority in the United States, where races from both gene pools are prevalent. The development of a set of near-isogenic lines (NILs) as differentials, each carrying a single resistance gene, is needed. This will facilitate race characterization and mapping as well as effective resistance breeding. The increasing demand for organically grown food may be an added incentive for resistance breeding, integrated with cultural practices that lower inoculum and disease levels.
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ACKNOWLEDGMENTS The authors thank the librarians of the University of the Free State, Bloemfontein, the North West Province Department of Agriculture, Conservation and Environmental, and of the ARC-Small Grain Institute, Bethlehem, for literature, and in particular Mrs. M. Harman and Mrs J. Kilian. Our sincere thanks to Dr. J. R. Steadman of the University of Nebraska, Lincoln, for reviewing the manuscript and for many valuable suggestions; to Dr. J. R. Stavely, previously of the USDA, Beltsville, for copies of scarce articles; and to anonymous reviewers. LITERATURE CITED Abd-Alla, H.M. 1996. Studies on rust disease of common bean. PhD Thesis, Univ. Minia, El Minia, Egypt. Acevedo, M., J.R. Steadman, J.C. Rosas, and J. Venegas. 2005. Annu. Rep. Bean Improv. Coop. 48:132–133. Aime, M.C. 2006. Systematics and molecular variability of bean rusts. Annu. Rep. Bean Improv. Coop. 49:45–46. Alexander, H.M., J.V. Groth, and A.P. Roelfs. 1985. Virulence changes in Uromyces appendiculatus after five asexual generations on a partially resistant cultivar of Phaseolus vulgaris. Phytopathology 75:449–453. Allen, D.J. 1974. A technique for measuring sporulation of rust (Uromyces appendiculatus) on Phaseolus vulgaris. Annu. Rep. Bean Improv. Coop. 17:16–17. Allen, D.J. 1975. Induced resistance to bean rust and its possible epidemiological significance. Annu. Rep. Bean Improv. Coop. 18:15–16. Allen, D.J. 1982. Verticillium lecanii on the bean rust fungus Uromyces appendiculatus. Trans. Br. Mycol. Soc. 79:362–364. Allen, D.J. 1995. An annotated list of diseases, pathogens and associated fungi of the common bean (Phaseolus vulgaris) in eastern and southern Africa. Phytopathological Papers 34, CAB Intl, Wallingford, UK. Allen, D.J., M. Dessert, P. Trutmann, and J. Voss. 1989. Common beans in Africa and their constraints. pp. 9–31. In: H.F. Schwartz and M.A. Pastor-Corrales (eds.), Bean production problems in the tropics. CIAT, Cali, Colombia. Allen, E.A., H.C. Hoch, J.R. Stavely, and J.R. Steadman. 1991. Uniformity among races of Uromyces appendiculatus in response to topographic signaling for appressorium formation. Phytopathology 81:883–887. Alleyne, A.T., J.R. Steadman, and K.M. Eskridge. 2008. Monitoring changing virulence patterns of Uromyces appendiculatus in the resistant pinto bean cultivar Olathe by repPCR. Eur. J. Plant Pathol. DOI 10.1007/s10658-008-9295-0. Alzate-Marin, A.L., M.R. Costa, E.G. de Barros, and M.A. Moreira. 2001a. Characterization of the anthracnose resistance locus present in cultivar Ouro Negro (Honduras 35). Annu. Rep. Bean Improv. Coop. 44:115–116. Alzate-Marin, A.L., M.R. Costa, A. Sartorato, E.G. de Barros, and M.A. Moreira. 2001b. Use of previously identified RAPD markers as a tool to verify presence of resistance gene in common bean. Annu. Rep. Bean Improv. Coop. 44:123–124.
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Skovmand, B., R.D. Wilcoxson, B.L. Shearer, and R.E. Stucker. 1978. Inheritance of slow rusting to stem rust of wheat. Euphytica 27:95–107. Skroch, P.W., J.B. dos Santos, and J. Nienhuis. 1992. Genetic relationships among Phaseolus vulgaris genotypes based on RAPD markers data. Annu. Rep. Bean Improv. Coop. 35:23–24. Smithson, J.B., and J.M. Lenne. 1996. Varietal mixture: a viable strategy for sustainable productivity in subsistence agriculture. Ann. Appl. Biol. 128:127–158. Souza, T.L.P.O., V.A. Ragagnin, D.A. Sanglard, M.A. Moreira, and E.G. Barros. 2007. Identification of races of selected isolates of Uromyces appendiculatus from Minas Gerais (Brazil) based on the new international classification system. Fitpatol. Bras. 32 (2). DOI: 10.1590/SO100-41582007000200002. Sprecher, S.L., and T.G. Isleib. 1989. Morphological and phenological diversity between bean gene pools. Annu. Rep. Bean Improv. Coop. 32:54–55. Statler, G.D., and M.A. McVey. 1987. Partial resistance to Uromyces appendiculatus in dry edible beans. Phytopathology 77:1101–1103. Stavely, J.R. 1982. Genetics of resistance to Uromyces phaseoli in Phaseolus vulgaris breeding line B-190. Phytopathology 72:1004. (Abstr.) Stavely, J.R. 1983. A rapid technique for inoculation of Phaseolus vulgaris with multiple pathotypes of Uromyces phaseoli. Phytopathology 73:676–679. Stavely, J.R. 1984a. Genetics of resistance to Uromyces phaseoli in a Phaseolus vulgaris line resistant to most races of the pathogen. Phytopathology 74:339–344. Stavely, J.R. 1984b. Pathogenic specialization in Uromyces phaseoli in the United States and rust resistance in beans. Plant Dis. 68:95–99. Stavely, J.R. 1984c. Pathogenic specialization in Uromyces phaseoli and rust resistance in bean germ plasm. Annu. Rep. Bean Improv. Coop. 27:14–15. Stavely, J.R. 1985. The modified Cobb scale for estimating bean rust intensity. Annu. Rep. Bean Improv. Coop. 28:31–32. Stavely, J.R. 1986. Pathogenic variability, resistance sources, and progress towards developing stable resistance to bean rust. Annu. Rep. Bean Improv. Coop. 29:24–25. Stavely, J.R. 1988a. Rust resistance in beans: The plant introduction collection as a resource and resistance development. Annu. Rep. Bean Improv. Coop. 31:64–65. Stavely, J.R. 1988b. Occurrence of rust resistance in Phaseolus plant introductions 0658 through 194331. Annu. Rep. Bean Improv. Coop. 31:128–129. Stavely, J.R. 1989a. Bean rust in the United States in 1988. Annu. Rep. Bean Improv. Coop. 32:121–122. Stavely, J.R. 1989b. Occurrence of rust resistance in Phaseolus vulgaris Plant Introductions 194333 through 289438. Annu. Rep. Bean Improv. Coop. 32:123–124. Stavely, J.R. 1990a. Recent progress towards obtaining rust resistant beans. Annu. Rep. Bean Improv. Coop. 33:63–64. Stavely, J.R. 1990b. Bean rust in the United States in 1989. Annu. Rep. Bean Improv. Coop. 33:183–184. Stavely, J.R. 1990c. Bean rust resistance of additional plant introductions. Annu. Rep. Bean Improv. Coop. 33:185–186. Stavely, J.R. 1990d. Genetics of rust resistance in Phaseolus vulgaris plant introduction 181996. Phytopathology 80:1056. (Abstr.) Stavely, J.R. 1993. Bean rust in the United States in 1992. Annu. Rep. Bean Improv. Coop. 36:162–163. Stavely, J.R. 1994. Bean rust in the United States in 1993. Annu. Rep. Bean Improv. Coop. 37:241–242.
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2 Bitter Gourd: Botany, Horticulture, Breeding Tusar K. Behera, Snigdha Behera, and L. K. Bharathi Indian Agricultural Research Institute New Delhi, 110012, India K. Joseph John National Bureau of Plant Genetic Resources KAU (P.O.) Thrissur 680656 Kerala, India Philipp W. Simon Vegetable Crops Research Unit ARS-USDA Department of Horticulture University of Wisconsin Madison, WI 53706 Jack E. Staub Forage and Range Research Laboratory ARS-USDA Logan, UT 84322 I. INTRODUCTION A. Origin and Domestication B. Nutritional Uses C. Medicinal Properties 1. Hypoglycemic Activity 2. Antioxidant Activity 3. Antifertility Effects 4. Antiviral Activity 5. Antimicrobial Activity
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II. BOTANY A. Taxonomy and Morphology B. Reproductive Biology III. HORTICULTURE A. Climate and Soil B. Culture C. Sex Expression and Modification D. Harvest E. Seed Production F. Insects and Diseases 1. Fruit Fly (Dacus cucurbitae) 2. Red Pumpkin Beetle (Aulacophora foveicollis) 3. Aphids (Aphis gossypii) 4. Fusarium Wilt 5. Anthracnose 6. Powdery Mildew 7. Downy Mildew 8. Virus IV. BREEDING A. Genetic Variation and Germplasm Development B. Inheritance 1. Seed and Fruit Characters 2. Sex Expression 3. Bitterness 4. Yield C. Character Association D. Goals and Cultivar Development E. Methods 1. Heterosis 2. Mutation Breeding 3. Testing F. Biotechnology V. CONCLUSIONS LITERATURE CITED
I. INTRODUCTION The vegetable Momordica charantia L., Cucurbitaceae, is known variously as bitter gourd, balsam pear, bitter melon, bitter cucumber, and African cucumber (Heiser 1979). Although it has many culinary uses, especially in south, southeast and east Asia, it is also grown as an ornamental and is used extensively in folk medicine (Heiser 1979). The fruits are cooked with other vegetables, stuffed, stir-fried, or added in small quantities to beans and soups to provide a slightly bitter flavor. However, for most food preparation, fruits are blanched, parboiled, or soaked in salt water before cooking to reduce the bitter taste. In addition to frying or cooking (e.g., for curries), the fruits can be dehydrated,
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OH
CH2 O
O OH OH Fig. 2.1.
O
OH
Basic structure of Momordicine, the primary bitter compound of bitter gourd.
pickled, or canned. Fruits, flowers, and young shoots are also used as flavoring agents in various Asian dishes. Young Momordica shoots and leaves are also cooked and eaten as leafy vegetables, and leaf and fruit extracts are used in the preparation of tea (Tindall 1983; Reyes et al. 1994). Unlike other cucurbitaceous vegetables, the bitter fruit flavor of M. charantia is considered desirable for consumption, and thus bitter flavor has been selected during domestication (Marr et al. 2004). The bitterness of most cucurbits is mainly due to cucurbitacins (Decker-Walters 1999). The bitterness of bitter gourd is due to the cucurbitacin-like alkaloid momordicine (Fig. 2.1) and triterpene glycosides (momordicoside K and L) (Jeffrey 1980; Okabe et al. 1982). These compounds lack the oxygen function at C-11 that characterizes “true” cucurbitacins (Neuwinger 1994) and are the bitterest compounds in the plant kingdom (Johns 1990). A. Origin and Domestication The center of bitter gourd domestication likely lies in eastern Asia, possibly eastern India or southern China (Walters and Decker-Walters 1988; Miniraj et al. 1993). Uncarbonized seed coat fragments have been tentatively identified from Spirit Cave in northern Thailand. However, there have been no archaeological reports of bitter gourd remains in China (Marr et al. 2004). Moreover, a comprehensive compilation of plant remains from 124 Indian archaeological sites does not include bitter gourd (Kajale 1991). Wild or small-fruited cultivated forms, however, are mentioned in Ayurvedic texts written in Indian Sanskrit from 2000 to 200 BCE by members of the Indo-Aryan culture (Decker-Walters 1999), indicating an early cultivation of bitter gourd in India. The lack of a unique set of Indo-Aryan words indicates that the Aryans did not know bitter melon before entering India (Walters and Decker-Walters 1988).
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The most modern Hindi (Indian language) term “karela” may ultimately be of Dravidian origin (Turner1966). The earliest written reference to M. charantia in China was made in 1370 CE (Yang and Walters 1992). Both the domesticated and putative wild bitter gourd progenitors of bitter gourd are listed in floras of India, tropical Africa, and Asia as well as the New World tropics, where it first arrived in Brazil via the slave trade from Africa and then spread into Central America (Marr et al. 2004). Based on both historical literature (Chakravarty 1990; Miniraj et al. 1993; Walters and Decker-Walters 1988), and recent random amplified polymorphic DNA (RAPD; Dey et al. 2006a), intersimple sequence repeats (ISSR; Singh et al. 2007) and amplified fragment length polymorphisms (AFLP; Gaikwad et al. 2008) molecular analyses, eastern India (includes the states of Orissa, West Bengal, Assam, Jharkhand, and Bihar) may be considered as a probable primary center of diversity of bitter gourd, where a wild feral form M. charantia var. muricata (Chakravarty 1990) currently exists. Wild germplasm of bitter gourd has been important to the development of today’s crop. For example, a gynoecious line (DBGy 201) was isolated from wild and/or diverse relatively unselected landraces indigenous to eastern India and has been maintained through sib mating. The hybrids produced by using DBGy 201 as one of the parents have shown high percentages of pistillate (female) flowers and remarkable yield potential (Behera et al. 2008b). B. Nutritional Uses Bitter gourd fruits are a good source of carbohydrates, proteins, vitamins, and minerals (Table 2.1) and have the highest nutritive value among cucurbits (Miniraj et al. 1993; Desai and Musmade 1998). The vitamin C content of Chinese bitter gourd varies significantly (440–780 mgkg1 edible portion). Considerable variation in nutrients, including protein, carbohydrates, iron, zinc, calcium, magnesium, phosphorous, and ascorbic acid, has been observed in bitter gourd (Kale et al. 1991; Yuwai et al. 1991). Moreover, the crude protein content (11.4–20.9 gkg1) of bitter gourd fruits is higher than that of tomato and cucumber (Xiang et al. 2000). C. Medicinal Properties Bitter gourd has been used for centuries in the ancient traditional medicine of India, China, Africa, and Latin America. Bitter gourd extracts possess antioxidant, antimicrobial, antiviral, antihepatotoxic, and antiulcerogenic properties while also having the ability to lower blood sugar (Welihinda et al. 1986; Raman and Lau 1996). These medical
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Table 2.1. Proximate principles and nutrient composition of bitter gourd (Momordica charantia L.) fruit. Proximate principles Moisture (g/100 g) Carbohydrates (g/100 g) Proteins (g/100 g) Fiber (g/100 g) Calcium (mg/100 g) Phosphorus (mg/100 g) Potassium (mg/100 g) Sodium (mg/100 g) Iron (mg/100 g) Copper (mg/100 g) Manganese (mg/100 g) Zinc (mg/100 g) b Carotene Vitamin C
Quantity 83.20 10.60 2.10 1.70 23.00 38.00 171.00 2.40 2.00 0.19 0.08 0.46 126.00 96.00
Source: Gopalan et al. (1993). Nutritive value of Indian foods. National Institute of Nutrition, ICMR, Hyderabad.
activities are attributed to an array of biologically active plant chemicals, including triterpenes, pisteins, and steroids (Grover and Yadav 2004). Ethno-medical reports of M. charantia indicate that it is used in folkloric medicine for treatment of various ulcers, diabetes, and infections (Gurbuz et al. 2000; Scartezzini and Speroni 2000; Beloin et al. 2005). While the root decoctions have abortifacient properties, leaf and stem decoctions are used in treatment of dysentery, rheumatism, and gout (Subratty et al. 2005). In addition, juice of M. charantia drawn directly from fruit traditionally has been used for medicinal purposes worldwide. Likewise, the extracted juice from leaf, fruit and even whole plant are routinely used for treatment of wounds, infections, parasites (e.g., worms), measles, hepatitis, and fevers (Behera et al. 2008c). 1. Hypoglycemic Activity. Bitter gourd extracts traditionally used as vegetable insulin possess hypoglycemic, antioxidative, and antidiabetic agents (Vikrant et al. 2001; Chen et al. 2003) that are useful in the treatment of diabetes (Baynes 1995). The hypoglycemic effects (i.e., blood sugar lowering) of extracts have been well documented in animal (Raza et al. 1996; Sarkar et al. 1996; Ahmed et al. 1998; Raza et al. 2000; Ahmed et al. 2001; Grover et al. 2001; Miura et al. 2001; Grover et al. 2002; Rathi et al. 2002a,b; Kar et al. 2003; Ahmed et al. 2004; Chaturvedi et al. 2004; Miura et al. 2004; Sathishsekar and Subramanian 2005; Shetty et al. 2005) and human (Baldwa et al. 1977; Leatherdale et al. 1981;
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Welihindal et al. 1986; Srivastava et al. 1993) experiments. The beneficial hypoglycemic properties in fruit pulp, seed, and whole plant extracts have also been documented in rat analyses (Jayasooriya et al. 2000; Kar et al. 2003), and the medicinal attributes of such extracts have received broad review (Basch et al. 2003; Subratty et al. 2005; Krawinkel and Keding 2006). One study cites that there was a significant increase in the number of cells in the pancreas of streptozotocin-induced diabetic rats after 8 weeks of bitter gourd fruit juice treatment (Ahmed et al. 1998). In a parallel in vivo clinical human study, oral ingestion of all parts of the bitter gourd plant resulted in low patient toxicity (Rathi et al. 2002b). A mixture of steroidal saponins known as charantin (insulinlike peptides), as well as alkaloids, appears to be responsible for the hypoglycemic actions in bitter gourd extracts. Some studies have shown that at least three components (steroidal saponins, insulinlike compounds, and alkaloids) were found in bitter gourd plant parts that elicited hypoglycemic potential and/or other benefits for sufferers of diabetes mellitus. The hypoglycemic effect of these chemicals is more pronounced in fruit, where they are present in great abundance. Of the rich mixture of hypoglycemic compounds in bitter gourd fruit, charantin, vicine, and polypeptide-P are thought to provide the major diabetic medical benefits (Yeh et al. 2003; Table 2.2). Polypeptide-P, a previously unidentified insulinlike protein similar to bovine insulin, was identified in bitter gourd fruit and seed and in tissue culture (Khanna and Jain 1981). Although the mechanism of action of these hypoglycemic compounds is still debated, they either regulate insulin release directly or alter glucose metabolism and its insulinlike effect. 2. Antioxidant Activity. The antioxidant properties of carotenoids that protect plants during photosynthesis may also protect humans from carcinogens and mitigate free radical effects associated with heart disease. Natural antioxidants, primarily plant phenolics and polyphenolic compounds (e.g., in fruits and seeds of bitter gourd), are alternatives to synthetic antioxidants for alleviating oxidative deterioration in fruit. For instance, bitter gourd fruit contains as many as 14 carotenoids depending on stage of maturity (5, 6, and 14 in the immature, mature-green, and ripe stage, respectively), where cryptoxanthins becomes the principal chloroplast and chromoplast pigment found in ripe fruit (Rodriguez et al. 1976). Other carotenoids, such as b-carotene, zeaxanthin and lycopene (at ripe stage), and lutein and a-carotene (immature fruit) are also prevalent in the fruits, where they could serve as a model for studying carotenogenesis during ripening (Rodriguez et al. 1976). For instance, carotenogenesis in bitter gourd is not affected by temperatures above 30 C (Tran and Raymundo 1999); in contrast, in
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Table 2.2. Major phytochemicals in bitter gourd (Momordica charantia L.) fruit, and their health benefits. Phytochemicals
Plant parts
b-momorcharin
Seeds
Vicine
Seeds
Charantin
Fruits
Momordicosides A and B MAP 30
Seeds
Polypeptide-p
Seeds, fruits
Phenols
Seeds,
Carotenoids
Seeds, fruits
Seeds, fruits
Usefulness Glycoprotein that acts as midterm abortifacient Hypoglycemic glycoalkaloid Nonnitrogenous substance having hypoglycemic principle Triterpene glycosides that inhibit tumor growth Basic protein that inhibits human immunodeficiency virus (HIV). Hypoglycemic peptide, called plant insulin Antioxidants that reduce blood pressure and lower incidence of cancer and cardiovascular diseases Antioxidants that lower the incidence of cancer and cardiovascular diseases
Reference Chan et al. 1984 Dutta et al. 1981; Handa et al. 1990 Lotlikar and Rao, 1962 Okabe et al. 1980 Lee et al. 1990, 1995
Khanna and Jain 1981 Horax et al. 2005
Rodriguez et al. 1975, 1976
tomato, high temperatures inhibit lycopene but not b-carotene synthesis. Likewise, the total carotenoid concentration of bitter gourd seeds can be a 100-fold higher in the ripe than the immature stage, which is exclusively attributable to lycopene (96% of the carotenoids in ripe seeds; Rodriguez et al. 1975). Other chemo-preventive antioxidants in plants include vitamin C, vitamin E, phenolic acids, and organosulfur compounds (Simon 1997). Bitter gourd is also a rich source of phenolic compounds, where gallic acid, gentisic acid, catechin, chlorogenic acid, and epicatechin are typically abundant. While the concentration of phenolics varies with plant organ (fruit, leaf, root) and cultivar type, the highest content has been found in the Indian white-fruited (Fig. 2.2E), followed by China white-fruited, China green-fruited, and last India green-fruited (Horax et al. 2005). These plant phenolic compounds are potentially excellent natural sources of food antioxidants, given their abilities to reduce total cholesterol/triglycerides (Jayasooriya et al. 2000; Ahmed et al. 2001), blood pressure, and the incidence of cancer and cardiovascular diseases
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Fig. 2.2. Fruits of bitter gourd (Momordica charantia). (A) Fruit diversity (Dey et al. 2006a). (B) Large fusiform fruits, pointed at both ends, numerous triangular tubercles, giving the appearance of a crocodile’s back classified as M. charantia var. charantia (Chakravarty 1990). (C) Chinese long fruit type, 30–60 cm, smooth ridges, light green in colour, and slightly bitter (Yang and Walters 1992). (D) Small fruits (M. charantia var. muricata; Chakravarty 1990) high in proteins, carbohydrates, iron, calcium, (Desai and Musmade 1998) and Vitamin C (Behera et al. 2008c). (E) Triangular fruit type, cone-shaped, 9–12 cm long, light to dark green with prominent tubercles, moderately to strongly bitter (Yang and Walters 1992).
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(Tanaka et al. 1993; Balentine et al. 1997; Bravo 1998; Surh 1999; Gorinstein et al. 2002; Wang and Mazza 2002; Hannum 2004). 3. Antifertility Effects. Excessive consumption of the fruit and leaves of bitter gourd can reduce sperm production (Prakash and Mathur 1976). Bitter gourd ethanol seed extracts have also shown to have potent male antifertility effects (Basch et al. 2003) when administered to dogs (Dixit et al. 1978) and guinea pigs (Udoh et al. 2001). 4. Antiviral Activity. In recent years, a number of chemical components that possess medicinal attributes have been isolated from bitter gourd, such as a-momorcharin, which inactivates ribosome function (Feng et al. 1990; Leung et al. 1997) and stimulates MAP30 (Momordica anti-HIV protein) production, which, in turn, simultaneously suppresses HIV (human immunodeficiency virus) activity (Lee et al. 1990, 1995). Interestingly, momordicoside A and B present in bitter gourd inhibit tumor growth (Okabe et al. 1980), and several bitter gourd phytochemicals have in vitro antiviral activity against viruses including Epstein-Barr, herpes, and HIV viruses (Takemoto 1983; Lee et al. 1990; Nerurkar et al. 2006). 5. Antimicrobial Activity. The leaf extracts of bitter gourd possess antimicrobial activity principally against Escherichia coli, Staphylococcus, Pseudomonas, Salmonella, Streptobacillus, and Streptococcus (Omoregbe et al. 1996). Moreover, whole plant extracts have shown antiprotozoal activity against Entamoeba histolytica. Generally, fresh fruit extracts have exhibited similar antibacterial properties; more specifically, fruit extracts of M. charantia L. have demonstrated activity against tuberculosis and the stomach ulcer–causing bacteria Helicobacter pylori (Hussain and Deeni 1991; Omoregbe et al. 1996; Yesilada et al. 1999). Application of bitter gourd fruit powder to wound sites is similarly effective in stimulating tissue regeneration and wound healing in rats (Prasad et al. 2006). II. BOTANY A. Taxonomy and Morphology The genus Momordica belongs to subtribe Thladianthinae, tribe Joliffieae, subfamily Cucurbitoideae, of the Cucurbitaceae (Jeffrey 1990). The genus Momordica has 45 species domesticated in Asia and Africa (Robinson and Decker-Walters 1997). The genus Momordica has only
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six valid species in India, which can be grouped under two headings: M. charantia L. and M. balsamina L. representing the monoecious group and M. dioica Roxb., M. sahyadrica Joseph & Antony, M. cochinchinensis (Lour.) Spreng., and M. subangulata Blume (ssp. renigera (G. Don) W.J.J. deWilde) representing the dioecious group. Although the genus, as circumscribed here, does not include Momordica cymbalaria Fenz. [Luffa cymbalaria ¼ M. tuberosa (Roxb.) Cogn.)], some workers still treat it under Momordica (Joseph John 2005). Indian bitter gourd is classified into two botanical varieties based on fruit size, shape, color, and surface texture (Fig. 2.2A): (1) M. charantia var. charantia has large fusiform fruits, which do not taper at both ends, and possess numerous triangular tubercles giving the appearance of a “crocodile’s back” (Fig. 2.2B); (2) M. charantia var. muricata (Wild), which develops small and round fruits with tubercles, more or less tapering at each end (Fig. 2.2C) (Chakravarty 1990). Both varieties are widely cultivated throughout tropical and subtropical regions of India. Yang and Walters 1992 classified bitter gourd into three horticultural groups or types: 1. A small-fruited type where fruit are 10 to 20 cm long, 0.1 to 0.3 kg in weight, usually dark green, and very bitter 2. A long-fruited type (most commonly grown commercially in China) where fruit are 30 to 60 cm long, 0.2 to 0.6 kg in weight, light green in color with medium-size protuberances, and are only slightly bitter 3. A triangular-fruited type where cone-shape fruit are 9 to 12 cm long, 0.3 to 0.6 kg in weight, light to dark green with prominent tubercles, and moderately to strongly bitter. More recently, Reyes et al. (1994) reclassified Indian and southeast Asian M. charantia botanical varieties based on fruit diameter (M. charantia var. minima Williams & Ng < 5 cm and M. charantia var. maxima Williams & Ng > 5 cm). The morphological difference among six cultivated species of Momordica is described in Table 2.3. Cytogenetic studies confirmed the diploid chromosome number (2n ¼ 22) of M. charantia. Another species of Momordica (M. dioica; 2n ¼ 28), a dioecious cucurbit, has a different karyotype from the other two species (M. charantia, M. balsamina; 2n ¼ 22), but the meiosis in thesespecies is regular (Bhaduri and Bose 1947; Roy et al. 1966; Trivedi and Roy 1972). Crosses of M. charantia and M. balsamina (2n ¼ 22) with M. dioica (2n ¼ 28) are sexually incompatible (Singh 1990).Likewise,the crossM.charantia M.dioica (and reciprocal), failed to set fruit when normal pollen was used (Vahab and Peter 1993).
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Table 2.3. Important Indian bitter gourd (Momordica charantia L.) cultivars and hybrids and their salient economic and botanic features. Cultivar Pusa Do Mausami (OP)
Fruit features z
Pusa Vishesh (OP)
Arka Harit (OP)
Coimbatore Long (OP) VK1 Priya (OP) MDU 1 (OP) CO1 (OP)
Konkan Tara (OP) Punjab-14 (OP) Pusa Hybrid-1 (Hybrid) Pusa Hybrid-2 (Hybrid)
CO (Bgo)H 1 (Hybrid) z
Medium long (15–25 cm), green, club shaped unbroken surface ridges, 80–100 g. Medium long (15–20 cm) medium thick, glossy green, smooth broken surface ridges, 100–115 g. Short to medium long (12–18 cm), medium thick, grayish green with smooth surface broken ridges, 60–70 g. White, medium, long (20–25 cm) and thin, broken surface ridges, weight 60–75 g. Extra long (40 cm), green-spiny, and the stylar end typically whitish. Greenish white with continuous spine; length varies from 30–40 cm, 120 g. Dark green, medium long (25–30 cm) and thick (6–8 cm) with characteristics warts, 100–120 g. Green, prickly, medium long (10–15 cm) and spindle shaped, weight 45 g. Oblong and green, 35 g. Medium long and small to medium thick, glossy green, smooth broken surface ridges, 100 g. Dark green, medium long with medium thickness (length: 112.5 cm; breadth: 4.5 cm) with irregular smooth ridges, 110 g. Creamy white, light green–tinged stout fruits, 300 g.
OP: Open-pollinated variety
B. Reproductive Biology Wild-type bitter gourd is monoecious, where staminate and pistillate flowers (Fig. 2.3A, B) are borne on separate nodes. Flowering and fertilization occur between 35 and 55 days after sowing depending on growing conditions (Rasco and Castillo 1990; Reyes et al. 1994), and then continue for about 6 months in the tropics (Reyes et al. 1994). Anthesis typically occurs between 3:30 and 7:30 a.m., when flowers are completely open (Miniraj et al. 1993), and pollen viability is lost relatively rapidly (Desai and Musmade 1998). The stigma is usually receptive for 1 day before or after flower opening, after which it dries and turns brown (Rasco and Castillo 1990).
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Fig. 2.3. Monoecious flowering habit of bitter gourd; pistillate (A) and staminate (B) flowers are borne at different nodes. (C) A new gynoecious line (DBGy 202) was bred from germplasm collected in the eastern India (Behera et al. 2006). Arrows indicate nodes with pistillate flowers.
Flowering behavior varies with cultivar, climatic conditions, and cultural practices (Deshpande et al. 1979). The average ratio of staminate to pistillate flowers in monoecious lines throughout the flowering period is typically 50 : 1 (Rasco and Castillo 1990), but ratios can vary dramatically (i.e., 9:1 to 48 : 1) (Dey et al. 2005). While long photoperiods cause staminate flowers to bloom up to 2 weeks earlier than pistillate flowers, short days have the reverse effect (Huyskens et al. 1992). Nearly 90% of pistillate flowers borne on the first 40 nodes, and majority of them mature at nodes 21 to 30. Judicious pruning of lower laterals stimulates subsequent lateral branch production, which in turn tends to increase the total number of flowers per plant (Rasco and Castillo 1990). Bees are important pollinators of bitter gourd in India (Behera 2004). The predominant bee species in India is Apis florae, followed by A. cerana and A. dorsata. The pistillate flower of bitter gourd consists of an inferior ovary and a three-lobed, wet stigma that is attached to a columnar, hollow style (Pillai et al. 1978). The ovary contains three carpels typical of many cucurbits, each with 14 to 18 ovules, surrounded by an ovary wall. Although the number of ovules in an ovary can be up to 60, the average is 40. Anatropous ovules are attached to parietal placenta in two irregularly aligned rows in each carpel. Unlike other cucurbits, however, no more than four ovules can be seen in ovary cross-section. Typically, pollen tubes penetrate papillae tissue within 1 hour of pollination, arriving at the ovary cavities about 6 hours after pollination, and thus fertilization is accomplished within 18 to 24 hours postpollination (Chang et al. 1999).
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III. HORTICULTURE A. Climate and Soil Most of the cultivated Momordica species are similar in their cultural needs, except for the space requirement per plant, which is based on the type and extent of vine growth. Some of the cultural practices described herein reflect empirical knowledge collected by many generations of farmers. Reports of cultural practices based on research by agricultural scientists are meager except for bitter gourd. Momordica species grow well in hot, humid areas but also grow abundantly in subtropical climates and are day neutral. They are tolerant to a range of environments (Lim 1998) and can be grown in tropical and subtropical climates (Reyes et al. 1994). Bitter gourd is mainly cultivated during the spring, summer, and rainy seasons, with some winter production in subtropical climates. In contrast, it is cultivated through out the year in tropical climates. The optimum temperature for good plant growth is 25 to 30 C. Frost can kill the plants, and cool temperatures will retard development. The bitter gourd crop can grow above 18 C (Larkcom 1991), with 24 to 27 C being optimum (Desai and Musmade 1998). Bitter gourd performs well in full sun and is adaptable to a wide range of soil types but grows best in a well-drained sandy loam soil that is rich in organic matter. It grows well in soils of shallow to medium depth (50–150 cm), and like most cucurbits, bitter gourd prefers welldrained soils. For bitter gourd, the optimum soil pH is 6.0 to 6.7, but plants tolerate alkaline soils up to pH 8.0, whereas spine gourd prefers a pH of 6.0 to 7.0. Sweet gourd, in contrast, can tolerate soil salinity up to < 4 dS/m. B. Culture In bitter gourd, direct seeding is the usual production practice. Sometimes seedlings are transplanted directly to the field. The seed has a hard seed coat and germinates slowly due to slow absorption of water. For rapid germination, the optimum temperature is between 25 and 28 C. Presowing treatments, such as soaking of seeds in slightly warm water for 30 minutes followed by retention of seeds in a wet gunny bag or cloth bag in a warm place for 3 to 4 days, can increase the speed of germination. Poor germination percentage is common at suboptimal temperatures (Peter et al. 1998). Presowing treatments such as priming (mixing seeds with moist vermiculite for 36 hours at 20 C) and hot water (soaking seeds
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for 4 hours in water at 40 C) are therefore recommended for successful seedling establishment under suboptimal temperature (Lin and Sung 2001; Hsu et al. 2003). The field should be well prepared, plowed, and harrowed twice to remove weeds and other plant debris. Bitter gourd seeds are sown in raised mounds (beds) for the rainy season crop and in shallow pits for the summer crop in north India. The planting layout used by most farmers is 1 to 3 m between furrows and 0.5 m between hills with 3 seeds per entry at 10 cm apart within the row. Plant densities vary considerably over locations depending on the species and cultivars. Optimum plant density varies with cultivar, from 6,500 to 11,000 plants/ha (Reyes et al. 1994) or as many as 20,000 plants/ha (Huyskens et al. 1992). Bitter gourd requires a trellis to support the climbing vine. There are several methods of trellising. During the initial period of plant growth, effective weed control is important to the productivity of bitter gourd. Most weeds can be removed effectively manually or mechanically. Cultivation is also an effective method of controlling weeds. Organic or plastic mulching is used frequently for controlling the weeds. In plastic mulch, planting holes are bored in the plastic sheet at the appropriate planting distance, stretched over the planting beds, with edges held down by thin bamboo slats, and the plastic is stapled into the soil every 20 cm. Organic mulch, such as paddy straw or dry grass, is usually less expensive than plastic mulch and thus is used often. For trellis systems, the pits are cleaned manually and covered with organic mulch, then the interspaces are sprayed with postemergence herbicides. Bitter gourd will not tolerate drought and water stress, which can severely reduce the yield. Thus, appropriate soil moisture should be maintained in the upper 50 cm of soil where the majority of roots are located. Irrigation typically is applied weekly, beginning from the day of sowing (Desai and Musmade 1998). Fertilizer application rates depend on soil type, fertility level, and soil organic matter. Compost manure or farmyard manure is added to each planting hole before sowing and at 10 to 12 t/ha. Typically, application of 100:50:50 kg (N:P2O5:K2O)/ha is recommended (Robinson and DeckerWalters 1997). Recommended fertilizer rates and application schedule in sandy soils at the Asian Vegetable Research and Development Centre (AVRDC) are 184, 112, and 124 kg of N, P2O5, and K2O applied as onetime basal dose with four side dressings as appropriate (Palada and Chang 2003). Bitter gourd is sensitive to lack of micronutrients (e.g., boron), and the micronutrients are often incorporated to improve growth (Njoroge and van Luijk 2004).
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C. Sex Expression and Modification There is a wide range of sex expression in cucurbits (Behera et al. 2006). Cucurbits are predominantly monoecious, but dioecism occurs in pointed gourd (Trichosanthes dioica), kakrol (Momordica dioica), ivy gourd (Coccinia indica), and some feral forms. In M. charantia, Wang et al. (1997) found that initially plants bear hermaphroditic bud primordia that can produce either staminate or pistillate flowers. This process is correlated with RNA and protein synthesis, where soluble protein profiles of hermaphrodite flower buds, and staminate and pistillate flowers differ at three early developmental stages (7, 10, and 13 days after initial bud formation) (Wang and Zeng 1998). Predominant 11 and 30 kD proteins are present in pistillate and staminate flowers, respectively, and it is speculated that these proteins may be associated directly with sex expression (Wang and Zeng 1998). Sex expression is affected by environmental conditions under which M. charantia seedlings grow (Wang et al. 1997). Short-day cultivars, when grown under short photoperiods, exhibit rapid development and comparatively high gynoecy. To encourage a high frequency of pistillate flowers, short-day treatments should begin at seedling emergence and proceed to sixth-leaf stage (20 days postemergence under growing optimal conditions). Pistillate flower production under short photoperiods is increased by low temperatures (20 C) and nighttime chilling (25 C day/15 C night) (Yonemori and Fujieda 1985). Consequently, optimal conditions for gynoecious M. charantia seedling growth are short days and low temperatures (Wang et al. 1997a). The concentration of endogenous growth regulators and polyamines (e.g., spermine, spermidine, cadaverine, and putrescine) in shoot meristems of bitter gourd changes during plant development (Wang and Zeng 1997a). For instance, pistillate flower number increases as indoleacetic acid (IAA) and zeatin concentration decreases after anthesis (Wang and Zeng 1997b). Cadaverine content is also higher in staminate and pistillate flowers when compared to vegetative tissues (e.g., leaf and stem), suggesting a possible role in sex determination (Wang and Zeng 1997a). It has been hypothesized that the variation in spermidine content is related to the initiation and development of pistillate flowers while increases in endogenous putrescine concentrations are related to staminate flower initiation (Wang and Zeng 1997a). Foliar application of growth regulators can also modify sex expression (Ghosh and Basu 1982). For example, foliar application of gibberellic acid (GA3) treatment (25–100 mgL1) can dramatically increase gynoecy in bitter gourd, while cycocel (CCC; chlormequat) at concentrations of
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50 to 200 mgL1 promotes staminate flower development (Wang and Zeng 1996). Moreover, the appearance of the first staminate flower is delayed and pistillate flower initiation is promoted by relatively low concentrations of GA3 (0.04 to 4 mgL1) (Wang and Zeng 1997c). Likewise, foliar application of CCC promotes staminate flower development at 50 to 200 mgL1, and gynoecy at 500 mgL1. Foliar application of (2-chloroethyl) phosphonic acid (ethephon), malic hydrazide (MH), GA3, naphthaleneacetic acid (NAA), kinetin, IAA, 3-hydroxymethyl oxindole (HMO), morphactin, silver nitrate, and boron, when applied at 2- and 4-leaf stage of bitter gourd plants, can dramatically affect sex expression (Prakash 1976). Foliar application of silver nitrate (i.e., 250 mgL1 at the 5-leaf stage or 400 mgL1 at the 3-leaf stage) induces bisexual flower formation, where ovaries and petals are larger than typical pistillate flowers (Iwamoto and Ishida 2005). Likewise, dramatic increases in early pistillate flower appearance can result from foliar application of MH (250 ppm) and ethephon (200 ppm), and staminate flower development can be promoted by application of GA3 (i.e., 50–75 ppm) (Damodhar et al. 2004). Interestingly, foliar treatment of bitter gourd plants with IAA or HMO at 35 mgL1 increases total flower formation, which may be due in part to increased ethylene evolution (Damodhar et al. 2004). Regarding such ethylene-dependent sex determination processes, foliar application of ethephon at relatively low concentrations (255 mgL1) enhances pistillate flowering while application of moderately high concentrations (100 mgL1) depresses pistillate flower development. Likewise, although exogenous application of GA3 (20–40 mgL1) increases pistillate and staminate flower number, comparatively high concentrations of GA3 (60 mgL1) increases only pistillate flower number (Ghosh and Basu 1983). Finally, foliar sprays containing 50 ppm NAA stimulate early and abundant pistillate flower development (Shantappa et al. 2005); boron at 4 ppm enhances pistillate flowers production and fruit number and weight (Verma et al. 1984). D. Harvest Optimal timing of bitter gourd fruit harvest is often difficult to ascertain since bitter gourds are consumed before fruits are at physiological maturity (i.e., mature fruits are unmarketable). Optimal harvest is indicated by slight changes in fruit color and increased exocarp development (i.e., fullness of ridges and bumps), which are difficult to evaluate. Seed coat color is a good indicator of optimal harvest maturity (i.e., creamy or pale green-brown, with overmaturity indicated by pink coloration), but obviously it is not useful for easy determination of marketable fruit.
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Since fruit continues to mature after harvest, fruit for immediate sale in local markets should be harvested just prior to harvest maturity (i.e., physiologically immature), whereas fruit for long-distance transport must be harvested several days/weeks earlier than this (color maturity indicators given in Vujovic et al. 2000). Physical appearance and nutritional quality varies with cultivars and the stage of fruit development for harvest (Pal et al. 2005). Optimal bitter gourd fruit harvest typically occurs between 15 to 20 days after fruit set (i.e., 90 days after planting; Reyes et al. 1994). Nevertheless, due to wide culinary preferences, broad variation in harvest date is common. Harvestable fruits are, in general light green, thick and turgid (Lim 1998), where seeds are typically soft and range from white (Huyskens et al. 1992) to creamy with hues of pale green-brown depending on fruit maturity and variety (Vujovic et al. 2000). Harvests typically are made every 2 to 3 days since fruit ripen quickly (Desai and Musmade 1998). Fruits increase in bitterness during maturation due to an accumulation of the alkaloid momordicine, but they subsequently lose bitterness during the ripening process (Cantwell et al. 1996). E. Seed Production Long photoperiods cause staminate flowers to bloom up to 2 weeks before the pistillate flowers while short days have the reverse effect (Huyskens et al. 1992). Flowers open early in the morning, except for spine gourd, which opens late in the evening. Hand pollination can be avoided in bitter gourd by introducing beehives or by blowing pollen with a mister. Roguing of “off-type” plants is essential for the production of highquality bitter gourd seed (Behera 2004). This requires considerable expertise since distinct cultivar preferences exist among different consumers. Since bitter gourd is a cross-pollinated species, it is critical to maintain an isolation distance of between 0.5 to 1.0 km between cultivars or inbred lines during seed production (Sirohi 1997). Honeybees typically act as the chief insect pollinator for this crop and should be in abundance at flowering time. Commercial hybrid seed production of bitter gourd is accomplished by hand pollination. Experienced labors can pollinate 11 to 12 flowers per hour to each produce 15 seeds per fruit in an average commercial operation (Devadas and Ramadas 1993). Thus, the labor requirement for production of 1 kg of seed is 29 hours. Shantappa et al. (2005) indicated that seed yield can be optimized (840 kg/ha) if 50 ppm NAA or 250 ppm ethephon is applied at the 2- to 4-leaf stage.
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Since bitter gourd is, with rare exception, a monoecious plant, landrace seed is produced by hand pollination without emasculation. In controlled pollination, pistillate flowers of the maternal parent and staminate flowers of the paternal parent typically are isolated by bagging with paper envelopes about 24 hours before flowers open. Buds of staminate flowers of the paternal parent also can be covered with nonabsorbent cotton. The next day as flowers open, pollen is collected from the paternal parent and dusted directly onto the stigmata of flowers of maternal plants (Sirohi 2000). After hand pollination (preferably before 9:30 a.m.), the pistillate flowers are tagged and covered again for 4 to 5 days. Hybrid seeds are then extracted from the ripe fruits collected from maternal parents. F. Insects and Diseases Foliage pests and diseases tend to be of little consequence in bitter gourd, likely due to toxic compounds in the plant (Robinson and DeckerWalters 1997). However, pests are a serious problem in case of other Momordica species. The common pests and diseases of bitter gourd are described next. 1. Fruit Fly (Dacus cucurbitae). Maggots of fruit fly cause damage to young developing fruits. The adult fly lays eggs below the epidermis of the young ovaries. The eggs hatch into maggots, which feed inside the fruits and cause rotting. In homestead gardens, the fruits typically are covered with polythene, cloth, or paper bags to provide mechanical protection, and infested fruits are destroyed. Use of “cue lure” traps (10 traps per h) has been found effective. Insects that parasitize the fruit fly and sterilized male fruit flies are used for biological control. 2. Red Pumpkin Beetle (Aulacophora foveicollis). Adult beetles eat the leaves, resulting in holes in the foliage, and they also damage roots and leaves. The insect attacks at seedling stage as adults feed on cotyledonary leaves. This insect typically is controlled with insecticides. 3. Aphids (Aphis gossypii). This small insect damages the plants by sucking the leaf sap. In the young plant stage, cotyledonary leaf margins “crinkle” and in severe cases, plants wilt. More serious losses are caused by aphids transmitting viral diseases. Some aphidicides are applied
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systemically to the foliage for insect control. Contact insecticides often are applied to the underside of the leaves. 4. Fusarium Wilt. The causal organism of Fusarium wilt has been identified as Fusarium oxysporum f. niveum. Leaves wilt suddenly, and vascular bundles in the collar region become yellow or brown. It is difficult to control the disease since the fungus persists in the soil. The use of disease-free planting materials during sowing is recommended as a disease control. The fungus can also be controlled by nonchemical methods, namely by cleft grafting bitter gourd shoot (scion) onto Luffa (rootstock). Luffa provides an excellent rootstock for bitter gourd, and grafting can increase yields substantially (e.g., in Taiwan), mainly by controlling Fusarium wilt infestation (Lin et al. 1998). 5. Anthracnose. Anthracnose is caused by Colletotrichum spp. Small yellowish spots appear on leaves as water-soaked areas, which enlarge in size, coalesce, and turn brown to black in color. Seed treatment, proper crop rotation, and clean cultivation minimize initial inoculums. The disease is also effectively controlled by systemic fungicides. 6. Powdery Mildew. Powdery mildew is caused by Sphaerotheca fuliginea. Initially white or fluffy growth appears in circular patches or spots on the undersurface of the leaves. Severely infected leaves become brown and shriveled, and defoliation may occur. Fruits of affected plants do not fully develop. Seed treatment and soil drenching with systemic fungicides provides protection at early stages of crop development. 7. Downy Mildew. Downy mildew is caused by Pseudoperonospora cubensis. Symptoms appear as irregularly shape yellow to brown angular spots appears on upper sides of the leaves, usually at the center of the plant. Under moist conditions, a purplish mildew typically develops on the underside of the leaf spots. Leaves die as neurotic spots increase in size and cause severe defoliation. Spread is often rapid from the crown toward new growth. Moist conditions favor the development of this disease, but the application of an array of different fungicides can prevent the spread of the fungus. 8. Virus. Bitter gourd is a host of watermelon potyvirus, cucumber green mottle virus (both transmitted by white fly), and bitter gourd mosaic virus (transmitted by aphid). Uprooting and destruction of affected plants and collateral hosts is a common means of control.
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IV. BREEDING A. Genetic Variation and Germplasm Development The morphological documentation (e.g., passport data) and characterization (assessment of genetic diversity) of bitter gourd germplasm (both cultivated and wild types) was undertaken between 1965 to 1972 by a consortium of workers from Germany, the United States, Japan, China, Thailand, the Philippines, and India. This consortium was funded through the National Bureau of Plant Genetic Resources, Indian Agricultural Research Institute, Kerala Agricultural University, and the Indian Institute of Horticultural Research. More recently, molecular markers (RAPD: Dey et al. 2006a; ISSR: Singh et al. 2007; and AFLP: Gaikwad et al. 2008) have been used to assess the genetic diversity of Indian bitter gourd genotypes including two promising gynoecious lines, DBGy-201 and DBGy-202 (Fig. 2.3C). Awide range in genetic diversity was detected, indicating that a standard accession reference array for future analyses might include Pusa Do Mausami-green, Pusa Do Mausami-white, DBTG-2, Mohanpur Sel-215, and Jaynagar Sel-1. Regardless of marker analyses type, however, several accessions from West Bengal (Eastern Indian province) are genetically distinct from other common landrace accessions in north Indian provinces [genetic similarity (GS) ¼ 0.57 to 0.72]. Genetic differences between M. charantia var. charantia and M. charantia var. muricata accessions are indicative of their use as potential parents for the establishment of narrow- and wide-based mapping populations (Behera et al. 2008b). Such exotic populations have been informative for the characterization of qualitative and quantitative traits in other cucurbit species (Serquen et al. 1997; Zalapa et al. 2007). In bitter gourd, gynoecy is particularly interesting for hybrid development (e.g., gynoecious monoecious lines) and their commercial production. The commercial deployment of gynoecy in hybrid technology avoids the tedious step of manual removal of staminate flowers during the hand-production of monoecious monoecious hybrids. The utilization of such gynoecious lines allows for the production of gynoecious or predominantly gynoecious lines that provide early, uniform, high-yield potential (Ram et al. 2002a). The hybrid Cuilli No.1 (China), for instance, was developed by utilizing a gynoecious line as a maternal parent (Zhou et al. 1998). Likewise, gynoecious lines originating in India were identified by Behera et al. (2006; lines DBGy-201 and DBGy-202) and Ram et al. (2002b; line Gy263B) for use in hybrid development programs. Commercial bitter gourd cultivars and a few accessions/lines with potentially important horticultural traits have been deposited and
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registered in national germplasm collections. For example, the National Bureau of Plant Genetic Resources (NBPGR), New Delhi, India, possesses unique accessions, such as IC 256185, IC 248256, IC 213311, IC 248282, IC 256110, and IC 248281 (Dhillon et al. 2005; resistant to fruit fly); NIC-12285 and VRBT-39 (Pandey and Singh 2001; resistant to downy mildew); IC 202195 (high yield and long-fruited type); TCR 404 (high yield and white-fruited type); EC 399808 (high yield and greater number of fruits); and INGR 03037 (gynoecious sex with high yield) that can be used directly by plant breeders. Wild bitter gourd ecotypes and botanical varieties (e.g., M. charantia var. muricata) are also important sources of economically important traits (e.g., resistance against Dacus cucurbitae; Dhillon et al. 2005). In the case of resistance to D. cucurbitae, host response varies dramatically among the cultivars (Yadav et al. 2003), where fruit fly infestation has been shown to be lowest in PBIG-123 (12.08%) and Pusa Do Mausami (13.39%), and highest in JMC-4 (41.49%). Breeding for nutritional/medicinal quality typically emphasizes accessions with relatively high vitamin C content (Dey et al. 2006b). For example, bitter gourd lines DBTG-3, DBTG-8, DBTG-6, and DBTG-9 contain > 1000 mgkg1 vitamin C in edible plant parts as compared to 500 mgkg1 in standard cultivated types (Dey et al. 2006b). These highvitamin-C lines are aggressively used in breeding programs whose focus is on the development of cultivars with high nutritional values. High quality is also found in Indian bitter gourd cultivars possessing high total soluble solid content (>3.1 Brix; MC-84, Preethi, RHRBG-5, and PBIG-1) and elevated vitamin C (>950 mgkg1; Konkan Tara, and Hirkani) and fruit protein (>1.5%; DVBTG-1, Preethi, Hirkani, and Konkan Tara) content (Kore et al. 2003). B. Inheritance 1. Seed and Fruit Characters. Light brown seed (lbs) coat color is recessive to dark brown (Srivastava and Nath 1972). Large seed (ls) size is recessive to small seed size (Srivastava and Nath 1972); white epicarp (w) is recessive to green (Suribabu et al. 1986; Vahab 1989); and spiny fruit (triangular tubercles) is dominant over smooth (Vahab 1989). Since immature bitter gourd fruits are sliced during the preparation of various Asian meals, exceptional internal fruit quality and uniform green peel color are desirable. Liu et al. (2005) reported high heritability of fruit color (green vs. white) controlled by two genes where green is dominant to white (Miniraj et al. 1993; Hu et al. 2002; Liou et al. 2002). In addition to appropriate internal color, fruit must be firm, without excessive seed
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development, and free of internal defects, such as decay and splitting. Fruit color also governs its marketability, although color preference differs among regions. For example, green-fruited types are in demand in southern China while white-fruited types are preferred in central China. Similarly, dark green to glossy green fruits are favored in northern India whereas white fruits are preferred in southern India. 2. Sex Expression. In contrast to recent findings of Ram et al. (2006) and Behara et al. (2009), gynoecy (gy1) is recessive to monoecy in India germplasm. Iwamoto and Ishida (2006) reported that gynoecious sex expression was partially dominant in bitter gourd. Their observations, however, were made using Japanese germplasms (i.e., line LCJ 980120; predominantly female). Regardless of genetic control, both studies suggest that such gynoecious or predominantly female lines hold promise for the development of gynoecious F1 hybrids. 3. Bitterness. Bitterness (higher amount of glycosides) is particularly important to cultivar development. It displays monogenic inheritance with more bitterness dominant to less (Suribabu et al. 1986). 4. Yield. Singh and Ram (2005) determined that complementary epistasis and dominance dominance interactions were important genetic determinates of yield. Given these facts, Devadas and Ramadas (1994) recommended that selection and hybridization (i.e., reciprocal recurrent selection) would be an appropriate breeding strategy for improvement of fruit triterpinoid content. The genetic analysis of a large-fruited (M. charantia var. charantia/maxima) small-fruited (M. charantia var. muricata/minima) population has indicated that small fruit was partially dominant over large fruit (Kim et al. 1990). In contrast, fruit length was incompletely dominant and is controlled by a minimum of five genes (Zhang et al. 2006). Likewise, the dramatic role of epistatsis in the development of fruits suggests that breeding for this trait will be challenging (Sirohi and Choudhury 1983; Chaudhari and Kale 1991). C. Character Association Genotypic correlation coefficients in bitter gourd are greater than phenotypic coefficients (Dey et al. 2005). Nevertheless, phenotypic evaluation of yield and quality characteristics used in path coefficient analysis revealed that fruit weight had the greatest direct effect on yield, followed by number of fruits per plant and fruit length. Ascorbic acid content and
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total carotenoid content had a strong negative but indirect effect on marketable yield based primarily on fruit weight, and fruit length and diameter. Thus, selection for small-fruited cultivars could improve ascorbic acid and total carotenoid content. Fruit length, average fruit weight, and number of fruits per vine are controlled by additive factors, and thus have direct positive effects on fruit yield (Sharma and Bhutani 2001; Dey et al. 2005). Consequently, simple selection strategies (e.g., backcrossing) focusing on flowering duration, harvesting span, fruit length and diameter, fruit rind thickness, average fruit weight, number of fruits per vine, dry fruit weight, dry matter per vine, and harvest index could be used to improve bitter gourd yield. In contrast, genetic dominance and complementary gene action associated with some of these traits combined with their low narrowsense heritability indicate that hybrid breeding would be an advantageous strategy when breeding for increased yield in this crop species (Celine and Sirohi 1998; Mishra et al. 1998). In bitter gourd, several genetic studies have determined that an association exists between morphological traits and insect resistance and that these associations may be useful for indirect selection during resistance breeding (Dhillon et al. 2005). For instance, percentage of fruit infestation by gourd fly is positively correlated with rib depth, flesh thickness, fruit diameter and length and negatively associated with fruit toughness (Dhillon et al. 2005). Thus, relative fruit toughness might be used as a selection criterion during the development of fruit fly–resistant cultivars. In this regard, Tewatia and Dhankhar (1996) reported resistance to fruit fly is dominant, and that additive and dominance gene effects, as well as duplicate epistasis, are important components of resistance. Thus, reciprocal recurrent selection was suggested as an appropriate breeding strategy for improvement of this trait. Dhillon et al. (2005) observed a significant and positive correlation (r ¼ 0.96) between percentage fruit fly infestation and several fruit characters. In fact, genetic analysis has indicated that total variation for fruit fly infestation and variation for larval density/fruit is associated with variation in flesh thickness and fruit diameter (r ¼ 0.93), and flesh thickness and fruit length (r ¼ 0.76), respectively. Thus, it appears that phenotypic selection during backcrossing could be practiced directly on these traits for population improvement. Fruit composition components including ascorbic acid, nitrogen, phosphorus, potassium, protein, reducing sugars, nonreducing sugars, and total sugars are negatively correlated with fruit fly resistance while the moisture content is positively associated with these components. The negative correlation between fruit quality and fruit fly resistance is,
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in fact, a challenge for breeding programs focused on combining both these traits in improved germplasm. D. Goals and Cultivar Development A wide range of quantitatively and qualitatively inherited phenotypic variation is present in Asian bitter gourd (Behera 2004). The manipulation of these traits forms the basis for plant breeding program goals. The seven most important points of consideration in this regard are: 1. Cultivars must meet international export standards (fruits must be green, 20–25 cm long, and possess a short neck. 2. Cultivars should possess characteristics that enhance nutrition, such as high vitamin (carotenoids and ascorbic acid) and mineral (iron and calcium) content. 3. Gemrplasm with improved abiotic stresses resistance (high temperature, water deficiency, salt tolerance) could be beneficial. 4. Nonbitter cultivars with medicinal benefits such as proteins (charantin), polypeptides (polypeptide-K), glycoalkoloids, phenolics and other antioxidants have better utility. 5. Gynoecious with high yield potential would increase profitability. 6. Germplasm with pest resistance (virus, powdery and downy mildew, and red pumpkin beetle) could broaden bitter gourd’s planting range. 7. Cultivars with high fruit quality with late seed maturity, minimized ridges, with uniform green color in a range of fruit sizes are desirable. Several hybrid and open-pollinated (i.e., usually landraces) cultivars have been released for bitter gourd cultivation (Sirohi 1997), and about 80% of the crop is from established F1 hybrids. Hybrids usually provide higher yields than open-pollinated cultivars, but hybrid seed is relatively expensive and must be purchased each planting season. In India, the choice of cultivar depends on regional consumer preference for fruit shape, internal and external color, ridging, and degree of bitterness. The most popular Indian bitter gourd cultivars are listed in Table 2.4. Several bitter gourd cultivars also have been released in China. Prominent among the hybrids grown is the Fusarium wilt and powdery mildew resistant Cuiyu, which produces dark green, warty-skinned fruit that are 30 to 35 cm long having an average fruit weight of between 500 and 700 g (Chang et al. 2005). Similar in fruit size (30–50 cm) and
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Table 2.4. Morphological variation among 8 species of Momordica (De Wilde and Duyfjes 2002) including M. sahyadrica. M. charantia L. Plant: Annual, slender climber, 2–4 m high, scarcely to densely pubescent (tender parts wooly), monoecious. Stem: Round, internodes 5–6 cm; tendrils delicate, 12–15 cm long. Leaf: Deeply and palmately 5–9 lobed, reniform to orbicular or suborbicular in outline, 2.5–8 4–10 cm, cordate at base, acute or acuminate at apex, lobes ovate or obovate, narrowed at base, margins sinuate to undulate, mucronate; petioles 1.5–5 cm long. Flower: Male flower stalks slender with bract midway or toward base; peduncle 2–5 cm long; bract reniform, 5–11 mm diam., green, pedicel 2–6 cm long; receptacle-tube cup shape, 2–4 mm long and 2–3 mm wide; sepals ovate-elliptic, 4–6 2–3 mm, pale green; petals obovate, 10–20 7–15 mm, mucronate at apex, scales 2; filaments 1.5–2 mm long, inserted in the throat of the receptacle tube; anthers coherent. Female flower peduncle 1–6 cm long; bract 1–9 mm diameter; pedicel 1–8 cm long; sepals narrow, oblonglanceolate, 2–5 mm long; petals smaller than or equal to that in male, 7–10 mm long; ovary fusiform, narrowly rostrate, 5–11 2–3 mm, muricate, tuberculate or longitudinally ridged; style 2 mm long. Fruit: Pendulous, stalk 2–8 cm long; fruit discoid, ovoid, ellipsoid to oblong or blocky, often narrowed at ends, sometimes finely rostrate, 3–20 2–5 cm, white or green turning orange on maturity, soft tuberculate with 8–10 broken or continuous ridges, splitting from base in to 3 irregular valves. Seed: 5–30, squarish rectangular, ends subtridentate, faces compressed, sculptured, 5–9 3–6 mm, margins grooved; testa brown or black. M. balsamina L. Plant: Annual, slender, trailing herb, 1.5–3.0 m high, subglabrous, monoecious. Stem: Round, internodes 5.5–6 cm; tendrils delicate, 11–13 cm long, basal 1–1.5 cm uncoiled. Leaf: Lobed (5–7), subcircular in outline, 4–6 cm diam., base cordate with a cuneate petiole-blade juncture, apex mucronate, lobes rhomboid, margins acutely 3–7 lobulate; petiole 1–4 cm long, slender, puberulous. Flower: Staminate flowers larger than pistillate; peduncles slender 3–5 cm long; bract subapical, suborbicular, up to 0.6 0.5 cm, pale green, cordate at base, margins finely dentate; pedicel 0.3–0.4 cm long, receptacle tube cup-shaped, up to 0.2 mm long; sepals ovate, up to 0.7 0.3 mm, obtuse, pubescent; petals obovate, 1–1.3 0.7–0.9 cm, pale yellow to creamish-yellow, undulate margins, scales in 2 petals only; filaments up to 0.2 mm long, inserted on the rim of the receptacle tube, anthers up to 1.2–1.8 mm long. Pistillate flowers 1.7–1.8 cm across; peduncles 0.2–0.3 cm long; pedicels 0.4–0.6 cm long; bract small; calyx minute, thread like, thin; petals 0.8 0.8 cm, pale yellow to creamish-yellow undulate margins; ovary ovoid to fusiform, 5–7 mm long, style short, slender, whitish yellow. Fruit: Ovoid to ellipsoid, bulged at middle, 2.5–3.5 (4.0) cm long, 1.8–2.0 cm in circumference and stalk 1–2 cm long, shortly rostrate, ashy-olive green with 2–3 white tubercles in lines across the whole length of fruits; fruits turning orange and later scarlet red on ripening; pericarp thin. Seed: 3–5, covered by deep red sarcotesta, ovate oblong, compressed, 8.5–9.5 5.9–6.2 mm, and margins finely grooved, crenulate; testa grey or light brown. (continued)
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M. dioica Willd Plant: Vine climbing up to 3–10 m high, tuberous roots, dioecious. Stem: Slender, the internodes 3–8 cm long. Tendrils axillary, 4–12 cm long, the basal 2–4 cm straight and the rest spiral. Leaf: Thin, light green to green, ovate-cordate, nearly triangular in outline, lobed and sublobed to various degrees or cordate and cuneate at base, the margins entire, undulate, irregularly or coarsely; the upper surface and margins with scattered short hairs, the lower surface densely short hairy; petiole slender to medium thick, 3–7 cm long, 1–1.5 mm in diameter, longitudinally grooved. Flower: Staminate flowers solitary; peduncles 3–7.5 cm long (usually 5–6 cm), light green, thin; pedicels sub sessile, 2–3 mm long, whitish yellow, subtended by and protected inside a reniform clasping swollen bract, 4–5 8–10 mm, light green; calyx funnelshaped, lobes 5, light green, narrow acute, up to 6 1 mm; petals 5, free, pale yellow, glandular, oblong-lanceolate, 12–22 5–8 mm. Stamens 5, two of them with a pair of anthers and the other with a single anther, filaments 2–3 mm long, anthers subtriangular, 2–3 mm long, yellowish brown on inner side. Pistillate flowers solitary in leaf axils; peduncles thin, very short 0.5–2.0 cm long; pedicels thin, 2–4 cm long, subtended by a small bract of 3–4 2–6 mm; bracts reniform with acute tip just like in male but of small size; sepals 5, semipersistent, green, narrow, 3–6 0.8 mm, acute at apex; petals 5; ovary oblong-ovoid, 6–9 2–3 mm, rounded at base; styles short, up to 4 mm long, glandular hairy. Fruit: Oblong, rounded at base, abruptly conical with rostrate tip at apex, 3–4 2–3 cm, the entire surface covered with soft short spines (except the beak), light green or dark green, turning uniformly orange on ripening, splitting from base into three irregular pieces and rolling back exposing scarlet red arils (seeds). Seed: 2–3 mm across, black lustrous and golden-lined (when fresh), sculptured on surfaces, small round to slightly oval or shortly stellate (round-ovate and smooth in Central Indian specimens), seed coat brittle, shell hard, membrane thin, whitish, endosperm oily with characteristic aromatic odor when crushed. M. sahyadrica Plant: Robust climber, vines up to 5–6 m high, tuberous roots with outer skin brownish and inner flesh whitish yellow, dioecious. Stem: Stout, the internodes 5–10 cm long, nodes quadrangular, blackish green, distinctly long hairy. Tendrils medium thick, unbranched, 8–15 cm long, 4–5 cm of base uncoiled, remaining coiled.. Leaf: 3–5 lobed or entire, 10–16 8–18 cm, deeply cordate at base with a subangulate juncture with petiole, petiole 3–8 cm long, 1–1.5 mm. in diameter; blades medium thick, ovate, broadly triangular in outline, sometimes hastate, acute, or acuminate at apex, margins highly variable, entire, undulate or coarsely crenulate, lateral veins 5–7 pairs, the lower pair running close to the margin of the subangulate petiole juncture, hairs short, scattered without, snowy white within. Flower: Staminate flowers axillary, solitary; peduncles 2–5 cm. long; dark green, pedicels short, 0.8–1 cm. long, whitish green subtended, and covered by an inflated bract, up to 1 1.5 cm, reniform; calyx base funnel shape, up to 8 mm long and 1 cm across; petals 5, free, fleshy, obovate, up to 4 1.5 cm, bright yellow with a greenish yellow narrow base; stamens 3, two of them with a pair of anthers, the other with a single anther, filaments up to 3 mm. Pistillate flowers solitary in leaf axils; peduncles 0.5–2.0 cm, pedicel short, up to 0.5 cm long, subtended by a small rudimentary bract, 1–3 0.5–5 mm; sepals 5, green, persistent, 0.8–1.3 1–3 mm, equal, lanceolate, acuminate at apex densely glandular
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Table 2.4 (Continued)
hairy within and without; petals 5, free, fleshy, up to 4 2 cm., narrow, greenish yellow, widening toward middle, bright yellow; ovary inferior, oblong-ovoid, 1–1.5 0.2–0.4 cm; style up to 6 mm long, whitish yellow, stigma up to 4.0 9.0 mm, cushiony, trifid. Fruit: Broadly ellipsoid, ovoid to fusiform with round blossom end and rostrate distal end, 5–7.5 3–4.2 cm in size, 9–12 cm in circumference, 35–50 gm in weight, dark green turning bright orange on ripening, densely clothed with soft short spines; spines 2–4 mm long; arils sweet taste, ripe fruits aromatic and slightly bitter. Seed: Black, shining, losing its luster on drying, round stellate to slightly cog wheel shape, warty-dentate on margins sculptured on faces with irregular furrows and ridges, 0.2–0.3 0.2–0.3 cm, seed coat brittle, hard shell–like, the membrane very thin, smooth, blackish green, conspicuously veined, endosperm oily, distinctly aromatic when crushed. M. subangulata Blume Plant: Vine climbing up to 8–10 m high, tuberous roots, dioecious. Stem: Stout, the internodes 7–11 cm, Tendrils simple, axillary, 15–17 cm long, the basal 5–7 cm erect, the rest when uncoiled. Leaf: Light green, ovate cordate, unlobed, 8–12 7–11 cm., acuminate at apex, cuneate at base, the basal flaps almost touching the petiole, the margins undulate; veins 3–5, ascending and many pinnate from midrib ending up in fine network of areoles, 4–5 mm across, glabrous above, glandular hairy below; petioles 7–10 cm long, thick, channeled longitudinally, margins finely ridged. Flower: Staminate flowers large, solitary, axillary, showy, creamish yellow, up to 9 cm across; peduncles 4–6 cm long, pedicel 0.5–1 cm long, subtended and covered inside a reniform bract, 2 2.5 cm, light green, sepals 5, greenish crimson, united at the base; petals 5, 5–6 3–4 cm, free, fleshy, 3 inner petals with blackish purple blotch of 7 6 mm size and long glandular hairs; nectary, orange yellow, enclosed in calyx cup; stamens 3, two of them with a pair of anthers, the other with a single anther, filaments up to 4 mm long, black on sides. Pistillate flowers with peduncles short, 1–1.3 cm long, pedicels 10–17 cm long; bracts minute, rudimentary, near axil, often a scar of 2 1 mm size; sepals 5, 5–9 1–1.5 mm persistent, acute at apex; corolla and scales as in male; ovary oblong ovoid, dark green, 1.5–2 0.6 cm., rounded at base, finely echinulate on surface; style 5 to 7 mm long, pale yellow, stigma cushiony, up to 4 6 mm, trilobed. Fruit: Broadly ellipsoid, with dome-shape ends, 7–8 13–14 cm, each weighing 50–80 g; densely softly echinate, rarely with remnant ridges at base, spines 2–3 mm long, light green turning yellow and finally bright orange on ripening, exposing the seeds (35–50 per fruit) by basal splitting of the fruit and rolling back of the split lobes; flesh thick (5–6 mm), aril deep red. Seed: Flat, suborbicular to subtridentate, rectangularly stellate–cog wheel shape, 6 3 mm and up to 4 mm thick, sculptured on faces with grooves and dented edges, margins with a double row of wart- like small protuberances. M. cochinchinensis (Lour.) Spreng Plant: Stout perennial climber up to 20 m high, roots tuberous, woody, all parts glabrous, dioecious. Stem: Round, internodes 5–6 cm; tendrils delicate, 11–13 cm long, basal 2–2.5 cm uncoiled. Leaf: Entire or 3–5, palmately lobed, or 3 foliolate (leaflets elliptic with minute petiole), broadly ovate or suborbicular in outline, up to 10 16 cm, base cordate (sometimes with 2–4 glandular beadlike projections toward cordate margin), acute or acuminate at apex or acuminate, margins entire, undulate or remotely dentate; petiole 5–12 cm long. (continued)
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Table 2.4 (Continued) Flower: Solitary, axillary, staminate sometimes in a loose fascicle of 5–7, with a separate basal one. Staminate flowers with subapical bract; peduncles 8–12 cm long, bract cucullate, suborbicular or reniform, 20–40 mm wide, rounded at base, acute at apex, margins undulate; pedicels 5–8 mm long, receptacle tube saucer shape, 4–5 8–12 mm, blackish outside; sepals 0–12 4–8 mm, ovate– oblong or triangular, acute at apex, blackish; petals subelliptic, 2.5–4 purple bull’s-eye mark at base, filaments short, fleshy, 5–6 mm long, inserted at the base of the receptacle tube, anthers variable in size, S shape, connective swollen. Female flower with small or rudimentary bract; sepals linear oblong, 4–10 mm long; petals as in male; ovary ellipsoid oblong, 12–15 mm long, densely soft muricate; style 8–9 mm long. Fruit: Ovoid or oblongoid, bulged at middle, 10–15 6–10 cm, rostrate at base and stalk 5–12 cm long; pericarp densely tuberculate with uniformly short round conical structures or interspersed with larger tubercles; single fruit weighing between 350–500 g or more, green turning orange on ripening and bursting irregularly. Seed: Many, variable in size, 1–1.5 0.8–1.2 cm, broadly ovate hexa-octagonal with flat sculptured surfaces, subtridentate at ends and margins, testa black.
Momordica foetida Schumach Plant: Dioecious, perennial herb, trailing or climbing with simple or bifid tendrils. Stem: Grows up to 4.5 m long, with dark green flecks when young, woody when old, rooting at the nodes. Leaf: Alternate, simple; stipules absent; petiole 1.5–17 cm long; blade broadly ovate–cordate to triangular–cordate, 1.5–16 cm 1.5–17 cm, base deeply cordate. Flower: Unisexual, regular, 5-merous; calyx with obconic tube and lobes up to 11 mm long; petals free, obovate-lingulate, up to 3.5 cm long, white, pale yellow to orange-yellow, 3 with scales inside at base; staminate flowers 1–9 together in fascicles on peduncle 2–23 cm long, with 3 stamens, anthers coherent in center of flower; female flowers solitary in leaf axils, with inferior, ovoid ovary, stigma 3-lobed. Fruit: Ellipsoid berry up to 7 cm 5 cm with a long-stalked, orange when ripe, densely and softly spiny, dehiscing with 3 valves and exposing the many seeds embedded in scarlet pulp. Seed: Oblong, flattened, c. 1 cm long, brown, testa sculptured, margins 2-grooved. Momordica rostrata Zimm. Plant: Dioecious, perennial herb with tuberous roots, trailing or climbing with simple tendrils. Stem: Grows up to 7 m long, becoming woody with gray bark. Leaf: Alternate, pedately 9-foliolate; stipules absent; petiole up to 2.5 cm long; central leaflet elliptical to almost circular, 1–4.5 cm 1–3 cm, lateral leaflets smaller. Flower: Regular, 5-merous; male flowers in axillary, 1–14–flowered, umbel-like clusters with peduncle up to 10 cm long, sepals triangular, 2–4 mm long, petals oblong, 7–13 mm long, rounded, pale orange-yellow, stamens 3, free; female flowers solitary, subsessile, sepals triangular-lanceolate, 1.5–2 mm long, petals c. 8 4 mm, ovary inferior, narrowly ovoid, 12–14 mm long and 2.5–3 mm across. Fruit: Ovoid berry 3–7 cm 1.5–3 cm, beaked, rounded or slightly 8-angled, bright red, with many seeds embedded in yellow pulp. Seed: Broadly ovate, ca. 14 mm long, blackish brown, testa sculptured and margins grooved. Source: Joseph and Antony (2007).
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weight (500 g) is the virus-resistant hybrid Hengza No. 2 (Xiao et al. 2005). It differs from Cuiyu in that fruits are straight, cylinderical, and glossy green. Another commonly grown bitter gourd is the powdery mildew resistant hybrid Chunyu, which bears green fruit with spines that are on average 26 to 28 cm in length and 326 g in weight (Hu et al. 2002). In Australia, open-pollinated cultivars (typically Vietnamese types) are preferred by growers. However, more recently growers are adopting hybrid cultivars, which provide comparatively greater yields (Morgan and Midmore 2002). Australian vegetable seed companies sell both hybrid and open-pollinated cultivars. The cultivars Kiew Yoke 59, Known You Green, Verdure, Moonrise, Moonlight, and Moon Beauty are widely grown. In southern Taiwan, three major bitter gourd cultivars, Pintong Black Seed, Moonshine (F1), and Highmoon (F1), constitute 70%, 20%, and 10% of the commercial production area, respectively (Liou et al. 2002). In addition, the popular open-pollinated heat-tolerant variety Pintong Black Seed is also suitable for tropical regions (Liou et al. 2002). E. Methods Several methods usually are employed in tandem to accomplish breeding objectives. Single plant selection, mass selection, pedigree selection, and bulk population improvement are common methods used for bitter gourd enhancement (Sirohi 1997). Pedigree selection typically is used after crossing two parents for the development of inbred lines with high, early yield borne on a unique plant habit, and/or with high-quality fruit [i.e., processing quality, high vitamin C and A (carotenes), and disease resistance]. However, strategies that incorporate selection for disease resistance and improved yield require judicious implementation, since selection for disease resistance can be negatively correlated with yield, as is found in cucumber (Staub and Grumet 1993). Marker-assisted selection could prove beneficial in this species if technologies (map construction and quantitative trait loci (QTL) analysis) were appropriately advanced (Staub et al. 2004; Fan et al. 2006). 1. Heterosis. As bitter gourd is a cross-pollinated crop, exploitation of heterosis (hybrid vigor) is an important aspect of its improvement. Heterosis in bitter gourd was investigated at the Indian Agricultural Research Institute, New Delhi, as early as 1943 (Pal and Singh 1946). Evidence of heterotic effects is supported by genetic analyses that have defined the presence of dominance and complementary gene action for yield in bitter gourd (Mishra et al. 1998). Heterosis for yield per vine
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ranges from 27% to 86% depending on genotype (Behera 2004). This heterosic effect is likely attributable to earliness, first node to bare fruit (first pistillate flowering node), and total increased fruit number (Celine and Sirohi 1998). Several hybrids developed by private and public sectors breeding efforts are cultivated in Asia, including China and India. Techniques used for hybrid development in bitter gourd are similar to those of melons and cucumber (Behera 2004). Even though it is essential to employ inbred lines to achieve hybrid uniformity, the degree of inbreeding required depends on the extent of uniformity that is desired in the resulting hybrid. In bitter gourd, vigorous parental inbreds routinely are maintained by selfing without inbreeding depression (Behera 2004). However, since selfing in later stages of plant development often results in poor fruit set, only the first 1 or 2 pistillate flowers are customarily self-pollinated. In some instances, it may be deemed unnecessary to produce highly inbred lines since “homozygous” genoptypes can be obtained from relatively homogeneous populations (i.e., uniform for morphological characters) and used directly as parents, as is the case for some self-pollinated crops such as tomato, eggplant, and sweet pepper (Swarup 1991). Under circumstances where highly inbred lines are needed for hybrid production, rigorous selection is applied over several selfing generations. These inbred lines then typically are tested for their combining ability through structured single crosses (e.g., North Carolina I or II mating design) and/or diallel analyses. Based on their general and specific combining ability, the most promising lines are chosen for F1 hybrid production. 2. Mutation Breeding. Bitter gourd progeny (M1) derived from radiation mutagenesis can possess economically important unique characters that are controlled by single recessive genes (Miniraj et al. 1993). One such bitter gourd cultivar, MDU 1, developed as a result of gamma radiation (seed treatment) of the landrace cultivar MC 103, was found to possess improved yield (Rajasekharan and Shanmugavelu 1984). Likewise, the white bitter gourd mutant Pusa Do Mausami (whitefruited type) was developed through spontaneous mutation from the natural population Pusa Do Mausmi (green-fruited type) at the Indian Agriculture Research Institute. 3. Testing. Testing of experimental bitter gourd cultivars and hybrids varies dramatically from country to country. In India, potentially important bitter gourd germplasm (e.g., improved landraces) and hybrids are evaluated in multi-location trials by cooperating public and private
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sector breeders [e.g., All India Coordinated Research Project (AICRP)]. This is typically performed in 3-year, large-scale yield and quality evaluations where entries are evaluated for economically important characters. In the first year, germplasms are tested in eight diverse geographical locations for initial evaluation in replicated (three to four) trials. The best varieties and hybrids are evaluated a second year at the same locations under the same experimental conditions. Then, in the third year, the best cultivars and hybrids are reexamined, and comprehensive information (three years) leads to recommendations for release of exceptional germplasm in the fourth year. F. Biotechnology The diverse morphological characters such as sex expression, growth habit, maturity, and fruit shape, size, color, and surface texture (Robinson and Decker-Walters, 1997) of M. charantia in India provide for relatively broad phenotypic species variation. Although DNA marker analysis can assist in diversity analyses (Behera et al. 2008a,c), only a few polymorphic markers have been identified in bitter gourd (Dey et al. 2006a; Singh et al. 2007; Gaikwad et al. 2008). The genome size of M. charantia is 2.05 pg per haploid nucleus, which is similar to tomato but 10 times that of Arabidopsis (Ingle et al. 1975). The few genes of Momordica that have been isolated include MAP 30, trypsin inhibitor, chitinase, and napin, and a seed storage protein (Lee et al. 1995; Vashishta et al. 2006; Xiao et al. 2007). MAP30 (30 kDa Momordica protein) was isolated and cloned to evaluate its antitumor property (Sun et al. 2001) and inhibition HIV-1 infection and replication (Lee et al. 1995). More recently, napin and chitinase, which impart fungal resistance, were cloned from bitter gourd plants (Vashishta et al. 2006; Xiao et al. 2007). In vitro regeneration of M. dioica and M. grosvenori has met with only a modicum of success. Nevertheless, regeneration from nodal explants of M. charantia has been achieved (Agarwal and Kamal 2004). Regeneration from cotyledons is unpredictable but is more practical than regeneration from either internodes or shoot tip explants. In vitro shoot multiplication of bitter gourd has been achieved and is now suggested for in vitro production of secondary metabolites (Agarwal and Kamal 2004).
V. CONCLUSIONS Bitter gourd is an important vegetable crop of several countries in the tropics. Bitter gourd fruit contain bioactive components with many
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important medicinal properties (Horax et al. 2005). Due to unavailability of improved cultivars, most of the species’ genetic development and cultivation has been the result of selection within landraces by farmers in local habitats. However, over the last two decades, increasing emphasis has been placed on more systematic bitter gourd improvement strategies in India and China. In India, this has resulted in the release of a number of improved open-pollinated cultivars and hybrids by state agricultural universities, the Indian Council of Agricultural Research, and private seed companies. A few cultivars and hybrids have also been released in China that are resistant to biotic stresses. Future breeding and genetic emphases in bitter gourd improvement should be placed on the development of nutritious, high-yielding cultivars with superior resistance to major diseases and exceptional fruit quality for both domestic and foreign markets. These efforts should focus on breeding for season and regional adaptation. LITERATURE CITED Agarwal, M., and R. Kamal. 2004. Studies on steroid production using in vitro cultures of Momordica charantia. J. Med. Arom. Plant Sci. 26:318–323. Ahmed, I., E. Adeghate, E. Cummings, A.K. Sharma, and J. Singh. 2004. Beneficial effects and mechanism of action of M. charantia juice in the treatment of streptozotocininduced diabetes mellitus in rat. Mol. Cell Biochem. 261:63–70. Ahmed, I., E. Adeghate, A.K. Sharma, D.J. Pallot, and J. Singh. 1998. Effects of Momordica charantia fruit juice on islet morphology in the pancreas of the streptozotocin diabetic rat. Diabetes Res. Clin. Pract. 40:145–151. Ahmed, I., M.S. Lakhani, M. Gillet, A. John, and H. Raza. 2001. Hypotriglyceridemic and hypocholesterolemic effects of anti-diabetic M charantia fruit extract in streptozotocininduced diabetic rats. Diabetic Res. Clin. Pract. 51:151–166. Baldwa, V.S., C.M. Bhandari. A. Pangaria, and R.K. Goyal. 1977. Clinical trials in patients with diabetes mellitus on an insulin-like compound obtained from plant source. Upsala J. Med. Sci. 82:39–41. Balentine, D.A., S.A. Wiseman, and L.C.M. Bouwens. 1997. The chemistry of tea flavonoids. Crit. Rev. Food Sci. Nutr. 37:693–704. Basch, E., S. Gabardi, and C. Ulbricht. 2003. Bitter melon (Momordica charantia): A review of efficacy and safety. Am. J. Health-System Pharm. 60:356–359. Baynes, J.W. 1995. Mechanistic approach to diabetes. Vol. 2. Ellis Horwood Limited, Chichester, UK. pp. 203–231. Behera, T.K. 2004. Heterosis in bitter gourd. pp. 217–221. In: P.K. Singh, S.K. Dasgupta, and S.K. Tripathi (eds.), Hybrid vegetable development. Haworth Press, New York. Behera, T.K., S.S. Dey, and P.S. Sirohi. 2006. DBGy-201 and DBGy-202: Two gynoecious lines in bitter gourd (Momordica charantia L.) isolated from indigenous source. Indian J. Genet. 66:61–62. Behera, T.K., A.B. Gaikward, A.K. Singh, and J.E. Staub. 2008a. Relative efficiency of DNA markers (RAPD, ISSR and AFLP) in detecting genetic diversity of bitter gourd (Momordica charantia L.). J. Sci. Food Agr. 88:733–737.
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Devadas, V.S., and S. Ramadas. 1993. Report of a seedling marker character in bitter gourd (Momordica charantia Linn.). South Indian Hort. 41:174–175. Devadas, V.S., and S. Ramadas. 1994. Genetic analysis of bitter principals in Momordica charantia Linn. Cucurbit Genet. Coop. Rep. 17:129–131. Dey, S.S., T.K. Behera, Anand Pal, and A.D. Munshi. 2005. Correlation and path coefficient analysis in bitter gourd (Momordica charantia L.). Veg. Sci. 32:173–176. Dey, S.S., T.K. Behera, and Charanjeet Kaur. 2006b. Genetic variability in ascorbic acid and carotenoids content in Indian bitter gourd (Momordica charantia L.). Cucurbit Genet. Coop. Rep. 28–29:91–93. Dey S.S., A.K. Singh, D. Chandel, and T.K. Behera. 2006a. Genetic diversity of bitter gourd (Momordica charantia L.) genotypes revealed by RAPD markers and agronomic traits. Sci.Hortic. 109:21–28. De Wilde, W.J. J. O., and B.E.E. Duyfjes. 2002. Synopsis of Momordica (Cucurbitaceae) in SE-Asia and Malaysia. Bot. Zhurn. 87:132–148. Dhillon, M.K., R. Singh, J.S. Naresh, and N.K. Sharma. 2005. Influence of physico-chemical traits of bitter gourd, Momordica charantia L. on larval density and resistance to melon fruit fly, Bactrocera cucurbitae (Coquillett). J. Appl. Entomol. 129:393–399. Dixit, V.P., P. Khanna, and S.K. Bhargava. 1978. Effects of Momordica charantia fruit extract on the testicular function of dog. Planta Med. 34:280–286. Dutta, P.K., A.K. Chakravarty, U.S. Chowdhury, and S.C. Pakrash. 1981. Vicine, a Favism-inducing toxin from Momordica charantia Linn seeds. Indian J. Chem. 208:669–671. Fan, Z., M.D. Robbins, and J.E. Staub. 2006. Population development by phenotypic selection with subsequent marker-assisted selection for line extraction in cucumber (Cucumis sativus L.). Theor. Appl. Genet. 112:843–855. Feng, Z., W.W. Li, H.W. Yeung, S.Z. Chen, Y.P. Wang, X.Y. Lin, Y.C. Dong, and J.H. Wang. 1990. Crystals of a-momorcharin: A new ribosome-inactivating protein. J. Mol. Biol. 214:625–626. Gaikwad, A.B., T.K. Behera, A.K. Singh, D. Chandel, J.L. Karihaloo, and J.E. Staub. 2008. AFLP analysis provides strategies for improvement of bitter gourd (Momordica charantia L.). HortScience 43:127–133. Ghosh, S., and P.S. Basu. 1982. Effect of some growth regulators on sex expression of Momordica charantia. Sci. Hortic. 17:107–112. Ghosh, S., and P.S. Basu. 1983. Hormonal regulation of sex expression in Momordica charantia. Physiologia Plantarum 57:301–305. Gopalan C., B.V. Rama Sastri, and S.C. Balalsubramanian. 1993. Nutritive value of Indian foods, 2nd ed. Hyderabad: National Institute of Nutrition, ICMR. Gorinstein, S., O. Martin-Belloso, A. Lojek, M. Ciz, R. Soliva-Fortuny, Y.S. Park, A. Caspi, I. Libman, and S. Trakhtenberg. 2002. Comparative content of some phytochemicals in Spanish apples, peaches and pears. J. Sci. Food Agr. 82:1166–1170. Grover, J.K., S.S. Rathi, and V. Vats. 2002. Amelioration of experimental diabetic neuropathy and gastropathy in rats following oral administration of plant (Momordica charantia, Eugenia jambolana, Mucuna pruriens and Tinospora cordifolia) extracts. Indian J. Expt. Biol. 40:273–276. Grover, J.K., V. Vats, S.S. Rathi, and S. Dawar. 2001. Traditional Indian anti-diabetic plants attenuate progression of renal damage in streptozotocin induced diabetic mice. J. Ethnopharmacol. 76:233–238. Grover, J.K., and S.P. Yadav. 2004. Pharmacological actions and potential uses of Momordica charantia: A review. J. Ethnopharmacol. 93:123–132.
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3 Dynamics of Carbohydrate Reserves in Cultivated Grapevines Bruno P. Holzapfel, Jason P. Smith, Stewart K. Field, and W. James Hardie National Wine and Grape Industry Centre Charles Sturt University Locked Bag 588 Wagga Wagga, New South Wales, 2678 Australia I. INTRODUCTION II. CARBOHYDRATE RESERVES A. Adaptive Advantages 1. Deciduousness 2. Seasonal Contingencies B. Biochemical Composition and Measurement 1. Carbohydrate Composition 2. Measurement of Carbohydrate Reserves III. ACCUMULATION OF CARBOHYDRATE RESERVES A. Dynamic Capacitance Model B. Carbohydrate Content within Grapevine Organs 1. Spatial and Temporal Variation in Carbohydrate Reserves 2. Seasonal Dynamics of Carbohydrate Reserve Concentration in Perennial Organs C. Environmental Influences on Carbohydrate Reserve Concentration D. Influence of Fruiting on Carbohydrate Reserve Concentration IV. PHOTOASSIMILATION AND STORAGE PROCESSES A. Sucrose and Starch Formation in Leaves B. Distribution of Sucrose from Leaves C. Genetic, Phenological, and Environmental Influences on Photoassimilation and Carbohydrate Accumulation 1. Genetic Influences 2. Phenological Influences 3. Environmental Influences V. MOBILIZATION AND UTILIZATION OF CARBOHYDRATE RESERVES A. Daily Metabolism B. Seasonal Growth and Development Horticultural Reviews, Volume 37 Edited by Jules Janick Copyright 2010 Wiley-Blackwell. 143
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1. Seasonal Reestablishment 2. Triggers for Mobilization of Reserves C. Carbohydrates from Perennial Reserves 1. Mobilization and Distribution 2. Recommencement of Growth D. Growth and Development of Perennial Organs 1. Predormancy 2. Postdormancy E. Grapevine Defense and Repair 1. Resistance and Tolerance to Environmental Stress 2. Resistance and Tolerance to Biotic Stresses F. Parasitism of Perennial Carbohydrate Reserve-Bearing Organs 1. Fungi 2. Phylloxera 3. Nematodes VI. VITICULTURAL MANAGEMENT OF CARBOHYDRATE RESERVES A. Impact of Viticultural Practices on Carbohydrate Assimilation, Utilization, and Net Reserves 1. Pruning and Fruit Bearing 2. Defruiting (Bunch Thinning) 3. Root Pruning 4. Cane and Trunk Girdling 5. Gibberellic Acid Application 6. Partial Leaf Removal 7. Harvest Pruning Dried and Wine Cultivars 8. Irrigation 9. Fertilization 10. Shoot Removal 11. Shoot Trimming B. Grapevine Balance VII. SUMMARY AND CONCLUSIONS LITERATURE CITED
I. INTRODUCTION For perhaps as many as 10,000 years, viticulturists have progressively learned to direct the inherent growth potential of the grapevine, Vitis spp., to reliably bear grapes with compositional attributes that meet human needs. As with other perennial plants in particular, carbohydrates, elaborated by photosynthetic tissues—principally leaves, but also stems and fruit—synthesized, distributed, and deposited in tissues throughout the plant, provide both the energetic and structural resources for growth, development, and survival of this normally deciduous genus. Viticulture most essentially involves the seasonal nurture and redirection of those carbohydrate resources. Practices with ancient origins such as trellising, annual pruning, trunk and stem girdling, fruit thinning, shoot topping,
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shoot thinning, root pruning, fertilization, and indeed the vegetative propagation of cultivated varieties, together with more recent refinements, such as the application of growth regulators and deficit irrigation practices, may all be viewed in this light. The recent introduction of quality management principles of manufacturing into viticultural and other biological production systems, together with rapidly rising atmospheric carbon dioxide levels, has become a powerful driver of the need to better understand the fundamentals of carbohydrate partitioning and storage within the grapevine as a primary base for improved prediction of responses to viticultural practices and environmental changes. However, within the broad physiology of carbon relations, the storage and utilization of carbohydrate reserves warrants specific attention because of the vital roles it plays in survival and successful cultivation. For grapevines, as for many other plant species, ecological resilience depends on carbohydrate reserves on which the plant may draw to meet seasonal contingencies, such as responses to pests and diseases and to environmental stresses. But of even more fundamental significance for deciduous species like Vitis, the annual reestablishment of growth and reproductive capacity depends entirely on carbohydrate reserves. In other words, carbohydrate reserves are both vital outputs of the grapevine carbon economy and inputs to it; as such, they are integral to seasonal performance. Attempts up to now to characterize the integrated responses of grapevines to cultural manipulation and growth conditions with carbonbased growth models, for example, VineLOGIC (White et al. 2002) and VitiSim (Lasko and Poni, 2005), are limited by lack of information, particularly in regard to the contribution of carbohydrate reserves— most notably those held within the root system—and regulation of their mobilization. A general outline of within-season changes in availability of carbohydrate reserves, in terms of their concentration in vegetative parts of grapevines, was provided by Winkler et al. (1974) based on responses in nonstructural carbohydrate to pruning and fruit thinning treatments in studies conducted between 1921 and 1928 (Winkler 1926, 1929, 1931) and carbohydrate analyses of field-grown grapevines (Winkler and Williams 1938, 1945). A notable limitation of the reports of those studies is the lack of measures of carbohydrate stores on a per organ basis, thus precluding assessment of quantitative responses and biosynthetic capacity. More recent reviews of the role and dynamics of grapevine carbohydrate reserves are confined to small sections in the text of Mullins et al. (1992) and within a comprehensive review of grapevine carbon relations by Williams (1996).
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Since 1996 there have been over 80 peer-reviewed publications specifically related to carbohydrate metabolism in grapevines. Most deal with aspects of the overall carbon status of grapevines—assimilation and dry weight accumulation—many in specific cultivated conditions. Few deal specifically with carbohydrate reserves and their dynamics as they relate to seasonal growth and responses to management, but nevertheless, those publications have made important incremental steps in the progress of knowledge of this fundamental aspect of grapevine physiology. Most of the findings reviewed here concern cultivars of Vitis vinifera but some concern cultivars of V. labruscana such as ‘Concord’, V. riparia, Muscadinia, and other interspecific hybrids. The chapter focuses on the seasonal cycle of grapevine carbohydrate reserves and the key physiological functions and viticultural practices that influence seasonal carbon assimilation and utilization and determine reserve status at salient stages in that cycle. In turn, we examine the impact of these reserves on reproductive development in regard to fruit yield and ripening. Also considered is the significance of roots and aboveground organs both as metabolic sinks and sources during the seasonal course of grapevine development and during environmental stress. We introduce the concept of stored carbohydrates performing a capacitorlike role in buffering imbalances in supply and demand of photoassimilates and consider how this relates to the viticultural concept of vine balance. In the course of the chapter, being cognizant that viticulture worldwide faces rising atmospheric carbon dioxide levels and climatic changes that will demand change in vineyard management practices, we identify aspects of grapevine carbohydrate relations that are likely to respond to such changes and aspects that cannot be forecast with current knowledge. In presenting this review, we are mindful that other classes of stored compounds, particularly organic acids and amino acids, play important roles in the seasonal cycle of this species. However, by placing carbohydrate reserves at the focal point of the complex network of biophysico-chemico interactions that determine plant carbon relations, we hope to draw particular attention to a physiological state of grapevines that has important vegetative and reproductive impacts that are not generally well appreciated— impacts that appear central to contemporary viticulture, namely stable and predictable production of a fruit with appealing sensory attributes. II. CARBOHYDRATE RESERVES A. Adaptive Advantages The cultivated grapevine is a deciduous, woody, liana generally adapted to warm, temperate climates (Mullins et al. 1992). The capacity of plants
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to store a portion of photoassimilate as carbohydrate reserves appears as an adaptation that supports survival in otherwise adverse abiotic and biotic environmental conditions, including cold, short-day, winter conditions that occur with seasonal regularity and those that may occur as contingencies from time to time. Deciduousness, which relies on the capacity to store carbohydrates from one season to the next, is a clear example of a seasonally driven imperative. The uses of stored carbohydrates to effect refoliation following extreme herbivory or severe drought stress are examples of adaptation to contingencies. Whereas trees and shrubs store much of their reserves of water, carbohydrates, and nutrients in stems, vines that are support-dependent plant forms have much less stem-to-leaf mass than do self-supporting plants (Mooney and Gartner 1991). In horticulture, this feature distinguishes grapevines from woody, fruit-bearing trees and shrubs. Carbon that in those woody forms contributes to substantial structural support may be utilized by vines for leaf development, thus compounding their growth potential (Monsi and Murata 1970). The potential for rapid growth is a feature of particular importance to grapevine species that, in their natural habitat, must annually consolidate favorable positions in foliar canopies of their—often also deciduous—tree hosts. Along with total canopy redevelopment required by deciduousness, this feature relies on carbohydrate reserves, but lack of structural strength may render stem tissue, and carbohydrates stored within it, relatively more vulnerable to physical damage (Fisher and Ewers 1991). Although grapevine stems typically contain significant nonstructural carbohydrates, the relatively higher root stores and their contribution to seasonal reestablishment of Vitis seem to reflect that vulnerability. The underground tuber-forming capacity of other members of the Vitaceae may represent a more specialized level of similar adaptation. 1. Deciduousness. This condition is considered to have first evolved in angiosperms at mid-latitudes marginal to the tropical zone during the early Cretaceous as an adaptation to moderate drought in the cooler part of the year (Axelrod 1966). The genera of the Vitaceae are thought to have evolved from an Asian Cissus-like progenitor (Lavie 1970). As all angiosperms arose in the tropics, deciduousness in Vitis was possibly acquired from deciduous progenitors, for example, the closely related Ampelocissus adapted to the dry winters associated with tropical monsoonal conditions. Deciduousness is an adaptation that relies on the accumulation of carbohydrates during favorable seasonal conditions to sustain plants through unfavorable winter conditions and provide for their regrowth in spring. Stored carbohydrate reserves from one season support
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reestablishment of photoassimilatory capacity and resumption of reproductive capacity in the next (Scholefield et al. 1978; Conradie 1980, 1986; Huglin and Schneider 1998). Deciduousness has been regarded commonly as a protection against an imbalance in respiratory carbon loss and photoassimilation during light-limiting, winter conditions at high latitudes. However, more recent studies discount that view (see Beerling 2007 and references therein). It is now suggested that deciduousness and associated dormancy may be an adaptation to avoid growth and transpiration during periods in which, at high latitudes, the heavier soils to which deciduous species are generally adapted or confined are more easily frozen and thereby preclude nutrient and water uptake (Givnish 2002). According to this view, as well as being an adaptation against low winter rainfall, deciduousness and dormancy also protect plants against frost drought, nutrient stress, and, possibly, anaerobiosis immediately accompanying the winter thaw. Features of grapevine carbohydrate regulation and phenology that accord with this view will be discussed in following sections. 2. Seasonal Contingencies. In addition to meeting the demand for carbohydrate to achieve the seasonal reestablishment integral to a deciduous existence, carbohydrate stores in various tissues play an important role in sustaining grapevine functions during other periods when internal demand exceeds supply from current photoassimilation. Common causes of such deficits include defoliation and suboptimal photosynthetic conditions. Grapevines do not generally become independent of overwinter carbohydrate reserves until around flowering (anthesis) in late spring to early summer, and reserves may offset carbohydrate stress-induced impairment of pollination, fertilization, and fruit set (Winkler 1929) under weather conditions adverse to photoassimilation (Zapata et al. 2004). Grapevines may also utilize carbohydrate reserves during winter for defense from cold injury and more generally for maintenance and nighttime metabolic functions. Other plant functions that may rely on carbohydrate reserves from time to time include defense against fungi, herbivores, and other plants; replacement of damaged tissue; and fruit ripening. B. Biochemical Composition and Measurement 1. Carbohydrate Composition. In grapevines, the greatest proportion (i.e., ca. 80%) of total seasonally assimilated carbon is allocated to structural compounds including hemicelluloses and cellulose (Winkler
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and Williams 1938). Deciduousness and the capacity to surmount seasonal contingencies involve accumulation of the balance of assimilated carbon as nonstructural carbohydrate reserves. Those reserves are regarded herein as the total amount of starch and soluble sugars present in the perennial vegetative organs. Starch is usually the predominant reserve form with sucrose, glucose, fructose, and raffinose—which is generally present only in cooler winter months (Koussa et al. 1998)— comprising the majority of the sugars (Jones et al. 1999). Other soluble carbohydrates including stachyose (Hamman et al. 1996), maltose and melibiose (Panczel 1962), and galactose (Koussa et al. 1998) have been reported. Typical amounts of starch and sugar reserves during dormancy are shown in Table 3.1. The fruit of the grapevine is rich in glucose and fructose and has small amounts of sucrose and starch (Amerine and Root 1960), but there is no evidence of their redistribution to other parts of the plant. In deciduous species, leaves are both diurnally and seasonally transient sources of carbohydrates, the levels of which vary according to photoassimilation rate and the rate of distribution to other organs. At most, leaves hold less than 0.4% dry weight (DW) of the total nonstructural carbohydrate reserves of the grapevine (Mullins et al. 1992). In grapevine stems, starch is stored in plastids within live cells of the cortex, phloem sieve tubes, phloem and xylem parenchyma and rays (Esau 1948; Goffinet 2004; Zapata et al. 2004) (Fig. 3.1). Starch occurs also in the cambial ray initials but only during dormancy (Esau 1948). In grapevine roots, starch is stored in both phloem and xylem ray parenchyma cells during dormancy. In those tissues, starch is most abundant during dormancy and becomes depleted, most notably from phloemcells, after budbreak(Zapataetal. 2004; Smith andHolzapfel2005) (Fig. 3.1). Starch stored within bud tissues during dormancy contributes to cold hardiness (Jones et al. 1999) and provides for initial bud growth before reactivation of phloem in early spring (Esau 1948). 2. Measurement of Carbohydrate Reserves. The three grapevine carbohydrate reserve moieties, starch, sucrose, and its hydrolysis products, glucose and fructose, are considered mutually interconvertible, and data relating to their aggregation are generally expressed in terms of glucose equivalents to provide a common basis for comparisons. Although A. J. Winkler and W. O. Williams, early investigators of carbohydrates in grapevines, argued for the expression of data “for mature plant tissue” on a residual (i.e., starch and sugar free) dry weight basis, as a more accurate measure than a total dry weight, “at least for changes occurring within a
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Fig. 3.1. Location of grapevine carbohydrate reserves. Starch granules (stained dark). Cane (lignified shoot) (a) and root tissue (b) at leaf fall. Tangential section of root tissue 40 (c), ‘Chardonnay’. Source: Photos by J.P. Smith.
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given tissue,” many subsequent researchers have adopted total dry weight as a suitable basis, at least for comparative purposes. However, measures on a dry weight basis are essentially expressions of concentration, and changes are difficult to interpret if unaccompanied by the residual dry weight changes over the measurement period. In woody grapevine tissues, total dry weight does change during seasonal development, if less so in more than 2-year-old wood (Weyand and Schultz 2006), and almost certainly residual dry weight does also, although there is little information distinguishing this component. Winkler and Williams (1945) describe appropriate choices of index for presentation of carbohydrate-related data. As mentioned earlier, the paucity of data on a per organ basis remains a serious limitation to interpretation of carbohydrate dynamics in grapevines. Analysis of nonstructural carbohydrates of grapevines is achieved by well-established methods and is relatively straightforward. Sugar Determination. Soluble sugars, mostly comprising glucose, fructose, and sucrose, are generally extracted from milled plant material with 70% to 80% aqueous combinations of ethanol, methanol, sometimes with addition of chloroform. Following extraction, soluble sugars may be determined using either colorimetry or high-pressure liquid chromatography or by gas chromatography. The colorimetric anthrone method (Hodge and Hofreiter 1962), along with a glucose standard, is commonly used, allowing expression of carbohydrate concentration in glucose equivalents. Soluble sugars may also be colorimetrically determined following phosphorylation and enzymatic formation of nicotinamideadenine dinucleotide phosphate (Sommer and Clingeleffer 1996). Sucrose concentration may be determined by enzymatic hydrolysis with b-fructosidase (invertase) and calculation of the difference in glucose before and after hydrolysis. Glucose, fructose, and sucrose may also be determined using highpressure liquid chromatography with appropriate columns and a refractive index or evaporative light-scattering detector (Clement et al. 1992). Those sugars may also be determined by gas chromatography with appropriate columns and a flame-ionization detector, after derivatization with a silylating reagent such as bis(trimethylsilyl)trifluorocetamide (Kiefer and Herwehe 1996). Starch Determination. Starch concentration is usually determined after the soluble sugars have been removed. It may be measured directly by colorimeter at 610 nm after reaction with acidic iodine solution (Zapata et al. 2004). Otherwise, starch may also be solubilized
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with dimethyl sulphoxide. Thereafter, component glucose molecules, released by enzymatic digestion with a-amylase or amylglucosidase, may be determined colorimetrically after conversion with glucose 6-phosphate dehydrogenase or glucose oxidase or by high-performance liquid chromatography, as for other soluble sugars. Amylase may also be used to digest starch into glucose, which may then be metabolized enzymatically to produce hydrogen peroxide in equivalent amounts determined by biochemical analysis (Lee et al. 1995). The rapid determination of starch as used for cereal crops utilizing near-infrared transmitting spectroscopy (Shimizu et al. 1999) might also be applied to determine grapevine carbohydrate reserve status in routine viticultural practice. Sap Analysis. Analysis of xylem sap from perennial plant organs is used as an indicator of the utilization of carbohydrate reserves (Campbell and Strother 1996). The sap, obtained from flows generated by natural or applied root pressure, is assumed to be free of phloem contents either because of occlusion of sieve elements by callose (in the early stages of postdormancy) or by phloem-specific, that is, ‘P’ protein, which rapidly follows wounding, at subsequent stages. III. ACCUMULATION OF CARBOHYDRATE RESERVES A. Dynamic Capacitance Model The spatial and temporal quantum of carbohydrate reserves in the various parts of grapevines may be conceptualized as a single, temporally variable buffer against seasonal environmental stresses in which the total available reserves at any point in time are determined by the difference in rate of accumulation and the rate of mobilization of carbohydrates (Fig. 3.2). According to this model, the carbohydrate reserve content of grapevines is thus determined by internal requirements for growth and development, by climatic conditions and soil resources in the form of water and nutrients, and by viticultural practices that impact on assimilatory capacity and perturb natural processes of carbohydrate distribution and utilization. Most, if not all, current carbon-based models of grapevine growth and development—for examples, see Gutierrez et al. (1985); Williams et al. (1985a,b); Wermelinger et al. (1991); Bindi et al. (1996, 1997a,b); Lakso et al. (2001); Vivin et al. (2002, 2003); Schultz (2003); Schultz and Lebon (2005)—that seek to account for carbon assimilation and partitioning, at either holistic or fundamental levels of biochemical
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Viticultural Intervention ASSIMILATION
UTILIZATION
Photosynthesis
Translocation
Metabolism
CARBOHYDRATE ACCUMULATION
Seasonal Reestablishment and Growth - Fruit - Shoots - Perennial organs
Mobilization
Seasonally dynamic
Seasonal Contingencies - Defense - Repair
Environment Fig. 3.2.
Dynamic capacitance model of grapevine carbohydrate reserves.
and physiological process, do not accommodate the central role of a seasonally fluctuating pool of carbohydrate reserves nor the impacts of environment and viticultural interventions on it. Thus, for dry weight accumulation, these models generally do not distinguish between carbon held as reserves and that contributing to grapevine structure. Nor do they currently account separately for stored and current photoassimilates that often are utilized concurrently for metabolism and growth (Kozlowski 1992). The ability to account for the capacity (or lack of capacity) of reserves to buffer seasonal contingencies and to account for the seasonal requirements for restoration of reserves seems vital for any practical, viticultural utility of models of grapevine carbon relations. In terms of having viticultural utility and representing physiological balance and grapevine performance from season to season within particular environmental settings (see Section VI.B), we favor a model in which carbohydrate reserves, because of their unique role in seasonal regeneration of photoassimilatory capacity and floral development, occupy a central position. Our dynamic capacitance model, although currently conceptual, has been conceived from that perspective and represents the organizational framework adopted for this chapter. In the following sections we examine the key carbohydrate inputs and outputs and viticultural practices that determine the level of reserves at a
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given time in the seasonal cycle. In view of the relatively small starch content of leaves at any point in time, for simplicity, we regard that component as a source of the carbohydrate held in the perennial organs (viz. roots, trunk, and shoots) rather than a significant reserve in its own right; we recognize, however, that, over time, the contribution from leaves to perennial organs (whether direct or from starch stores) is axiomatic and that leaves also supply nonstorage functions. B. Carbohydrate Content within Grapevine Organs The general seasonal course of growth of grapevines and component organs, on a dry biomass basis, is shown in Fig. 3.3. During the course of the seasonal growth cycle, carbohydrate reserves vary in amount and composition within and between organs (Mullins et al. 1992; Sommer and Clingeleffer 1996) and with perturbations caused by physical and biotic environmental events and viticultural interventions. 1. Spatial and Temporal Variation in Carbohydrate Reserves. The literature contains surprisingly little data concerning the absolute content of nonstructural carbohydrates at key points in the seasonal cycle of field-grown grapevines. Winkler (1929) reported that after normal spur pruning of ‘Monukka’, the weight of nonstructural carbohydrates 8000 Permanent Leaf Stem Bunch
Dry Weight (g vine–1)
6000
4000
2000
0 BB Sep
A Nov
V Jan
M Mar
LF May
Fig. 3.3. The seasonal course of growth (dry biomass) of grapevines and component organs (‘Shiraz’ on own roots, 10 years old). The times of budbreak (BB), anthesis (A), veraison (V), maturity (M), and leaf fall (LF) are indicated. Source: S.K. Field et al. unpublished data.
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remaining was 0.82 kg/vine compared to 2.78 kg/vine for nonpruned vines. This compares closely to 0.80 kg/vine for spur-pruned ‘Chenin Blanc’ (Mullins et al. 1992). It may be safely determined from these and other reports (e.g., R€ uhl and Clingeleffer 1993; Sommer and Clingeleffer 1996) that peak, aggregate contents of nonstructural carbohydrates in roots, trunk, and cordons (i.e., the perennial or “permanent” parts of cultivated grapevines) generally occur between fruit maturity and leaf fall and are in the order of 0.5 to 2.2 kg per vine. By inference, carbohydrate reserves not utilized for growth during autumn are retained through dormancy (Winkler and Williams 1945), albeit with some small respiratory losses (Winkler and Williams 1945) and possibly with some conversion to nitrogenous metabolites in roots prior to recommencement of growth during spring (Yang and Hori 1979). Typical carbohydrate reserve contents during dormancy from a number of field studies in a range of viticultural conditions are presented in Table 3.1. At dormancy, grapevine roots and trunks typically have the greatest contents of total carbohydrate reserves, but data presented in Table 3.1 indicate that the relative proportion in roots at that time ranges widely, from 18% to 75%. However, root reserve content may be underestimated in some cases due to the difficulty in excavating entire root systems. Yang and Hori (1979), working with potted grapevines, found that the Table 3.1. Grapevine carbohydrate reserves (grams dry weight per organ) during dormancy in a number of field studies under different climatic conditions. Trunkz
Roots Cultivar Shirazy Cabernet Francx Cabernet Francw Chenin Blancv Pinot Noiru z
Vine
Age Sugars Starch Total Sugars Starch Total Sugars Starch Total 10 15 15 10 14
56 91 93 19 25
771 473 311 322 314
828 564 404 341 338
111 278 425 46 18
173 1114 1367 409 163
284 1392 1793 455 181
167 369 518 65 43
944 1587 1678 731 477
1111 1956 2196 796 519
Including all other part of the aerial perennial structure. Single cordon, spur pruned, spacing 3 m 2.0 m, own roots, irrigated (S.K. Field et al. unpublished). x Single cordon, spur pruned, spacing 3 m 2.4 m, own roots, irrigated (R€ uhl and Clingeleffer 1993). w Single cordon, minimal pruned, spacing 3 m 2.4 m, own roots, irrigated (R€ uhl and Clingeleffer 1993). v Single cordon, spur pruned, spacing 2.4 m 2.4 m, own roots, irrigated (Mullins et al. 1992). u Single cordon, spur pruned, spacing 3 m 1.5 m, 99 Richter, irrigated 5 years prior (Hunter 1998). y
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roots acquired a greater proportion of radiolabeled summer and autumn photoassimilates (as soluble carbohydrates) than trunks or canes. Clingeleffer and R€ uhl (1993), after mechanically excavating mature, fieldgrown vines, found 18% of accumulated nonstructural carbohydrates in roots of minimal pruned vines. Lowest contents of carbohydrate reserves occur after reserves have been utilized for seasonal reestablishment but before seasonal carbon balance becomes positive. Depending on conditions, they may occur any time from several weeks after budbreak to several weeks after anthesis. Aggregate reserve contents of less than 1.0 kg per vine may be expected within that period. Data presented by Mullins et al. (1992) shows that by 2 weeks after anthesis, the aggregate carbohydrate reserve content of the perennial parts was restored to that at budbreak. 2. Seasonal Dynamics of Carbohydrate Reserve Concentration in Perennial Organs. Grapevine roots, trunks, and canes are the major storage organs, and contain the highest concentrations, on a dry weight basis, of nonstructural carbohydrates. In this section, we generalize the seasonal course of the concentration of carbohydrate reserves from the findings of several studies, albeit with different grapevine cultivars. Allowing for some interpretation, made necessary by differences in sampling (i.e., by either phenological event or calendar date), general seasonal patterns are evident. Roots and Trunks. Typical seasonal dynamics of carbohydrate reserve concentrations in grapevine roots and trunks are shown in Fig. 3.4. The figure has been compiled from three different studies (Winkler and Williams 1945; Williams 1996; and Bennett et al. 2005) that provide mostly complete courses of seasonal values for both roots and trunks. In both organs, the relative contributions of starch and sugars to the total carbohydrate reserve concentration vary greatly during the season, due mainly to large changes in starch concentration which at times may exceed that of soluble sugars by as much as 15-fold and at other times may be similar. For additional data concerning carbohydrate reserve concentrations in grapevine roots and trunks, see Weaver and McCune (1960); Eifert et al. (1961); Scholefield et al. (1978); Korkas (1994); Hamman et al. (1996); Bates et al. (2002); Zapata et al. (2004); and Weyand and Schultz (2006). The total concentration of nonstructural carbohydrates in grapevine roots typically declines from ca. 22% to 25% DW at budbreak to minimal levels, ca. 5% to 16% DW at or after anthesis. After anthesis, the total concentration rises but commencement of the rise varies considerably
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES
Roots A
157
Trunk M LF
A
M LF
50
Starch (%DW)
40 30 20 10 0 25
Sugar (%DW)
20 15 10 5 0
Total CHO (%DW)
50 40 30 20 10 0 –100
0
100
200
300
Days after budbreak
–100
0
100
200
300
Days after budbreak
Fig. 3.4. Seasonal carbohydrate reserve concentration dynamics in perennial root and trunk tissueofseveralgrapevinecultivars.*, ;‘Carignane’,4-year-old,fromWinklerandWilliams (1945). Carbohydrate concentrations originally expressed on a residual dry weight basis have been recalculated on a total DW basis for this comparison. Root carbohydrate concentration is the average of 2-year and older root sections. Trunk carbohydrate concentration is the average of separate data for bark (phloem) and wood (xylem) tissue. &, &; ‘Thompson Seedless’, 5-year-old, from Williams (1996). ~, ~; ‘Chardonnay’, 10-year-old, from Bennett et al. (2005). The times of anthesis (A), fruit maturity (M), and leaf fall (LF) are indicated.
.
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(e.g., from near anthesis [Williams 1996] to about 1 month later [Winkler and Williams 1945]). Root starch concentration in grapevines generally decreases from ca. 18% to 22% DW at budbreak to minimal levels, ca. 3% to 11% DW, around anthesis or later and increases thereafter. Root starch concentrations at leaf fall are conserved or decline slightly during winter. Total soluble sugar concentration in grapevine roots generally decreases from ca. 3% to 6% DW at budbreak to minimal levels, ca. 2% to 4% DW, around anthesis and increases sometime thereafter to peak levels, ca. 3% to 6% DW, near fruit maturity. Through autumn and winter, changes in the concentration of soluble sugars within roots are minor. In grapevine trunks, the total nonstructural carbohydrate concentration decreases from ca. 18% to 20% DW at budbreak to ca. 10% to 12% DW between anthesis and veraison. Thereafter, according to conditions, the concentration rises to peak levels, ca. 15% to 18% DW, around fruit maturity, from when it may decrease slightly. Starch concentrations in grapevine trunks generally decrease from ca. 10% to 14% at budbreak, to minimal levels, ca. 6% to 12% DW, at anthesis, or very much later, and increase to a maximum, ca. 10% to 16% DW, after fruit maturity. The midsummer minima in trunk starch concentration reported by Williams (1996) contrasts greatly with the maxima in roots at that time. Also in contrast to roots, trunk starch concentration decreases to a midwinter minimum and subsequently rises, a phenomenon attributable largely to interconversions with sugars (Winkler and Williams 1945). The total soluble sugar concentration in grapevine trunks generally declines from a peak, ca. 4% to 12% DW, in midwinter, to a minimum of ca. 1% to 4% near anthesis or several weeks later; thereafter, it increases during mid to late summer until midwinter. Phloem and Xylem. Winkler and Williams (1945) separated the phloem (bark) and xylem (wood) tissues from both roots and trunks and found differences between the seasonal course of total nonstructural carbohydrate concentrations in each tissue (Fig. 3.5). In roots, total carbohydrate reserve concentration was greater in the phloem than the xylem throughout the season. From budbreak, the concentration in phloem and xylem decreased, from about 34% DW and 15% DW, respectively, to values of less than 10% DW in both tissues near fruit maturity, and increased thereafter. In contrast, in trunks, the total reserve concentration was greater in phloem only during dormancy. From budbreak, the total reserve concentrations in phloem and xylem decreased from ca. 22%
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES
Roots A
159
Trunk M LF
A
M LF
50
Starch (%DW)
40 30 20 10 0 25
Sugar (%DW)
20
15
10
5
0
Total CHO (%DW)
50
40
30
20
10
0 –100
0
100
200
Days after budbreak
300
–100
0
100
200
300
Days after budbreak
Fig. 3.5. Seasonal carbohydrate reserve concentration dynamics in &, &; phloem (bark) and *, ; xylem (wood) of root and trunk tissue of four year-old ‘Carignane’ grapevines (source: Winkler and Williams 1945). Carbohydrate concentrations originally expressed on a residual dry weight basis have been recalculated on a total DW basis. Root carbohydrate concentrations are the average of 2-year and older root sections. The approximate times of anthesis (A), fruit maturity (M), and leaf fall (LF) are indicated.
.
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DW and ca. 18% DW, respectively, until near anthesis, when the concentration in phloem decreased to ca. 5% DW while that in xylem underwent much less change and remained above ca. 15% DW. In both roots and trunks, the total concentration of reserves in both xylem and phloem generally reflected changes in starch and sugar concentrations except during dormancy, when starch and sugars in both tissues in the trunk underwent the interconversion described earlier. Shoots and Buds. In the current season’s shoot tips (phloem and xylem) the total carbohydrate concentration increases rapidly from ca. 4% DW to ca. 14% DW over about 2 weeks from budbreak, decreases to ca. 5% near veraison, and increases thereafter to ca. 19% DW at leaf fall when the shoot, having undergone maximal lignification, may be regarded as a cane (Winkler and Williams 1945). The carbohydrate concentration in other parts of the shoot follows a similar course, but within those parts, the concentration differs between phloem and xylem tissue; there is relatively higher concentration and less variation in phloem. However, as Winkler and Williams (1945) noted, expression of carbohydrates on a dry weight basis is inappropriate for succulent tissues of low residual dry weight. Thus, apparent changes in carbohydrate concentration and differences between parts of the same organ may be due to differences in residual DW. On the more appropriate basis of water content, they generally found that total carbohydrate concentration in all organs and tissues therein increased gradually from budbreak to leaf fall. Notably after veraison, when grapevine shoot growth ceases and residual dry matter likely becomes a greater proportion of total DW, there is little difference in the seasonal course of carbohydrate concentration, whether expressed on a dry weight or water content basis. In shoot tips, the starch concentration is very low at budbreak and increases to ca. 2% DW over the following 2 weeks, decreases to ca. 1% DW near veraison, and increases gradually thereafter to ca. 13% to 16% DW at leaf fall (Winkler and Williams 1945; Koussa et al. 1998). Over the seasonal cycle, the total soluble carbohydrate concentration in grapevine buds is generally similar to that of the shoot internodes (Wample and Bary 1992; Koussa et al. 1998). Canes. Following the transition from shoot to cane, through dormancy to budbreak, the total concentration of reserve carbohydrates in canes decreases slightly, by ca. 2% to 4% DW. From a level of ca. 8% to 12% DW at budbreak, the concentration decreases to ca. 3% to 6% DW sometime between about 3 weeks before and 2 weeks after anthesis. Thereafter, it rises to ca. 13% to 16% DW by leaf fall, from when the canes are regarded
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES
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as 2-year-old branch or cordon wood (Winkler 1929; Weaver and McCune 1960; Scholefield et al. 1978; Weyand and Schultz 2006). Notably, at anthesis, there may be a small peak in total nonstructural carbohydrate concentration in short, woody, 1-year old shoots of lightly pruned grapevines that does not appear in fully formed canes of grapevines pruned more heavily—see Winkler (1929); Weyand and Schultz (2006). During dormancy, cane starch concentration may decrease from ca. 5% to 16% DW to midwinter levels of ca. 5% to 8% DW and subsequently increase as a result of interconversion with soluble sugars. From a midwinter low, the starch concentration in grapevine canes rises to ca. 7% to 15% DW at budbreak and then decreases to ca. 1% to 2% DW between anthesis and veraison. Thereafter, the starch concentration increases to ca. 6% to 8% DW in late summer but may decline to ca. 5% DW by leaf fall (Winkler 1929; Winkler and Williams 1945; Weaver and McCune 1960; Koussa et al. 1998; Weyand and Schultz 2006). Starch concentrations in both cane xylem and phloem tissues reflect this seasonal course (Winkler and Williams 1945; Goffinet 2004). During the winter starch: sugar interconversion, the soluble sugar concentration in canes peaks at ca. 6% to 12% DW in midwinter and decreases to ca. 1% to 2% DW at budbreak as starch re-forms (Winkler 1929; Weaver and McCune 1960; Koussa et al. 1998; Weyand and Schultz 2006). During the same process, raffinose also appears along with the other hexoses in cane internodes and buds. The concentration of raffinose in the internodes is notably higher than that in buds while the concentration of other hexoses may be similar or higher (Koussa et al. 1998; Jones et al. 1999). After budbreak, the soluble sugar concentration of 1-year-old grapevine canes generally increases from budbreak to ca. 4% to 5% DW near anthesis; thereafter, it decreases to ca. 1% to 3% DW at leaf fall. Goffinet (2004) found that the sucrose concentration in phloem of grapevine canes increased a little, as temperature rose, from ca. 3% DW several weeks before budbreak to ca. 3% to 4% DW at budbreak, and diminished rapidly to minimal levels, ca. 1% DW, about 2 weeks before anthesis. Thereafter, the sucrose concentration increased nearly fivefold during summer to maximal levels, ca. 4% to 5% DW, by leaf fall. General Perspective. In the examples cited, lack of accompanying data concerning seasonal residual dry weight changes obviously precludes close interpretation of reserve carbohydrate dynamics from concentration data expressed on a DW basis—either total or residual. However, seasonal courses of carbohydrate reserve concentrations, on a DW basis,
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B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE
reveal an inherent phenologically related sequence in which external conditions (including viticultural interventions) affecting photoassimilation and/or utilization impose considerable variation in terms of both seasonal reserve concentration maxima and minima and their temporal occurrences. In terms of the dynamic capacitance model, variation in carbohydrate reserve concentration, within and between seasons and locations, partly reflects the extent to which carbohydrate reserves serve to buffer incapacities in current photoassimilation and partly the extent to which constraints on growth and development (such as edaphic impediments to root growth, viticulturally limited fruit bearing, and nutritional deficiencies) restrict carbohydrate utilization.
C. Environmental Influences on Carbohydrate Reserve Concentration Experiments with potted grapevines in controlled environmental conditions indicate that the most important external conditions to influence nonstructural carbohydrate concentration are those that impact on photoassimilatory capacity including light, temperature, and water availability and viticultural practices such as leaf canopy management (R€ uhl and Alleweldt 1990; Grechi et al. 2007). External conditions that influence carbohydrate reserve concentration through utilization include those that limit utilization such as drought and low temperature and many viticultural interventions, including fertilization, pruning and defruiting. Highest total reserve carbohydrate reserve concentrations (both seasonal maxima (during dormancy) and minima (between anthesis and bunch closure)) in grapevine trunks (including branch and cane extensions thereof greater than 1-year-old) have been reported from warm climatic regions, including California’s warm San Joaquin (Williams 1996) and Sacramento valleys (Winkler and Williams 1945), where reported maximum values range from ca. 18% to 21% DW; in coolclimate conditions, maximum values range from 13% to 18% DW. Minimal values generally range between ca. 4% to 8% DW and 3% to 11% DW for warm and cool climates, respectively (Winkler and Williams 1945; Eifert et al. 1961; Korkas 1994; Williams 1996; Bennett et al. 2005; Weyand and Schultz 2006). Across a range of warm to cool vineyard conditions in New South Wales, Australia, the total nonstructural carbohydrate concentration of dormant grapevines ranged from 5.9% to 41.8% DW (Table 3.2). In that study, lowest values were found in nonirrigated vines. Differences
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Table 3.2. Influence of cultivar, region, and water supply on carbohydrate reserve concentration (%DW) of grapevines’ prior pruning. Average tissue carbohydrate concentration (%DW) Starch
Sugar
Total
Grouped by
Root
Trunkz
Spur
Root
Trunk
Spur
Root
Trunk
Spur
Cultivar Chardonnay Shiraz
19.3 25.5
8.3 8.2
7.3 6.7
2.5 2.4
5.9 5.5
5.6 6.2
21.8 27.9
14.2 13.7
12.9 12.9
Region Riverina SW slopes
23.8 21.5
9.0 7.6
7.4 6.7
2.2 2.6
6.3 5.2
6.2 5.7
26.0 24.1
15.3 12.8
13.5 12.4
Irrigation practice Furrow 22.1 Drip 25.7 Rainfall/drought 15.1
8.4 8.8 6.7
7.4 6.9 6.8
2.2 2.4 2.7
6.1 6.3 3.8
5.9 6.4 4.8
24.4 28.1 17.9
14.5 15.0 10.5
13.3 13.2 11.6
Rangey minimum maximum
3.1 12.4
5.5 9.0
1.8 3.5
2.8 9.5
3.4 8.2
12.0 41.8
5.9 18.6
10.0 14.8
9.3 39.8
z
Combined tissue sample of trunk and cordon. Lowest and highest concentrations of single vineyards. Source: J.P. Smith and B.P. Holzapfel (unpublished). y
between cultivar and climatic region were small and not statistically significant. Holzapfel et al. (unpublished) followed seasonal carbohydrate reserve concentration dynamics in a single cultivar, ‘Shiraz’, grown in three different Australian geographic regions, at similar latitude, but a fivefold range in altitude (Fig. 3.6). Regardless of location, total nonstructural carbohydrate concentration in roots and trunks generally followed similar seasonal courses as described previously, but concentrations in roots were generally higher due to greater starch concentrations. D. Influence of Fruiting on Carbohydrate Reserve Concentration Edson et al. (1993), studying 2-year-old, potted ‘Seyval’ grapevines, found that fruit load decreased leaf area and that leaf area per fruit was correlated with the capacity of vines to store carbohydrates (measured as the proportion of dry weight increment in storage organs). In a study conducted in warm vineyard conditions in Australia, where all fruit was removed soon after the onset of ripening for two successive
164
B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE
Roots A
Trunk
M
LF
A
M
LF
50
Starch (%DW)
40
30
20
10
0 25
Sugar (%DW)
20
15
10
5
0
Total CHO (%DW)
50
40
30
20
10
0 –100
0
100
200
Days after budbreak
300
–100
0
100
200
300
Days after budbreak
Fig. 3.6. Seasonal carbohydrate reserve concentration dynamics (in root and trunk tissue of cv. Shiraz grapevines in three Australian grape-growing regions, *, ; South West Slopes (35 050 S, 147 350 E; 200m) in season 2005/06. &, &; Canberra (35 140 S, 148 590 E; 600m) and ~, ~; Riverina (34 320 S, 146 070 E, 125m), both in season 2006/07. Locations and altitude indicate origin of samples. The approximate times of anthesis (A), fruit maturity (M), and leaf fall (LF) are indicated. Source: B.P. Holzapfel et al., unpublished.
.
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES
165
Table 3.3. Influence of pre-ripening fruit removal and post-harvest leaf removal for two successive seasons on carbohydrate reserve concentration (% DW) in perennial organs of grapevine ‘Semillon’ shortly after leaf fall (early winter) in the following seasonz. Average tissue carbohydrate concentration (% DW) Starch Treatment Control Leaf removalx Crop removalw
Roots Trunk 22.4 13.4 28.8 ns
9.0a 4.3b 9.6a
y
Sugars
Total
Spurs Roots Trunk Spurs Roots Trunk Spurs 10.2a 5.9b 10.7a
3.0 2.5 3.0 ns
6.6b 10.4a 5.3c
6.9b 8.7a 5.3c
25.3 15.9 31.8 ns
15.5 14.7 14.9 ns
17.1a 14.6c 16.0b
Source: Derived in part from Smith and Holzapfel (2009), with additional unpublished data. Means separated within columns using Fishers’ LSD test. Different letters within a column indicate a significant difference (p ¼ 0.05). , , , and ns indicate significance at p < 0.05, <0.01, <0.001, and not significant respectively. z Data shown are samples from one site in Australia’s Riverina regions. y Combined tissue sample of trunk and cordon. x All leaves and regrowth removed from harvest to leaf fall. w All fruit removed at the onset of ripening, about 5 weeks before harvest.
seasons, at four ‘Semillon’ vineyards. At two of these sites, where productivity was not limited by water availability, yields increased by ca. 30% when fruit was retained until commercial harvest in the following season (Holzapfel et al. 2006). At harvest, the total carbohydrate reserve concentrations in perennial organs (i.e., roots and trunks) were respectively 5% and 37% lower than those of untreated control vines (Table 3.3). Those responses demonstrate that under those conditions, fruit ripening placed significant demand on photoassimilates at the expense of carbohydrate accumulation. Without the significantly greater fruit load of the defruited vines before defruiting in the second season (see Holzapfel et al. 2006), the carbohydrate concentrations are likely to have been greater. IV. PHOTOASSIMILATION AND STORAGE PROCESSES A. Sucrose and Starch Formation in Leaves Following the initial steps of photosynthesis, triose phosphate produced in chloroplasts by the photosynthetic carbon reduction (PCR) cycle is recycled to generate ribulose bisphosphate or used in the synthesis of
166
B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE
either sucrose or starch. Starch is formed in chloroplasts, and sucrose is synthesized in the surrounding cytosol after export of triose phosphate from plastids via an inner membrane-bound phosphate transporter (Atwell et al. 1999). Synthesis of sucrose starts with the export of dihydroxy acetone phosphate and glycerol phosphate from chloroplasts to the cytosol and proceeds via a series of enzymatic steps to the formation of fructose bisphosphate and, subsequently, sucrose-6-phosphate, from which the phosphate group is removed and returned to the chloroplast for adenosin triphosphate (ATP) synthesis. Sucrose is then available for general distribution via the phloem. When the rate of sucrose formation exceeds the rate of removal by the transport system, photoassimilate is diverted into starch formation. Starch consists of two types of glucose polymer: amylose, a long, unbranched chain of D-glucose units, and amylopectin, a branched form. Synthesis of starch begins with the formation of adenosin diphosphate (ADP)-glucose from glucose 1-phosphate and ATP. Starch synthase transfers glucose residues from this molecule to the nonreducing end of a preexisting molecule of starch. The starch concentration in grapevine leaves cycles diurnally. Maximal starch levels typically occur just before sunset and minima at sunrise. Under optimal light conditions in California’s warm Central Valley, the daily leaf starch concentration (‘Thompson Seedless’) 3 weeks after anthesis ranged from 28 to 71 mg/g DW (Roper and Williams 1989). The balance between sucrose and starch synthesis, and plant carbohydrate metabolism in general, is thought to be regulated principally by fructose bisphosphate (Huber 1986). However, the nature and regulation of degradation of starch within plastids of grapevine leaves and other sites of accumulation is not well understood. Information in this regard is inferred from studies in other plants, most notably Arabidopsis. Recent studies in that species (Smith et al. 2005) indicate a process in which the surface of starch granules is degraded with the involvement of glucan water dikinase and possibly a-amylase, debranching of resultant glucans, and subsequent formation of glucose, maltose, and triose phosphate, all of which may be transported across the plastid envelope into the cytosol, where each may participate in cellular metabolism and the formation of sucrose and subsequently other soluble sugars. While the operation of this pathway remains to be confirmed in both leaves and storage tissues of grapevine, it does indicate a common route by which starch-derived sucrose, plus glucose and fructose, may be formed for symplastic and apoplastic transport systems, respectively.
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The midwinter decline in starch concentration in grapevine canes is correlated with decreasing abscisic acid (ABA) concentration and increasing a-amylase activity, indicating that starch concentration may be controlled by ABA, which is known to inhibit a-amylase activity. However, near budbreak, starch concentration in both internodes and buds (on a DW basis) and a-amylase activity are all high, a condition that may be related to some physiological effect of winter chilling (Koussa et al. 2005). B. Distribution of Sucrose from Leaves Sucrose, formed directly from photosynthate or from the degradation of starch stored within chloroplasts, is the main carbohydrate transferred within grapevines and is transported exclusively in phloem sieve elements (Mullins et al. 1992). Sucrose from mature leaves is translocated either acropetally (to shoot tips, stems, and young leaves) or basipetally (to developing fruit clusters and perennial organs), depending on the temporal demand in those organs. The movement of sucrose within the phloem is generally described by the pressure flow model of M€ unch (1930) and facilitated by loading of sucrose into the sieveelement companion cell complex against a concentration gradient involving cotransport with protons and a respiratory expenditure of about 1.45% of the amount of sucrose available for translocation (Giaquinta 1983). Whether the loading of sucrose into, and unloading from, sieve elements in grapevine occurs by an apoplastic or symplastic path or both has not been resolved (see Lucas and Madore 1988; Turgeon 1989; Van Bel 1993 for evidence from other species). According to Kozlowski (1992), most radial xylem-to-phloem sugar transport and all phloem-to-xylem transport occurs symplastically through the ray parenchyma. Sucrose is distributed from leaves to various grapevine organs to provide energy and carbon for structural growth and development and storage changes during the growing season according to shifts in demand that accompany phenological development and environmental contingencies (Hale and Weaver 1962; Koblet 1969). Apportionment of sucrose to different organs appears to be demand driven; the determinant of the amount of sucrose apportioned probably is the rate of sucrose uptake from the transport system in response to genetic control of metabolic processes within the cells of the particular organ—for example, developing fruit and shoots or storage organs. Sucrose transport from photoassimilatory activity in the period following fruit maturity, in some
168
B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE
circumstances, may be vital for the replenishment of carbohydrate reserves (Hunter et al. 1994). Based on experiments with potted ‘Delaware’ (V. labruscana) grapevines using 14C isotopes of carbon dioxide (CO2) to label photoassimilates, Yang and Hori (1979) estimated that 28%of labeled carbon assimilated throughout the season was retained in the vine at the end of the season, of which 10%, 23%, and 67% were distributed to the cane, trunk, and roots, respectively. However, the proportions representing insoluble, nonstructural carbohydrates (i.e., starch) were not determined. Sucrose translocated from leaves (and other photosynthetic tissues) provides the substrate for starch formation in the plastids (amyloplasts) of root, trunk, and nonphotosynthetic stem and bud tissues. In these tissues, sucrose is hydrolyzed, probably by a cytosolic alkaline invertase to glucose and fructose and/or a sucrose synthase, to fructose and uridine diphosphate (UDP)-glucose and then to hexose phosphate before transport via a phosphate translocation across the inner plastid membrane (Atwell et al. 1999) prior to starch formation, which probably involves starch synthase, as it does in leaves and other photosynthetic tissue. C. Genetic, Phenological, and Environmental Influences on Photoassimilation and Carbohydrate Accumulation 1. Genetic Influences. Grape cultivars, even of different ecological origin, show no differences in maximum photosynthetic rates and in the response to varying light intensities under optimum, well-watered conditions (Albuquerque and Carbonneau, 1992). However, cultivarassociated differences do appear in responses to environmental factors that influence photoassimilation (e.g., impacts of water deficits on stomatal conductance) (D€ uring 1978; Schultz 1996) and temperature (Zuffery et al., 2000). There is little or no definitive information concerning genetic influences on the propensity of grapevines to store carbohydrates. 2. Phenological Influences. In grapevine, like other deciduous species, maximal photoassimilation rates generally follow the seasonal reestablishment of leaf canopies. Peak photosynthetic activity of individual leaves is attained about 40 days after unfolding and declines gradually thereafter (Kriedemann et al. 1970). Whole canopy photosynthesis reaches maximal rates near veraison, the onset of fruit ripening (Poni et al. 2000). During fruit ripening, photoassimilation appears to be demand driven. Highest rates are maintained on fruit-bearing shoots, and rates decline
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES
169
when fruit is removed (Downtown et al., 1987; Hof€acker 1977). Although photoassimilation usually declines after fruit maturity (Scholefield et al. 1978), it may contribute a considerable amount of carbohydrate if leaves remain functional and conditions favor photosynthesis. Thus in the lead-up to dormancy, photoassimilation and possibly redistribution of leaf carbohydrates prior to leaf abscission may contribute to increases in trunk carbohydrate content. Storage of current season’s reserves in perennial organs of grapevines is confined to living phloem and xylem tissues within those organs. Carbohydrates of the current season may be stored in the older xylem. Although grapevine phloem usually becomes functionless after two seasons, it may remain functional for up to four, particularly in trunks. This feature is more pronounced in some cultivars than in others. However, it seems likely that in grapevine, most current season’s reserves are accumulated in vascular tissues formed by cambial activity in that season, a process initially sustained by carbohydrate reserves from the previous season (Esau 1948). Grapevines show a basipetal course of cambial reactivation characteristic of woody dicotyledons. It first occurs in tissue adjacent to each bud and about 2 weeks after the bud breaks. In accord with apical dominance of budbreak, reactivation proceeds from cane apices, to the trunk, and is completed in roots more than 8 weeks later (Esau 1948), near the time of anthesis. While the evidence indicates that current photoassimilates are directed to trunks and roots, at least toward the latter part of the reactivation period (Hale and Weaver 1962; Koblet 1969), it appears, from the general phenologically related course of carbohydrate reserve concentration, that net accumulation in those organs and others may take place during and after that time through to leaf fall, but only during periods of relatively inactive cell division and growth in that organ. For example, Esau (1948) found that starch accumulation in 1-year-old canes first commenced in preexisting xylem and subsequently new phloem and xylem after fruit set and after cambial activity in the canes was complete. In new shoots, starch deposition occurs in midsummer after cambium formation and its production of a xylem increment, wherein accumulation first becomes apparent in the innermost tissue (Yang et al. 1980; Goffinet 2004). 3. Environmental Influences. Environmental factors, both physical and biotic, influence photoassimilation in grapevines in terms of both biophysical function and capacity. Defoliation by natural causes (e.g., drought, hail, and herbivory) commonly diminishes photoassimilatory capacity and, consequently, carbohydrate reserve dynamics. If leaves are
170
B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE
removed, daily carbohydrate requirements for fruit development and vegetative growth may be met from reserves in the perennial parts (Candolfi-Vasconcelos et al. 1994) and/or compensatory photoassimilation in remaining leaves (Petrie et al. 1939; Waring et al. 1968). However, studies involving leaf removal reveal that the nature and quantum of the impact on carbohydrate status depends on the extent and phenological stage of defoliation. Defoliation between Budbreak and Fruit Set. Winkler (1929) showed that total leaf removal 2 weeks before anthesis reduced fruit set and berry development. These responses were associated with a decrease in the total sugar concentration in opening flowers and a decrease in the germination of pollen. Although leaves arising after fruit set were allowed to develop, it is likely that berry development was impaired by carbohydrate stress well after fruit set. Given the high dependence of the grapevine on reserves for seasonal reestablishment between budbreak and fruit set, leaf removal might be expected to delay reestablishment and the restoration of reserves. Defoliation between Fruit Set and Harvest. Complete defoliation of ‘Concord’ at the onset of ripening (veraison) reduced the rate of sugar (soluble solids concentration) accumulation and the survival of primary buds during winter and delayed budbreak in the following spring. Partial (50%) defoliation had similar effects, but responses depended on how defoliation was achieved—removal of alternate leaves, removal of leaves on alternate shoots, or removal of all leaves from one-half of grapevines— and generally increased with distance between the foliated and defoliated parts of the vine (Howell et al. 1978). These effects are consistent with carbohydrate stress, although, other than fruit sugar, carbohydrates were not measured in that study. Sugar accumulation in the complete absence of leaves provided strong evidence for mobilization of carbohydrate reserves. After completely defoliating minimally pruned grapevines of the same cultivar about 2 weeks after veraison, Goffinet (2004) found cane phloem and xylem starchlevels atthe budbreakofthe following season werealmost half those of nondefoliated grapevines and remained low. In that season, leaf number and area were also reduced, generating only low reserves for the next season. Defoliation had little effect on the timing of floral development, but defoliated grapevines had fewer flowers per cluster. On a percentage basis, fruit set was greater but fruit yield was halved. Bennett et al. (2005) found that 75% defoliation (removal of all but 4 basal leaves) 4, 8, and 12 weeks after anthesis of ‘Chardonnay’ decreased
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES
171
winter carbohydrate reserves in both roots and trunks, with earlier defoliation causing greatest reductions. Roots were most affected with early defoliation, reducing starch concentrations at budbreak to 1.5% DW compared to 17% in nondefoliated vines. Lowered root and trunk carbohydrate reserves were closely associated with decreases in inflorescence number per shoot and flower number per inflorescence (up to 50% less than nondefoliated vines). Differences in carbohydrate concentrations in both trunks and roots were maintained to veraison, but percent fruit set was unaffected. Berry weight was also unaffected, suggesting that yield reductions in that season were due to the fewer inflorescences and flowers per inflorescence. Percent budbreak and shoot length were not affected, but cane weight and diameter at the end of the season were reduced greatly by defoliation in the previous season. Defoliation from Harvest to Leaf Fall. Scholefield et al. (1978) showed that in conditions favoring up to 3 months of postharvest photoassimilation, annual, autumnal partial leaf removal (60%) from ‘Sultanina’ had no significant effect on carbohydrate storage but erratically induced decreases in fruiting in the following season by up to 15% (see Scholefield et al. 1977). Removal of all leaves at harvest led to decreased fruiting, ranging from 44% to 75% less than fully foliated control vines in the following season, but the impact on carbohydrate reserves was not established. However, Holzapfel et al. (2006), in climatically similar locations, found that after one season of total defoliation of ‘Semillon’ at harvest, fruit bearing was reduced by ca. 22% and, after two seasons, by ca. 35%. At leaf fall, after two successive seasons of total defoliation, the total carbohydrate concentration (%DW) of roots, trunks, and spurs was reduced by 37%, 5%, and 15%, respectively (Smith and Holzapfel 2009) (Table 3.3). In that study, partial defoliation (50%) had no effect on carbohydrates reserves or fruiting in the following season (Holzapfel and Smith 2007). Both these studies indicated a compensatory increase in photosynthetic intensity of leaves remaining after defoliation at levels up to 60% and point to compensatory mechanisms such as delayed senescence and maintenance of high photoassimilation rates that are well known in other plants (Petrie et al. 1939; Waring et al. 1968). Other Abiotic Influences. Light, temperature, and water greatly affect photoassimilation and carbohydrate storage in grapevines (Kriedemann and Smart 1971; Downtown et al., 1987; R€ uhl and Alleweldt 1990). Fig. 3.7 indicates grapevine responsiveness of photoassimilation rate
B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE
Relative rate (% of maximum)
172
100
(a)
30ºC
(b) 20º
20ºC
80
10ºC
60
40ºC
40
45ºC
30º
20
35º
0 [CO2]=364 ppm
–20 0
500
1000
1500
PFD (umol
m–2s–1)
2000
0.0
0.4
0.8
1.2
1.6
Leaf water tension (kPa x 10–3)
Fig. 3.7. Responses of grapevine photosynthesis to environmental factors. (a) Relative photosynthesis rates (single leaf) of potted ‘Shiraz’ vines at different temperatures and light regimes (short time exposure) at ambient CO2. Source: J.P. Smith and S.K. Field, unpublished data. (b) General relative response of net photosynthetic rate to vine leaf water tension at three air temperatures). Source: Redrawn from Hardie and Martin (1990).
to each of these environmental factors. Light and temperature generally follow seasonal and diurnal courses but may vary transiently from either and thus create a need for contingencies in terms of carbohydrate supply. The potential impact of environmental limitations on photoassimilation and reserve accumulation during the period from fruit harvest to leaf fall may be inferred from responses to leaf removal during that period, as mentioned previously. In warm climates, where significant carbohydrate reserve accumulation occurs after fruit maturation, environmental impacts on photoassimilation during that period may strongly influence reserve levels at leaf fall. In cool regions, where there may be a short period between fruit maturity and leaf fall, environmental conditions generally limit photoassimilation and carbohydrate reserve accumulation. Temperature also appears to directly influence the concentrations of sucrose and starch in grapevine leaves. Increasing temperature results in the apparent conversion of starch to lipidlike material within leaf chloroplasts (Buttrose and Hale 1971). A similar conversion occurs in the plastids of the developing fruit (Hardie et al. 1996), but whether this is due to temperature or inherent developmental processes may be elucidated along with better understanding of the process of starch degradation. Water availability influences not only current photoassimilation rate but also the relative growth of grapevine organs (Van Zyl 1984; Dry and
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Loveys 1999) and may thus determine the net accumulation and seasonal dynamics of carbohydrate reserves. The direct impact of water availability on carbohydrate reserves has been examined by several groups. R€ uhl and Alleweldt (1990), using 6-week-old rooted cuttings (‘Riesling’, ‘M€ uller-Thurgau’, ‘Trollinger’, and the V. riparia V. berlandieri hybrid ‘Kober 5BB’) found that water stress affected carbohydrate accumulation in the roots and stems. The concentration of carbohydrates usually increased while the total amount accumulated decreased. Water stress caused a severe reduction in carbohydrate accumulation in ‘Kober 5BB’ but not in ‘Riesling’. In mature vines, at leaf fall, the total concentration of carbohydrate reserves in roots of water-stressed vines grown without irrigation was very low (ca. 12% DW) and, within the season, varied much less than that of vines that were adequately watered (Smith and Holzapfel 2009). Impacts of Global Climate Change. The predicted global rises in atmospheric carbon dioxide concentration and temperature are likely to influence photoassimilation in grapevines. A near doubling of atmospheric CO2 concentration from the current ambient (370 ppm) increased net photoassimilation of field-grown ‘Riesling’ by about 35% (Schultz 2000). However, effects of increasing CO2 concentrations on photoassimilation may, in some places, be offset by effects of supraoptimal temperatures, which include reductions in photosynthesis, increased respiration, and shorter phenological stages (Bindi et al. 2001). Kriedemann et al. (1976) showed that a combination of high temperature (37–40 C day and night) and high CO2(1200–1300 ppm) for 14 days induced a higher rate of photoassimilation relative to transpiration in ‘Cabernet Sauvignon’ in growth chamber conditions. This was accompanied by an increase in leaf starch accumulation, a more than twofold increase in growth rate, and a shift in dry matter production toward root growth. However, longer-term exposure to elevated CO2 concentration generally leads to downregulation of photosynthesis associated with sink saturation by assimilates (Samarakoon and Gifford 1995). Current models of grapevine carbon relations do not appear to have addressed this aspect. Biotic Influence. Biotic stresses imposed by herbivorous insects and fungi reduce the photoassimilatory and hence carbohydrate storage capacity of grapevines, chiefly by reducing leaf area and hence photosynthetic capacity of vines (Boucher et al. 1987). In viticultural regions globally, there are many insect species, some endemic and some exotic, that cause this type of photoassimilatory stress. For example, in
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Australia, the grapevine moth (Phalaenoides glycine) is common, and larvae, if uncontrolled, may consume a large proportion of leaf area (Buchanan and Amos 1992). Several globally dispersed fungal diseases, such as the powdery mildew (Uncinula necator) and downy mildew (Plasmopara viticola), similarly disrupt photoassimilation. Infected leaves or parts of leaves become photosynthetically dysfunctional with negative, carbohydrate-related impacts on growth and development in the following season (Nail and Howell 2005). A general perspective of the likely impact of pests and diseases that consume foliage can be gained from previously mentioned studies on the impacts of defoliation. Several common grapevine virus infections may also reduce carbohydrate accumulation in perennial parts (R€ uhl and Clingeleffer 1993). Grapevine leaf role virus, globally the most widespread virus disease of grapevines, reduces photosynthesis, resulting in reduced growth and fruiting capacity and delayed fruit maturity (Cabaleiro et al. 1999). Grapevines infected with ‘Esca’ disease, involving a complex of several fungal species, including Phaeomoniella chlamydosporum, Phaeoacremonium aleophilum, and Fomitiporia mediterranea, which mainly invade nonfunctional trunk wood, show reduced photosynthetic capacity, lower winter carbohydrate reserves, and, consequently, diminished vegetative growth and fruit bearing in the following season (Petit et al. 2006). Strictly from a grapevine perspective, shoot pruning and other foliar interventions by humans are essentially seasonal damages inflicted by a biotic agent; however, recognizing this relationship may be useful in understanding inherent response capacities of vines to similar damage from other sources. Responses to pruning and similar viticultural interventions are reviewed in more detail in Section VI.A. Essentially, the removal of most regenerative buds through shoot pruning directs carbohydrate and other reserves to those remaining and results in both growth andreproductiveenhancementofindividualshootsbutatacosttotheplant of total photoassimilation capacity, both in terms of reduced leaf area and delayed full canopy development and perturbation of carbohydrate dynamics compared with grapevines in the natural or near-natural condition.
V. MOBILIZATION AND UTILIZATION OF CARBOHYDRATE RESERVES A. Daily Metabolism Photoassimilate, whether directly from current photosynthesis or from previously stored starch reserves, is exported from plastids (chloroplasts
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and amyloplasts) to the cytosol and mitochondria, where it undergoes glycolysis and respiration, respectively. ATP and redox equivalents generated by these processes energize essential functions, such as growth and mineral nutrient uptake (Atwell et al. 1999). Carbon skeletons, also formed during mitochondrial respiration, are utilized in synthesis of other essential plant products, including organic acids, amino acids, carotenoids, phenolics, nucleotides, porphyrin pigments, lipids, sterols, and carotenoids. During sunlight, the primary sources of carbohydrates for respiration are soluble sugars and/or starch from recent carbon assimilation in photosynthetic tissues, principally leaves but also shoots, fruit, and fruit stems. At night (and during other light-limited conditions), respiration utilizes surplus photoassimilate accumulated as starch within plastids of leaves and all other organs of the grapevine.
B. Seasonal Growth and Development 1. Seasonal Reestablishment. In early spring, following dormancy, grapevines, like other deciduous plants, depend on carbohydrate reserves, chiefly starch, as respiratory substrates for the seasonal redevelopment of photoassimilatory capacity, resumption of reproductive development suspended during dormancy, and incremental growth in perennial organs. Reestablishment of the first two functions takes place from primordial shoots contained within compound buds formed in previous seasons, predominantly from the most recent one. When buds start to swell before budbreak, the inflorescence primordia borne on primordial shoots and initiated in the preceding season resume branch development and commence flower formation (May 2000; Goffinet 2004). 2. Triggers for Mobilization of Reserves. Release from dormancy is characterized by depletion of nonstructural carbohydrates in roots and subsequently other perennial parts of grapevines (Winkler and Williams 1945), hydration of buds, and resumption of cell division within buds several weeks before budbreak (May 2000). Around that time, xylem sap flow, from cut or damaged stems (Winkler and Williams 1945; Andersen and Brodbeck, 1988; Campbell and Strother 1996), is indicative of root pressure associated with the presence of solutes in the sap. Solutes include minerals, sugars, and amino acids, most notably glutamate, which may make the greatest contribution to osmotic generation of root pressure (Andersen and Brodbeck 1989a,b).
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The onset of xylem pressure coincides with commencement of starch degradation in roots (Winkler and Williams 1948). Glucose and fructose from starch degradation contribute to the osmotic potential of xylem sap, although, on a concentration basis, sugars form a small fraction of the total organic compounds and minerals present (Andersen and Brodbeck, 1989). The creation of an osmotic gradient within the xylem is thought to lead to an influx of water from the roots to refill and pressurize the xylem vessels after winter (Scholander et al. 1955; Kramer 1983). Although these events precede transpirational flow by several weeks, rehydration and solutes within the sap may well induce and/or sustain early season development of aboveground organs. It is not clear where or how the release from dormancy, and the associated stimulus for the degradation of starch and mobilization of reserves, is initiated. Available evidence suggests that rising temperature is the principal environmental driver and that air temperature determines resumption of bud activity (De Candolle, 1885; Poenaru and Lazarescu 1959; May and Antcliff 1963) while soil temperature determines the resumption of xylem activity and the ensuing transport of water, carbohydrates, and other metabolites and growth substances that sustain early-season shoot growth and inflorescence development (Gladstones 1992; Field et al. 2009). In addition to the avoidance of winter drought stress previously referred to, mobilization of root reserves based on soil temperature, which is generally buffered from diurnal variation, would obviously afford protection against general release of dormancy by transient changes in air temperature, but there is little information concerning this aspect in grapevines. Moncur et al. (1989), by extrapolating a rate of budbreak versus temperature relationship, indicated that internal processes leading to budbreak in some grapevine cultivars may commence at mean daily air temperatures well below 10 C and as low as 0.4 C. Field et al. (2009) found that depletion of total nonstructural carbohydrates from grapevine roots between late dormancy and anthesis was much greater in warmer soil. In aboveground organs (trunks and canes) during dormancy, decreasing temperature appears to drive the conversion of starch to sugars; however, the reconversion to starch occurs as air temperatures rise after middormancy. In roots where such reconversion to starch does not occur and concentrations of both remain comparatively stable during winter, some other temperature-determined process, probably associated with development of root pressure, may be a prerequisite for mobilization of carbohydrates from roots in late dormancy. The cytokinin zeatin riboside, presumably root generated, appears to be associated with the
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mobilization of carbohydrate reserves at the end of dormancy and ensuing shoot growth (Field et al. 2009). C. Carbohydrates from Perennial Reserves 1. Mobilization and Distribution. There is no vascular movement of carbohydrates within grapevines during dormancy; phloem sieve plates are occluded with callose (b- (1 ! 3) glucan) (Esau 1948), and xylem vessels are filled with air (Scholander et al. 1955). The first visual indicator of reserve mobilization in cultivated grapevines is the flow of solute-containing xylem sap from cut stems, which usually occurs several weeks before budbreak (Winkler and Williams 1945). Glucose and fructose are the predominant sugars in xylem sap (Andersen and Brodbeck 1989a; Glad et al. 1992), and their concentrations fluctuate diurnally (Andersen and Brodbeck 1989a). The presence of both sugars plus the absence of sucrose is indicative of xylem sap. Sucrose has been reported in trace amounts in xylem sap but only from the onset of “bleeding” (Galet 1979; Glad et al. 1992) and is generally regarded as an entrant from phloem tissues (Andersen and Brodbeck 1989a). Reported concentrations of carbohydrates in bleeding xylem sap vary widely. Ohkawa (1981, 1982) reported total carbohydrate concentrations of approximately 25 mg per milliliter (ca. 139 mM glucose equivalents) in sap of ‘Muscat of Alexandria’, significantly more than values of 120 mg glucose equivalents per liter (ca. 660 mM glucose equivalents) reported in ‘Waltham Cross’ (Campbell and Strother 1996) and 500 mM reported in ‘Chardonnay’ grafted to 41B rootstock (Glad et al. 1992), and similar levels between ca. 100 to 500 mM in xylem exudate of several Muscadinia rotundifolia (formerly Vitis rotundifolia) cultivars reported by Andersen and Brodbeck 1989a,b 1991. After budbreak, the total carbohydrate concentration of xylem sap decreases to zero over the course of 2 to 3 weeks (Ohkawa 1981, 1982; Campbell and Strother 1996). The presence of glucose and fructose in xylem sap, together with the absence of sucrose, points to inversion of starch-derived sucrose within parenchyma cells of the xylem and phloem (possibly by a membranebound invertase) and distribution through the xylem. Loading of sugars into the xylem may possibly be facilitated by transfer cells or, in secondary tissues, by close association of living ray parenchyma and xylem vessels (Atwell et al. 1999). In 1-year-old grapevine canes following dormancy, removal of callose from sieve plates of phloem formed in the previous season commences near budbreak (as the upper axillary buds are breaking through scales)
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and proceeds in a basipetal direction, until about 6 weeks later, when preexisting phloem is completely reactivated and newly formed phloem is fully functional (Esau 1948). Trunk phloem reactivation follows a similar course to that of 1-year-old canes. Root phloem, unlike aboveground phloem, does not appear to become dormant (Esau 1948). In early spring, until phloem reactivation is complete, the vascular route of distribution of carbohydrate from perennial reserves from phloem and xylem (parenchyma) tissues in wood and roots is initially xylem mediated. After xylem sap becomes devoid of sugars and for the remainder of the season, phloem-mediated sucrose transport distributes carbohydrate within grapevines. 2. Recommencement of Growth. Both early seasonal grapevine development and subsequent vegetative growth and fruiting utilize stored carbohydrate. However, in addressing the source-sink relations involved, we note that inferences based on proximal observations and analyses form a considerable source of current insights of carbohydrate reserve utilization in grapevines. We caution that interpretation of utilization relations based on contemporaneous depletion of reserves and physiological development in other parts of the plant may oversimplify or misrepresent actual utilization because depletion of reserves in particular organs, or tissues thereof, may in part reflect in situ demand for maintenance and structural development rather than utilization elsewhere. For this reason, findings based on the movement and fate of labeled carbohydrates provide the most definitive evidence as to utilization of reserves, notwithstanding interpretational limits also associated with some tracer-based approaches. In grapevines, budbreak and commencement of shoot growth precede root growth by several weeks (Freeman and Smart 1976; Richards 1983; Mohr 1996). In aerial organs, reactivation of the previous season’s phloem precedes cambial activity by about 2 weeks and is fully functional before much of the new phloem has been produced (Esau 1948). As noted previously, cambial activity first recommences each season opposite the most apical buds and proceeds in a basipetal direction—a process possibly induced and sustained by a hormone produced in those adjacent buds (Esau 1948). Starch depletion characteristics indicate that the carbohydrate requirements for these developments are mobilized from reserves in proximal parenchyma (Esau 1948), but they may also be drawn from static, pretranspirational, pressurized xylem sap. For several weeks after budbreak, as leaf development occurs and mediates transpirational flow, and before preexisting phloem is fully reactivated and new phloem is formed, low xylem pressure due to low
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soil water potential (due to cold, drought, or soil solutes) may have a direct bearing on the rate of transport of carbohydrate to developing organs. In the first stages of budbreak in ‘Concord’, starch stored in the primordial shoot and surrounding bud scales during the previous season evidently supports early shoot development. Thereafter, starch, from canes emerging from dormancy, is utilized and sucrose export progresses from conductive phloem and phloem rays, outer xylem rays and outmost wood fibers, and then from inner wood fibers and innermost xylem rays (Goffinet 2004). As shoot growth proceeds, reserves from trunks and roots of the grapevine are also utilized. Experiments with potted ‘Delaware’ grapevines, using 14C isotopes of CO2 to label photoassimilates in the preceding season, showed that their products were retranslocated at their greatest rate to the new season’s shoots at the 6- to 10-leaf stage (Yang and Hori 1979; Yang et al. 1980). About half the products were carbohydrates, and the other half were amino and other organic acids. All were considered to have been translocated and mostly from the roots where most labeled carbon had accumulated as carbohydrates. Mobilization of starch from root tissue follows a similar drawdown sequence to that from the canes (Zapata et al. 2004). At about the 9- to 10-leaf stage, generally about 9 weeks after budbreak, and near anthesis, as the photosynthetic capacity of upper leaves becomes sufficient to support growing shoot tips, there is a distinct switch as newly assimilated carbon begins to be exported from the lower leaves toward the perennial and reproductive organs the grapevine (Hale and Weaver 1962; Yang and Hori 1979; Yang et al. 1980). Some of that carbon may contribute to nonstructural carbohydrate reserves, but the actual amount is likely to depend on metabolic demand within recipient organs. From budbreak until 1 week after anthesis, on a dry weight basis, total root nonstructural carbohydrate initially declines before restoration commences (see Fig. 3.4). Over that period, Roper and Williams (1989) found that 93 g of nontructural carbohydrates were utilized from the trunk and cordons of mature, field-grown grapevines (‘Chenin Blanc’) and nonstructural carbohydrate content in the root increased by a similar amount. D. Growth and Development of Perennial Organs 1. Predormancy. Grape shoots arise from bud primordia initiated in the axis of each leaf commencing from about anthesis at the basal shoot node. Carbohydrate reserve status during the period between initiation and dormancy appears to have little effect on early shoot development,
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including differentiation of inflorescence primordia attached. For example, Goffinet (2004), for two successive seasons, subjected minimally pruned, field-grown grapevines (V. labruscana ‘Concord’) to carbon stress (by defoliation about 14 days after ripening commenced) or carbon destress (by fruit removal about 30 days after anthesis). At dormancy, despite differences in cane xylem starch and phloem starch of 53% and 50% (estimated from carbohydrate measurements at budbreak in the following year) between the control and most-stressed vines, respectively, buds of all treatments varied little in length and number of leaf primordial, although cross-sectional area of the stems of control vines, with least carbohydrate stress, was greatest. Notably, at that stage, differentiation of inflorescences was similar for all treatments. 2. Postdormancy Shoot Growth and Floral Development. Effects of carbohydrate reserves on floral differentiation, and probably inflorescence branching and retention, following dormancy significantly influence fruit yield in that season and, through effects on bud initiation, account for variation in fruiting from season to season (Goffinet 2004; Bennett et al. 2005; Smith and Holzapfel 2009). Following dormancy and through to anthesis, shoot growth and floral differentiation take place during a period when net carbohydrate balance is negative. During this period, the accumulated carbohydrate reserves of previous seasons is a significant determinant of the rate of shoot growth and the ultimate foliar canopy size in the following season and of the continued development of inflorescences initiated in the previous season. In the field study of Goffinet (2004) cited previously, depleted starch reserves at budbreak were accompanied by depressed shoot growth, leaf production, and maturation rates, and leaf area per shoot. At anthesis, flower number per inflorescence was half that of non–carbon stressed, that is, nondefoliated, vines. In Australia’s Riverina region, average flower numbers per inflorescence of ‘Semillon’ starting the season with low or high carbohydrate reserves ranged from 234 to 317, respectively, although the number was not significantly different (Smith and Holzapfel 2009). Similarly in New Zealand, the number of flowers per inflorescence of ‘Chardonnay’ increased from approximately 149 to 258 with increasing carbohydrate reserves (Bennett et al. 2005). S anchez and Dokoozlian (2003) found that near the time of anthesis when shoot primordia begin to form, bud carbohydrate concentration was directly correlated with the number of fruit primordia formed.
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Fruit Growth and Ripening. During fruit set and early stages of berry growth, there is sometimes a strong, competitive demand by shoots and almost certainly other organs, such as roots and trunks, for photoassimilates (Koblet 1969). Indirect evidence of such demand is provided by increased fruit set following application of growth retardants (Coombe 1970) or removal of shoot tips (Coombe and Dry 1992) and increased berry size following trunk or stem girdling (phloem severance) (Coombe and Dry 1992). Those responses may be attributed to redirection of current photoassimilate to fruit development. However, evidence that carbohydrate nutrition in general (i.e., leaf area and carbohydrate reserves) is positively correlated with pollen germinability and fruit set (Winkler 1929) indicates that carbohydrate reserves may contribute to fruit development under some conditions, such as those during suboptimal photoassimilatory periods. During ripening, sucrose translocated to the fruit is accumulated as fructose and glucose. Experiments with radioactively labeled carbohydrate reserves show that carbohydrate reserves may be utilized for fruit ripening but carbohydrates do not move from reserves to the fruit in the last few weeks before harvest (Candolfi-Vasconcelos et al. 1994), probably because vascular connections to the fruit (Rogiers et al. 2001) and cell membranes within the fruit pericarp become dysfunctional before that time. Cane and Trunk Growth. Radial growth of shoots older than one season (i.e., canes and trunks) accompanies the reactivation of cambial activity each season. Prior to anthesis cambial activity in these organs (see Section C.2) utilizes reserve carbohydrates from the previous season. Thereafter, current photoassimilates may be used, but stored carbohydrates are likely to buffer photoassimilatory contingencies, as they do for fruit development. Root Growth. Radial growth of roots accompanies the reactivation of cambial activity, which commences some 4 weeks later than in canes. Root elongation growth proceeds from initials arising from older roots. Commencement of elongation generally lags behind shoot growth and may not occur until shortly before anthesis, when shoot growth rate normally peaks (Hiroyasu 1962; Freeman and Smart 1976; McKenry 1984; Van Zyl 1984; Araujo and Williams 1988; Williams and Matthews 1990; Mohr 1996; Comas et al. 2005). Following an initial period of growth lasting several weeks, further elongation may take place in autumn, in warm regions, after fruit has been removed (Van Zyl and Van Huysteen, 1987; Bates et al. 2002; Conradie 2005). A contribution of
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carbohydrate reserves to root elongation has not been established. Based on the alternation of growth between aerial organs, Mullins et al. (1992) suggested that root elongation occurs only when excess photosynthate is available. However, part of the typical depletion of root reserve carbohydrates after budbreak must contribute at least to cambial reactivation and radial growth before the export of current photoassimilate from shoots. Morinaga et al. (2003) found that root activity (and vegetative growth) of potted, greenhouse-grown ‘Aki-queen’ were strongly affected by fruit load and that vines with greatest fruit loads accumulated less photoassimilates in roots (and shoots), thus demonstrating that fruit imposes predominant demand in the accumulation of photoassimilates. E. Grapevine Defense and Repair During the normal seasonal course of growth and development, environmental stresses and herbivory (encompassing attacks on the biomass of the plant by other organisms) represent contingencies that impose demands that either divert resources from core metabolism (including reserve accumulation) or consume reserves directly. Defense, repair, and recovery of biomass (e.g., refoliation) after herbivory draws on carbohydrate (and other metabolites) that otherwise would participate in normal growth and development. As an adaptive advantage, it is likely that carbohydrate reserves support those processes by providing respiratory substrate for their biosynthesis in times when current photoassimilation is limited. In this section we examine evidence for such a role, particularly evidence that directly associates low reserves with suboptimal functioning of those processes. Of course, direct feeding of reserves by herbivores limits their utilization by the plant, with likely direct consequences, particularly in early spring. 1. Resistance and Tolerance to Environmental Stress Cold Hardiness and Freeze Protection of Buds and Trunk Tissues. In buds and trunk tissues of grapevine, the process of acclimation to winter cold is accompanied by dehydration and carbohydrate storage (Goffinet 2000). As mentioned previously, conversion of starch to soluble sugars takes place in aboveground organs in a process generally associated with falling temperature (Fig. 3.8). Starch-derived sugars have long been implicated in cryoprotection of plant parts during winter (Levitt 1980). Increasingly negative osmotic potential has been thought to cause freezing point depression of cellular sap, providing a measure of
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20
Glucose (%DW)
Sugar Starch Total CHO Temperature
15
10
5
LF
BB
10 0 –10
Temperature (ºC)
20
0
–20 October November December January
February
March
April
Fig. 3.8. Dynamics of starch, sugars, and total carbohydrate concentration in shoots (at the 10th internode) of Riparia portalis during dormancy and average air temperature (adapted from Eifert et al. 1961). The times of leaf fall (LF) and budbreak (BB) are indicated.
protection against freezing to buds, canes, and trunks (Sakai and Larcher 1987). However, the association between carbohydrates and cold hardiness remains essentially correlative (Jones et al. 1999) and brings into question a protective role of soluble carbohydrates through freezing point depression (Vasil’yev 1961; Wample and Bary 1992; Wample et al. 2000). Other mechanisms involving sugars include lowered ice nucleation point (Gunnink 1989), energy production (Sakai and Larcher 1987), and cryoprotection of proteins and membranes (Ashworth et al. 1993; Hincha et al. 1990). Grapevine roots, although rich in carbohydrate reserves during dormancy, apparently have little cold resistance (Guo et al. 1987; Wample et al. 2000), a feature possibly related to the observation that they lack the overwinter conversion of starch to sugars that takes place in aboveground organs. Raffinose, a sugar derived from the conversion, is consistently associated with cold hardiness in grapevine buds and canes (Barka and Audran 1996; Hamman et al. 1996; Jones et al. 1999). Regardless of the adaptive mechanism, measurable differences in cold hardiness occur, and carbohydrate reserves must have a role in any protective process, at least as a source for associated respiratory activity.
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Frost Injury. Reestablishment of shoots and foliage in conditions of diminished photoassimilatory capacity after frost injury places direct demand on carbohydrate resources. However, direct utilization of stored reserves is likely only following frost damage prior to anthesis, before growth is normally independent of stored carbohydrate reserves. We have not seen measures of this additional demand on carbohydrate reserves, but weak regrowth of shoots after severe damage is common, indicating that the impact may be considerable. Heat, Light, and Water Stress. Photoassimilation in grapevines is limited by excessive heat, soil water deficits, and low light intensity (Kriedemann and Smart 1971; Sepulveda and Kliewer 1986). Recovery of photosynthetic systems impaired by heat and drought stress may be protracted, extending to several days (Kriedemann et al. 1975; Sepulveda and Kliewer 1986). Utilization of carbohydrate reserves during the recovery period may be expected but appear to be unreported. 2. Resistance and Tolerance to Biotic Stresses. Low carbohydrate reserves sometimes are considered responsible for increased susceptibility of grapevines to biotic diseases. For example, Petri disease (formerly known as black goo), a fungal disease of grapevine trunks leading to retarded shoot growth and caused by Phaeomoniella chlamydosporum, is one of many causes of a condition known as restricted spring growth. Susceptibility to the disease is thought by some to be associated with depleted carbohydrate reserves due to excessive cropping of young grapevines (Gladstones 2004). However, evidence as to the cause of the condition is indirect and based on recovery following improved water and nutritional regimes and, by inference, improved carbohydrate status. F. Parasitism of Perennial Carbohydrate Reserve-Bearing Organs 1. Fungi. The trunk-wound-invading fungus Eutypa lata spreads slowly through xylem vessels, apparently utilizing trunk and stem starch reserves in characteristic V-shaped sectors delimited by ray tissue. Gradual spread of the fungus leads to a characteristic dieback of perennial parts accompanied by shoot stunting and, eventually, failed budbreak and death of the entire plant (Rolshausen et al. 2008). 2. Phylloxera. The root-feeding insect grape phylloxera (Daktulosphaira vitifolii), an aphidlike parasite of grapevines, is one of the most devastating pests of Vitis vinifera and its cultivars. Its high reproductive rates sustain large populations that inhibit root and shoot growth, causing grapevine decline over a number of years and eventual death. Fleshy galls,
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known as nodosities, induced by phylloxera on primary roots by swelling of the root cortex, accumulate starch and appear to function as feeding reservoirs (Kellow et al. 2004). Nodosity weight is positively correlated with content of starch, sugar, and proline (Du et al. 2008). Stunted spring shoot growth is indicative of depleted carbohydrate reserves but could also be due to lack of other organic or inorganic nutrients. Symptoms accompanying decline are consistent with depletion of reserves, but secondary invasion by soil-borne pathogens may also contribute. The effect of phylloxera on grapevine dry biomass is exacerbated by water stress. In container-grown grapevines, Bates et al. (2001) found that phylloxera alone reduced annual dry matter accumulation by 21%, nd water stress alone by 34%; combined, the reduction was 54%. 3. Nematodes. Soil-borne nematodes of several species are parasites on grapevine roots and cause growth decline in susceptible cultivars. Root knot nematodes, among the most common parasites of grapevines, generally induce only minor localized accumulation of starch in plant roots, although they do create specialized feeding sites. Inoculation of potted grapevines (‘Thompson Seedless’) by the root knot species Meloidogyne incognita, a gall-forming nematode, increased total carbohydrate in roots by ca. 36% and decreased root dry weight by 18% (Kesba and Al-Sayed 2005). Shoot growth and fruit-bearing capacity of susceptible grapevines is progressively reduced in nematode-infested vineyards (Cirami et al. 1984). As with phylloxera, grapevine responses to nematodes are consistent with depletion of carbohydrate (and other) reserves.
VI. VITICULTURAL MANAGEMENT OF CARBOHYDRATE RESERVES In foregoing sections, we have identified the key processes involved in the assimilation, accumulation, and utilization of carbohydrate reserves in grapevines. In this section, we consider how viticultural practices interact with those processes to elicit responses sought from cultivation and examine the role of carbohydrate reserves within the context of grapevine “balance.” A. Impact of Viticultural Practices on Carbohydrate Assimilation, Utilization, and Net Reserves The phenological stage of seasonal growth and development of grapevines is principally under genetic regulation and therefore an obvious,
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and generally well-identified, temporal determinant of viticultural intervention. It is also well recognized that growth and fruiting responses are generally conditioned by environmental factors, together with inherent capacities for photoassimilation and growth. However, in general, carbohydrate reserve status at the time of intervention is not commonly integrated with viticultural protocols. In particular, we highlight evidence that points to carbohydrate reserve status as a principal determinant of those responses. 1. Pruning and Fruit Bearing. In grapevines, pruning, which is the annual removal of much of the previous season’s shoot growth and hence retention of only a portion of the annual regenerative organs—the primordial shoots (buds)—is a primary limiter of fruit bearing but results in enhanced development of the buds that are retained and those inflorescences that they bear. In addition to fewer shoots per vine, responses to pruning include prolonged shoot growth, reduced photoassimilation capacity (measured as leaf area per vine), and less seasonal accumulation of carbohydrates in canes (Winkler 1929). Spur pruning (removal of all but several of the most basal buds on selected canes) of mature, field-grown grapevines (‘Muscat of Alexandria’) reduced the starch concentration in the basal portion of canes during dormancy compared with nonpruned vines (from which some inflorescences had been removed). Lower reserves in the canes at budbreak were associated with the slower development of the new shoots. As noted previously, after normal spur pruning (‘Monukka’), the total weight per vine of nonstructural carbohydrates remaining was only 30% that of nonpruned vines. Winkler (1929) also showed that normal pruning induced a decrease of ca. 28% in total nonstructural carbohydrates (on a dry weight basis) in the basal portion of canes at anthesis. Based on greater ratios of shoots to the weight of vines at the start of the season, and lower leaf-to-shoot ratios, of normal and severely pruned vines, he posited that in early summer, the active shoot growth and smaller leaf area of severely pruned vines combine to accentuate the draw on carbohydrate reserves, thus impairing the developmental nutrition of inflorescences and causing poor pollen germinability and fruit set in some cultivars. Subsequent studies have borne this out. With less fruit to nourish, shoots of cultivated vines in this situation generally become rampant, creating poor canopy conditions for floral initiation and contributing less to carbohydrate reserves (Winkler 1929; Bindra and Chohan 1976; Bains et al. 1981), thus establishing seasonal cycles of excessive vegetative growth and diminished fruit bearing.
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Winkler also considered that pruning-induced prolongation of shoot growth into the ripening period created competition for nourishment between the ripening fruit and restoration of reserves (Winkler 1929, 1931). After several seasons of normal or severe spur pruning, this becomes evident in the lower nonstructural carbohydrate concentration in the basal portion of 1-year-old canes and shoots but less so in the trunk or roots (Winkler 1929; R€ uhl and Clingeleffer 1993). Minimal Pruning. Minimal pruning—the practice of allowing grapevine shoots to proliferate from season to season without pruning, save for occasional, minor trimming to prevent foliar contact with the ground— was essentially characterized in terms of seasonal growth and carbohydrate relations as the nonpruned control treatments in the pruning experiments of Winkler (1926, 1929) noted previously. The practice was introduced to Australian viticulture in 1983 to reduce production costs (Clingeleffer 1983a) and has subsequently attracted interest elsewhere (Carbonneau, 1991; Pool et al. 1993; Howell 2001; Intrieri et al. 2001; Weyand and Schultz 2006). Non- or minimally pruned grapevines typically have greater leaf area per vine, earlier seasonal canopy development, smaller inflorescences, a greater proportion of flowers that set fruit, and a greater number of bunches and berries than vines that are pruned (Winkler 1926; Clingeleffer 1983a,b). In his experiments, Winkler also included a treatment whereby, before anthesis, he removed those inflorescences “in excess of what was thought necessary for a good crop of fruit” (a practice he originally considered impractical in commercial production although harvesting machines have since been used to remove a proportion of the fruit several weeks after anthesis). In warm areas with long seasons, higher total fruit bearing associated with minimal pruning often may be sustained (without partial inflorescence or fruit removal), but evidence suggests that in cool regions with short seasons and the extended ripening period associated with higher fruit loads, the normal seasonal restoration of carbohydrate reserves is incomplete and maximal fruit loads cannot be sustained. Biennial bearing and, in severe cases, triennial bearing are typical responses to excessive fruit bearing in grapevines (Intrieri et al. 2001; Goffinet 2004). The condition is encountered in lightly or minimally pruned vines (Intrieri et al. 2001), particularly late-ripening cultivars in (but not confined to) cool locations. It is almost certainly associated with depletion of carbohydrate reserves, as inferred from carbohydrate stressinducing defoliation treatments that induce a similar condition (Holzapfel et al. 2006; Smith and Holzapfel 2009). In cool climate conditions at Fredonia, New York, throughout the season, phloem starch
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concentration in 1-year-old canes was not much affected by pruning; however, minimally pruned vines had much lower starch concentration in cane xylem than those that were pruned, except for several weeks after anthesis, when starch concentrations in both were at seasonally minimal levels and similar. From budbreak to leaf fall, phloem sucrose concentration showed a similar, pruning-related trend to that of xylem, but during dormancy the levels were similar (Goffinet 2004). In cool conditions at Geisenheim, Germany, Weyand and Schultz (2006) compared the carbohydrate reserve status of aboveground parts of severely pruned (‘Riesling’) vines (19 buds per vine) with that of similar vines that had been minimally pruned for three seasons. At most samplings over the next three seasons, they showed that minimally pruned vines had lower concentrations of total nonstructural carbohydrates, particularly in 1and 2-year-old wood (phloem and xylem aggregated) at leaf fall. Balanced Pruning. Partridge (1925) considered that achieving maximal ripe fruit without depressing vegetative growth represented “balance” and proposed that pruning weight be used as an indicator of the upper limit of the vine’s capacity to produce and ripen a crop in the following season. He introduced, and Shaulis later modified, a system of balanced pruning whereby the number of buds retained at pruning—potentially determining the following season’s shoot number and fruit load—is based on the previous season’s shoot growth, as measured by the weight of prunings (Shaulis 1948; Shaulis et al. 1953). However, although the approach uses the weight of prunings as an indicator of future grapevine growth capacity, it appears likely that lack of sufficiently close relationships with carbohydrate reserves, a fundamental determinant of seasonal growth and fruiting capacity, limit its usefulness. In summary, pruning subsequently reduces carbohydrate reserves in perennial organs, but this viticultural intervention directs their utilization to the nutrition of a limited number of primordial shoots early in the season (between budbreak and anthesis) to enhance inflorescence development. After anthesis, fruit development is enhanced by the greater proportion of canopy leaf area to fruit. However, reduced foliar development caused by pruning creates competitive physiological imbalance between carbohydrate distribution for fruit development and seasonal restoration of reserve carbohydrates that do not occur in the natural (nonpruned) state. Those imbalances appear to be readily reconciled for lightly pruned, and hence more heavily fruit-bearing, grapevines in warmer climates (e.g., in California’s Sacramento Valley [Winkler 1929] and Australia’s Murray Valley [Clingeleffer 1983b]) where conditions favor postharvest photoassimilation and restoration of shoot carbohydrates.
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In less favorable conditions (i.e., short growing seasons and short postharvest photoassimilatory periods) or where seasonal or cultural contingencies occur, the imbalance may not be reconciled without removal of flowers or immature fruit (Clingeleffer 1993; Pool et al. 1993; Sommer et al. 1993; Intrieri et al. 2001). From this perspective, pruning is essentially a means of regulating the distribution of carbohydrate reserves and the forgone fruiting capacity is a trade-off necessary in some climatic circumstances to ensure that the carbohydrate assimilation capacity of the grapevine is directed at fruit ripening and restoration of reserves to sustain the seasonal cycle. 2. Defruiting (Bunch Thinning). This practice is a means of ensuring adequate nourishment (carbohydrate and mineral) and hence enhanced ripening of the retained fruit (Winkler 1926), promoting vegetative growth (shoots and roots) (Winkler 1926), and avoiding alternate bearing (Intrieri et al. 2001) or vine death from overcropping (Weaver and McCune 1960). Each of these responses has been shown to be a result of relieving carbohydrate stress or improving the carbohydrate status of the grapevine (Weaver and McCune 1960). Responses to defruiting practice depend on the stage of reproductive development when fruit is removed, the total fruit load, the proportion of fruit removed, the carbohydrate status of the vine, and the size of the vine. Weaver and McCune (1960) showed that reducing the fruit load from 99 to 57 kg per vine (‘Alicante Bouschet’) by defruiting several weeks before veraison increased the total starch and sugar reserves in the shoots and roots in the following winter by ca. 30% and 43%, respectively. A condition known in Australia as ‘Doradillo decline’, in which vines of this very lateripening, high-yielding cultivar die prematurely, has been attributed to inadequate restoration and gradual depletion of carbohydrate reserves over several seasons (W. J. Hardie, pers. comm.). In ‘Semillon’, a generally lesser fruit-bearing cultivar, grown under favorable conditions, removal of all fruit at the inception of ripening for two successive seasons increased the concentration of carbohydrate reserves in vine roots by 21% (Table 3.3). Bains et al. (1981) found low carbohydrate concentrations in shoots and canes of grapevines (‘Anab-e-Shahi’) that had become devitalized by heavy fruit bearing. These responses to defruiting indicate that fruit bearing utilizes carbohydrates that might otherwise contribute to reserves. In addition, studies using radiolabeled assimilates provide evidence that ripening fruit may draw on carbohydrate reserves, particularly when photoassimilation is limited by factors such as defoliation (Candolfi-Vasconcelos et al. 1994; Koblet et al. 1996).
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There is generally an inverse relationship between fruit load and ripening rate (Weaver and McCune 1960), and hence harvest date, through which fruit load determines the duration of photoassimilation after harvest and pre–leaf fall and hence the capacity for restoration of carbohydrate reserves. 3. Root Pruning. Severance of grapevine roots by plowing, deep ripping, or with specialized cutting tools is sometimes used to limit vegetative growth (Dry et al. 1998). Typical responses include reduced shoot growth rate and leaf development (Buttrose and Mullins 1968; McArtney and Ferree 1999) and reduced photoassimilation due to changed grapevine hydraulic characteristics (Smart et al. 2006). This practice is particularly effective (and at times destructive) at the break of dormancy, evidently due to the heavy dependence of shoot growth on carbohydrate reserves stored in the roots. Richards (1983) demonstrated a correlation between number of shoots and root tips. In soils that limit root growth, deep ripping also serves to remove that limitation and thus increase shoot growth as a consequence of greater root growth (Van Zyl and Van Huysteen 1987). 4. Cane and Trunk Girdling. Girdling (cincturing or ringing) involves the removal of a narrow ca. 5 mm annular band of bark (phloem) from around the cane or trunk leaving the xylem tissues intact. Under favorable conditions, regrowth of phloem tissue generally takes 4 to 6 weeks. Trunk girdling at anthesis increases fruit set and, in seedless table grape production, is often used (with gibberellin-induced flower thinning and berry size enhancement) to increase berry size. For seeded table cultivars, girdling is used later in the season to enhance fruit maturity (i.e., coloration and sugar concentration)—see Winkler et al. (1974) for a more complete account of this very old practice. Girdling reduces carbon assimilation rate and stomatal conductance (Kriedemann and Lenz 1972; D€ uring 1978; Hof€ acker 1978; Harrell and Williams 1987). Severance of phloem resulting from this practice temporarily prevents normal transport of sucrose to roots and lower parts of the grapevine. Consequently, the store of carbohydrates in acropetal stems and leaves is enhanced (Weaver and McCune 1959a; Roper and Williams 1989). Resultant enhancements in fruit development reveal a competing demand at that time for carbohydrate between fruit and perennial organs to meet current needs (e.g., root growth or reserve restoration). Where reserves are already low, girdling may preclude or delay root extension growth that usually takes place from anthesis. Although sustainable for many successive seasons in some viticultural environments, trunk girdling does
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have a debilitating effect, probably related to reduced photoassimilation capacity and disruption of normal reserve restoration, which precludes its use in some locations, notably those with limited soil water (Winkler et al. 1974). Goffinet et al. (2004) girdled canes of grapevines (‘Concord’) at weekly intervals from budbreak to anthesis. Responses were related to the carbohydrate status of the grapevines. In general, the earlier the girdling, the greater is the stunting of shoots and loss of flower clusters and flowers. The floral effects were absent in grapevines of high carbohydrate status but were accentuated in grapevines that had very low carbohydrate reserves due to defoliation or heavy fruiting in the previous season. The responses demonstrate the strong dependence of shoot growth and floral development on carbohydrate status during this period. 5. Gibberellic Acid Application. In table-grape production, gibberellic acid sprays are often applied at anthesis to reduce the number of flowers that set and shortly after (often also with trunk girdling) to increase berry size. Weaver and McCune (1959b) found that gibberellic acid application alters partitioning of photoassimilates in grapevines, but the mechanism for this remains unclear. Roper and Williams (1989) found that gibberellin application alone had little effect on leaf carbohydrate concentration but, when applied with girdling, may have offset abscisic acid– induced stomatal closure associated with that practice (D€ uring 1978). Gibberellins often stimulate a-amylase, an enzyme commonly associated with the degradation of starch in many plant species, but this has received little attention in woody perennials (Loescher et al. 1990). In many grapevine cultivars, application of gibberellic acid at anthesis leads, in the following season, to delayed budbreak or complete failure of buds to break. This response has been associated with rapid elongation and subsequent abscission of primordial shoots (Lavee and May 1997). Similar symptoms have been associated with highly vigorous shoots and high endogenous gibberellin levels (Bernstein 1969; Lavee et al. 1981; Dry and Coombe 1994). In both circumstances, gibberellins may well be involved in the premature mobilization of starch during the early stages of bud development, but this needs to be verified. 6. Partial Leaf Removal. Partial leaf removal (“leaf-plucking”), by either manual or mechanical means, is generally used in viticulture to increase exposure of developing fruit to improve compositional aspects and/or to improve ventilation of the foliar canopy, chiefly to avoid fungal diseases. Defoliation by this practice generally takes place after fruit set and is confined to the basal 1 to 2 leaves of each shoot, resulting in
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perhaps removal of 15% to 20% of the total leaf area. This practice, by reducing potential photosynthetic capacity, must rely on other sources of carbohydrates to avoid major perturbation in the carbohydrate status of the plant and attendant consequences in growth and fruit development. As noted previously, compensatory adjustment in the photosynthetic rate of retained leaves may, in the absence of fruit, accommodate the loss of up to 60% of leaves, but in the presence of fruit or under suboptimal photosynthetic conditions, some drawdown of carbohydrate reserves seems likely. The consequences of removing leaves supporting newly initiating and developing buds from late spring onward appears to have received little attention, although studies with radiolabeled carbon indicate that acropetal flow of photosynthate probably accommodates this aspect of partial leaf removal under most conditions. 7. Harvest Pruning Dried and Wine Cultivars. The severance of fruitbearing shoots at the time of fruit maturity, known as harvest pruning, is commonly used by raisin producers to accelerate desiccation and reduce susceptibility of fruit to wet weather–induced deterioration. A similar practice is used to desiccate grapes for certain wine styles. The practice typically reduces leaf area by up to 60% and prematurely so, by as much 12 weeks, in warm viticultural locations. Scholefield et al. (1978) showed that harvest pruning of ‘Sultana’ had no impact on the concentration (% residual dry weight) of either starch or sugars in the perennial organs in winter. Under the warm, irrigated conditions in which the vines were growing, compensatory photoassimilation by the remaining leaves (ca. 40% of initial total) may account for this result. The impact of the practice on the usual autumn growth of the trunk and/or roots (and hence residual dry weight) was not established in the study. However, previous field trials (May and Scholefield 1972; Scholefield et al. 1977) showed that harvest pruning treatments induced annual reductions in fruit of ca. 10% but without causing a cumulative deleterious effect when repeated annually for 10 years on the same vines. 8. Irrigation. Irrigation is widely used in viticulture, essentially to avoid consequences of severe water deficits on vine growth and development. Precisely scheduled water applications are now widely used in vineyards to control grapevine growth and development and to achieve water use efficiencies through the induction of water deficits over time or within the root zone. Kriedemann and Goodwin (2003) provide a comprehensive account of these approaches, both of which avoid severe water deficit stress and thus some of the consequent impacts on
3. DYNAMICS OF CARBOHYDRATE RESERVES IN CULTIVATED GRAPEVINES 25
50
(a) CHO Reserves (%DW)
193
(b)
40
20
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15
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10
10
5
CON Starch RDI Starch PRD Starch
Sugars Sugars Sugars
0
0
BB
A
V
M
LF
BB
A
V
M
LF
Fig. 3.9. Impact of irrigation strategies on carbohydrate concentrations in (a) roots and (b) trunks at key phenological stages in cv. Shiraz (Riverina, Australia). CON:,control, irrigation according to evaporative demand; RDI: regulated deficit irrigation; PRD: partial rootzone drying. The times of budbreak (BB), anthesis (A), veraison (V), maturity (M), and leaf fall (LF) are indicated. Source of data: S. K. Field and B. P. Holzapfel, unpublished.
carbohydrate reserves described previously. Seasonal impacts on carbohydrate dynamics have been observed (Fig. 3.9), which indicate that both approaches reduce carbohydrate accumulation, but longer-term impacts remain to be investigated. 9. Fertilization. Fertilizers are widely used in viticulture, particularly to replenish nutrients that are lost to vineyards by removal of grapes or by leaching from the root zone. Globally, nitrogenous fertilizers are among the most used and have well-known impacts on photosynthetic activity of grapevines (Williams and Smith 1985) and consequent growth. It is also well known that grapevines may become barren in association with excessive growth and that the condition may be induced by overfertilization, particularly with nitrogen (Winkler et al. 1974; Dry and Coombe 2004). While the onset of the condition may be attributable to excessive nitrogen, the physiological cause seems more precisely attributable to a nitrogen-induced carbohydrate deficiency or at least nitrogeninduced carbohydrate imbalance. For example, in shoots and canes of overvigorous, poorly fruiting, field-grown vines, Bains et al. (1981) found lower total nonstructural carbohydrate content and higher nitrogen content compared with shoots and canes of fruit-bearing vines. In further support of this suggestion, there is evidence that nitrogen application decreases the amount of total nonstructural carbohydrate in perennial organs at dormancy. For example, Xia and Cheng (2004) found
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that nitrogen (urea) applied to leaves of potted grapevines (‘Concord’) 3 days before leaf fall decreased the amount of carbon stored as total nonstructural carbohydrate and increased the carbon stored in proteins and amino acids. Using small, aeroponically raised, vegetative grapevines (‘Merlot’), Grechi et al. (2007) found that nitrogen-enriched vines had greater leaf area and dry weight but less total nonstructural carbohydrate whereas root growth and total nonstructural carbohydrates were enhanced in nitrogen-depleted vines. We have also found that postharvest foliar application of urea to potted grapevines (‘Shiraz’) elicits a similar response, chiefly in roots, by reducing the amount of starch and increasing nitrogenous compounds (S. K. Field, unpublished data). Impairment of fruiting associated with the condition includes necrosis of primary bud axes, and stems of inflorescences and fruit clusters at all stages of development; however, further research is required to determine whether nitrogenous derivatives or carbohydrate deficiency play a direct role in the necrotic responses. In contrast to these deleterious effects of nitrogen, at moderate levels of application, nitrogen had little effect on carbohydrate reserve status in 1and 2-year-old wood (Korkas 1994). Furthermore, even after high concentrations of nitrogen delivered in split applications prior to veraison for 3 years, Wample et al. (1993) (‘White Riesling’) found few significant effects on cane carbohydrate levels within that period. They concluded that “under otherwise good management practices of pruning, crop load, irrigation and rootstock selection there should be little concern regarding a detrimental influence of nitrogen applied before harvest on cold hardiness or carbohydrate reserves of grapevines.” In that study, excessive growth and fruit fruiting were avoided by balanced pruning, thus pointing to excessive pruning per se as the principal cause of carbohydrate: nitrogen balances within grapevines. Deficiencies of other nutrients directly related to photosynthetic rate such as phosphorus and magnesium (Skinner and Matthews 1990) are also likely to limit the seasonal replenishment of carbohydrate reserves. 10. Shoot Removal. Removal of whole shoots (deshooting, shoot thinning), usually prior to anthesis when shoots are less than 15 to 20 cm long, is used to control foliar density, improving light penetration and ventilation within vine canopies. Generally, nonfruitful shoots are selectively removed, but removal of fruit-bearing shoots also regulates fruit load. Shoot removal, as an intervention when grapevines are dependent on carbohydrate and other reserves, appears to direct reserves to the remaining shoots (including unopened buds after early or severe shoot removal)
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and in some situations leads to the nitrogen-associated reproductive disorders discussed in the previous section (Dry and Coombe 2004). Impacts of shoot removal on carbohydrate status in grapevines have received little attention. By limiting leaf area, this practice may reduce total photoassimilation and carbohydrate accumulation, although enhancement of light conditions and compensatory photosynthetic rates of retained leaves (see Section VI.A.6, “Partial Leaf Removal”) are likely. 11. Shoot Trimming. Trimming of shoots, generally to no less than 10 to 12 nodes, is used, often up to 6 times per season, in viticultural systems to confine vine canopies within various training systems to facilitate management. As for other viticultural practices that remove leaves, compensatory increases in the photosynthetic rate of remaining leaves (Hof€ acker 1977) may leave carbohydrate reserves unaffected, provided that the retained leaves are functional. Repeated shoot trimming has long been recognized as the cause of progressive decline of vine growth over several seasons under some conditions (De Castella 1893), presumably due to the depletion of carbohydrate reserves. However, the impacts of shoot trimming on grapevine carbohydrate relations of field-grown vines have not been determined directly and probably vary considerably according to vine health, phenological development, and environmental conditions. General impacts are inferred from responses of potted vines under controlled conditions and knowledge of seasonal carbon distribution patterns within vines (Hale and Weaver 1962). Between budbreak and several weeks after anthesis, while shoot tips and juvenile leaves remain “sinks” for photoassimilates, their removal appears to redirect carbohydrate reserves to growth elsewhere as evident in enhanced development of lateral shoots (Smith et al. 1988). Improvements in fruit set sometimes achieved by shoot trimming, topping (removal of 150 mm or more of shoot tip), or tipping (removal of 75 mm or less) during anthesis (see Coombe 1959 and references therein) have long been attributed similarly to redirection of photoassimilates (M€ ullerThurgau 1883). In some cultivars, for example, ‘Shiraz’, shoot trimming at that time induces primary bud necrosis (Dry 1986), presumably in response to imbalances in carbohydrate and nitrogenous derivatives also caused by the redirection of photoassimilates. B. Grapevine Balance Viticulturists generally aim to consistently produce grapes of highest possible ripeness-dependent qualities in greatest quantity within site constraints. In viticultural parlance, this invokes the concept of maintaining
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“vine balance.” Imbalances are associated with, on one hand, a large amount of fruit but failure of the fruit to fully ripen and, on the other, very little albeit well-ripened fruit. These conditions are often accompanied by inadequate or excessive leaf canopies, respectively, although environmental constraints alone may preclude some cultivars from bringing large fruit loads to ripeness. As most commonly perceived, balance infers an “ideal” fruit load (fruit mass per vine) or “fruit to wood” ratio (Gladstones 1992; Howell 2001). Recognizing the importance of leaves for fruit ripening, Ravaz (1930) proposed the ratio of fruit weight to pruning weight (pruning weight being a proxy for leaf area) (Ravaz Index) as a convenient retrospective seasonal indicator of equilibrium between fruit bearing and leaf growth. One obvious limitation of this approach is the implied equivalence of leaf area and photoassimilatory activity. Grapevine balance, expressed as fruit to pruning weight, essentially relates to a result of a seasonal imbalance between the reproductive and vegetative demand for photoassimilate, that is, the balance between two carbohydrate sinks or yields (see Partridge 1925), each dependent on carbohydrate reserves for initial development following dormancy, but ignores the total capacity of the grapevine to provide for those sinks and thus provides little guidance for achieving balance. Subsequent attempts to sustain an ideal equilibrium from season to season, based on the weight of prunings (e.g., “balanced pruning” or “pruning to vigor”) (see Section VI.A.1, “Pruning and Fruit Bearing”) have not been entirely satisfactory (Jackson 2000). Variability in bud fertility, unaccounted for by pruning weight, is considered a significant source of seasonal variation in fruit loads (Morris et al. 1984; Jackson 2000). However, carbohydrate reserve relations provide a more fundamental explanation of that variation. Carbohydrate reserves at leaf fall—as progenitors of carbohydrate (and other organic nutrients) at budbreak—are principal determinants of seasonal reestablishment and subsequent shoot growth and fruiting. From this perspective, we suggest that pruning weight, which is determined largely between budbreak and anthesis, is more appropriately viewed as a carbohydrate-dependent feature with only limited (if any) bearing on potential fruiting and growth. In support of this view, Clingeleffer and Krake (1992) found that the weight of 1-year-old shoots (‘Cabernet Franc’) was not well related to fruiting in the following season. Rather, they found more significant correlations between fruit load and the mass of old wood, and between the mass of old wood and total vine mass. These findings indicated that the total vine mass or old wood mass is a more appropriate indicator of reproductive capacity and signaled putative relationships to carbohydrate reserves in perennial organs.
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More recently, Bennett et al. (2005) identified close relationships between the concentration of carbohydrate reserves (after defoliation treatments) in roots and trunks at budbreak and floral development and fruiting, and grapevine capacity (estimated seasonal shoot and fruit dry matter production), in the cool environmental setting of high southern latitude New Zealand. We have found similar but quantitatively different, and generally less statistically significant, relationships in warmer conditions in Australia where the range of carbohydrate concentrations (after defruiting and defoliation treatments for two successive seasons) and yield per vine were up to 2 and 4 times greater, respectively (Fig. 3.10). In our studies, there was a very strong effect of site—related to soil water availability—which influenced relationships between floral development and carbohydrate status (Fig. 3.11). At the well-irrigated sites where carbohydrate reserves were greatest, the relationships were closest, whereas at the drier sites, correlations were nonexistent. These findings, and defoliation-induced changes in the Ravaz Index (Bennett et al. 2005), point to balance between reproductive and 26 24 22
r ² = 0.6059
Yield kg/vine
20 18 16 r ² = 0.1007 14 12 10 8 6 0
5
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35
40
Starch reserves (%DW) Fig. 3.10. Relationship between fruit yield and starch reserves in ‘Semillon’ (trunk &, roots ) during the preceding winter. Differences in starch concentration were induced by defruiting and defoliation treatments in the two preceding seasons. Source of data: J.P. Smith and B.P. Holzapfel, unpublished.
.
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B. P. HOLZAPFEL, J. P. SMITH, S. K. FIELD, AND W. J. HARDIE Flower number infloresence–1
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% Fruit-set
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(a) Site 1 y = 13.1 x + 191
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r 2 = 0.62
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y = 1.27 x + 46.5 r = 0.13
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y = 9.2 x + 201 r 2 = 0.32
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y = 2.62 x + 40 r 2 =0.47
y = 12.3 x + 69.1 r 2 = 0.64
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(g) Site 3 y = 10.1 x + 144
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r 2 = 0.32
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y = 2.12x + 18.9 r 2 = 0.29
y = 6.07 x + 26.5 r 2 = 0.47
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Fig. 3.11. Relationships between floral development and fruiting of grapevine (cv. Semillon) and starch concentration (% DW) in cordon (trunk branch) wood at leaf fall at four different sites. Location: Riverina, Australia. Vines at Sites 1 and 2 were adequately irrigated and received more water than those at Sites 3 and 4. Source: B.P. Holzapfel and J.P. Smith, unpublished.
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vegetative growth in cultivated grapevines as a manifestation of carbohydrate reserve status at budbreak and primarily its seasonal maxima at leaf fall. However, as carbohydrate reserve status is itself an equilibrium condition reflecting relative seasonal rates of photoassimilation and carbohydrate utilization (Fig. 3.2), these findings indicate that, in conditions where vine imbalances occur, they may be corrected by viticultural interventions that restore that equilibrium. Furthermore, as buds regenerate both photoassimilatory capacity and depletion of carbohydrate reserves during their formative stages, and because the development of those buds from budbreak is dependent on carbohydrate reserves in perennial organs, we venture that vine balance is ultimately a function of the number of buds and carbohydrate reserves at budbreak. This, we suggest, reveals the fundamental need for pruning in most, but not all, viticultural systems, depending primarily on environmental conditions. From consideration of pruning and fruiting effects, for each cultivar, there is a climate-driven balance between fruiting capacity (i.e., fruit mass) and carbohydrate reserve restoration capacity that must be achieved for successive cycles of sustainable production. Where fruit mass is excessive, delays in ripening in particular are likely to preclude seasonal restoration of carbohydrate reserves. Where fruit mass is too small, seasonal carbohydrate restoration is likely to be substantial, favoring vegetative growth in the following season. As carbohydrate reserves at leaf fall represent the net accumulation of the preceding season and are the potential resource for the following season’s accumulation, we suggest that grapevine balance, at least in relation to fruit load, is expressed, ideally, as the ratio of the mass of the season’s fully ripened fruit to the total carbohydrate reserves (or an organ-based, e.g., trunk or root, proxy thereof) at leaf fall.
VII. SUMMARY AND CONCLUSIONS Nonstructural carbohydrates accumulate as reserves in all organs of grapevines in quantities that vary temporally, both diurnally and seasonally, according to differences in rates of photoassimilation and utilization. Perennial organs (trunks and roots) accumulate most nonstructural carbohydrates and in seasonally maximal quantities at leaf fall, which are used to regenerate development of shoots (and inflorescences) following winter dormancy. Soluble sugar derivatives may also be involved in cold hardiness in aboveground organs.
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A large body of evidence demonstrates the fundamental role of carbohydrate reserves as a physiological buffer against seasonal contingencies associated with biotic and abiotic environmental conditions. That evidence also reveals that environment and most, if not all, viticultural management practices directly impact on the accumulation of carbohydrate reserves in all parts of the grapevine and prompts the observation that cultivation of Vitis essentially involves constraining Vitis cultivars in human systems. Sustaining those systems to meet human needs essentially relies on perturbation of inherent carbon relations of the species, as exemplified most vividly by pruning and other interventions to achieve an anthropogenically acceptable balance between fruiting and vegetative growth at specific locations within a broad range of environmental conditions. Responses in shoot and fruit development, and ripening, to perturbations in carbohydrate reserve status induced by pruning and defoliation indicate that the equilibrium in seasonal photoassimilation and carbohydrate utilization underlies the balance between fruiting and vegetative growth. These findings indicate that, in conditions where vine imbalances occur, they may be corrected by viticultural interventions that restore that equilibrium. Grapevine buds regenerate both photoassimilatory capacity and depletion of carbohydrate reserves during their formative stages. Because the development of those buds from budbreak is dependent on carbohydrate reserves in perennial organs, we venture that vine balance is ultimately a function of the number of buds and carbohydrate reserves at budbreak. This, we suggest, reveals the fundamental need for pruning in most, but not all, viticultural systems, depending primarily on environmental conditions. For each grapevine cultivar, there appears to be a climate-driven balance between fruiting capacity, that is, fruit mass, and carbohydrate reserve restoration capacity. For successive cycles of stable and sustainable production, a balance must be achieved regardless of the net seasonal carbon accumulation capacity of the grapevine. The ratio of the mass of the season’s fully ripened fruit to the total carbohydrate reserves (or an organ-based, e.g., trunk or root, proxy thereof) at leaf fall, emerges from this chapter as a potential indicator of vine balance and sustainable fruiting. However, in order to maintain vine balance, viticulturists need to understand the immediate and future impact of environmental factors and management practices on carbohydrate reserves. Key aspects and fundamental interactions that need to be considered—and due to systemic complexity, mathematically modeled— are identified conceptually within a dynamic capacitance model.
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4 Elderberry: Botany, Horticulture, Potential Denis Charlebois Agriculture and Agri-Food Canada Horticultural Research and Development Centre 430 Gouin Boulevard Saint-Jean-sur-Richelieu, Qu ebec, J3B 3E6 Canada Patrick L. Byers Cooperative Extension Service University of Missouri Springfield, MO 65802 Chad E. Finn Horticultural Crops Research Laboratory U.S. Department of Agriculture Agricultural Research Service 3420 NW Orchard Avenue Corvallis, OR 97330 Andrew L. Thomas Southwest Research Center University of Missouri 14548 Highway H Mt. Vernon, MO 65712 I. INTRODUCTION II. BOTANY A. Taxonomy B. Distribution 1. Sambucus canadensis 2. Sambucus nigra
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C. Habitat D. Morphology E. Reproductive Biology 1. Pollination 2. Fruit Ripening F. Plant Development III. HORTICULTURE A. Winter Hardiness 1. Sambucus canadensis 2. Sambucus nigra B. Site Selection and Preparation 1. Soil Preference 2. Site Preparation 3. Irrigation C. Orchard Establishment D. Fertilization and Mycorrhizae E. Pruning 1. Maintenance 2. Rejuvenation 3. Corrective F. Weed Control G. Pests and Diseases 1. Insects 2. Mammals and Birds 3. Fungal, Viral, and Bacterial Diseases 4. Abiotic Stress H. Harvest I. Yield 1. Sambucus canadensis 2. Sambucus nigra IV. PROPAGATION A. Selection and Breeding B. Seed Propagation 1. Seed Germination 2. Planting C. Vegetative Propagation 1. Hardwood Cuttings 2. Softwood Cuttings 3. Root Cuttings 4. Micropropagation V. USES A. Folklore B. Utilitarian C. Food 1. Chemical Composition and Nutritive Value 2. Toxicity D. Traditional Medicine E. Modern Medicine 1. Leaf 2. Flower
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3. Fruit 4. Antiviral and Antimicrobial Properties 5. Anthocyanins and Antioxidant Capacity F. Ecological Value and Ornamental Potential G. Markets and Production Costs H. Processing VI. CONCLUDING REMARKS LITERATURE CITED
I. INTRODUCTION The elderberry or elder (Sambucus spp.), in production or growing wild in the northern hemisphere, may have the widest range of applications of all small fruits. Members of the genus Sambucus have a multitude of uses, including riverbank stabilization and windbreaks (Paquet and Jutras 1996); wildlife food and refuge; ornamental, crafts, and games; versatile human food source, and multipurpose medicinal (Valles et al.2004). Although the scientific documentation related to elderberries has increased over the last two decades, few reviews have been published. Martin and Mott (1997) reviewed the selection, cultivation, and management of American elderberry for wildlife and habitat management. More recently, the ecology of the European elderberry in the British Isles was thoroughly reviewed by Atkinson and Atkinson (2002). Finally, Charlebois (2007) reviewed the medicinal properties of elderberries, some of which were already mentioned in Dioscorides’ Materia Medica, written around the first century CE. Despite a well-established commercial production in many countries of Europe and an increasing interest in North America, little attention has been paid to the horticultural aspects of this genus and its potential as a food and a medicinal crop. Recent works linking an antioxidant-rich diet to disease prevention (Prior 2003; Willcox et al. 2004; Scalbert et al. 2005; Zafra-Stone et al. 2007; Seeram 2008), along with the versatility of elderberry as a crop, a food, and a medicine, have generated a renewed interest in this genus. This chapter reviews European and American elderberries.
II. BOTANY A. Taxonomy American and European elderberries have been harvested by native people since before recorded history and have been written about around
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Table 4.1. Language
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Vernacular names of Sambucus nigra and Sambucus canadensis. Sambucus nigra
Sambucus canadensis
English
black elderberry, bour tree, bore tree, elder, common elder, European elder
French
arbre de Judas, grand sureau, haut bois, sambequier, sambuquier, samp^echier, seu, seuillet, seuillon, sureau, sureau commun, sureau noir, sus, suseau, susier
American elder(berry), bourtree, Canada elder, eastern elderberry, elderberry, common elder, sweet elder, pie elder, elder-blow, blackberry elder, Mexican elder sureau blanc, sureau du Canada, sirop blanc
Afrikaans Danish German
Hungarian Italian
Polish Portuguese Russian Spanish
Kanadese vlier almindelig hyld Flieder, memeine Holunder, Holunder, schwarzer Flieder, schwarzer Holunder fekete bodza sambuco, sambuco nero, sambuco nostrale, zambuco, zambuco arboreo bez czarny sabugueiro, sabugueiro negro, sabugueiro preto sau´co, canillero, can˜ilero, linsusa, sabuco, sabugo, sau´co blanco, sauquero, sayugo, yezgo
sabugueiro do Canada
sauco del Canada
Source: S anchez-Monge y Parellada 1980; Wunderlin and Hansen 2008; www. telabotanica.org/eflore/BDNFF/4.02/nn/60241/vernaculaire.
the world for centuries, leading to a plethora of vernacular names (Table 4.1). The generic name Sambucus is apparently derived from the Greek word sambuke or the Latin word sambuca, which designates either a kind of flute that was made out of elderberry twig (MarieVictorin 1935) or a small harp (Rich 1859). Members of the Sambucus are small trees, shrubs, or herbs (Fernald 1970). Since no definitive taxonomic DNA studies have been conducted, and because species of this genus are difficult to delimit based solely on morphological characteristics, no clear consensus has been reached about the exact number of species it contains. Depending on the author, it can range from 9 to 40 (Bailey 1930; Marie-Victorin 1935; Lawrence 1951; Elias 1980; Hickey and King 1981; Stang 1990; Bolli 1994; Dzhangaliev et al. 2003). Thus, it
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is not unusual to find some confusion on delimiting species, subspecies, and varieties in regional floras (Bailey and Bailey 1976; Brinkman and Johnson 2008) even in the scientific literature. Ourecky (1970) stressed more than 30 years ago the necessity of a taxonomic clarification of the genus Sambucus. Bolli (1994) recently proposed a revision of Sambucus in which the phylogenetic tree was simplified by submerging many species to the rank of subspecies. By emphasizing morphological similarities within the group, Bolli (1994) concluded that only nine species are reputed to be part of this genus. He also proposed giving the two most economically important members of the genus, the European elderberry (S. nigra L.) and the American elderberry (S. canadensis L.), the status of subspecies. According to Bolli (1994), they should be designated as S. nigra ssp. nigra (L.) R. Bolli (European elderberry) and S. nigra ssp. canadensis (L.) R. Bolli (American elderberry). Because Bolli’s work lacks molecular information, the scientific and horticultural communities have been reluctant to adopt the new terminology. According to the U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) germplasm resources information network (GRIN) (USDA 2008a), 14 Sambucus species are recognized, and the names S. nigra (European elderberry) and S. canadensis (American elderberry) should be used, a recommendation widely followed in the literature (European and Mediterranean Plant Protection Organization 2008; UDSA, ARS, National Genetic Resources Program 2008b) and used in this study. The results reported by Clarke and Tobutt (2006) in their study on microsatellite primers tend to support the idea that American and European elderberries are two different species. Furthermore, it should be noted that numerous authors, such as Yatskievych (2006), disagree with Bolli’s (1994) revision. The genus Sambucus is most often included with the Caprifoliaceae (Guangwan et al. 2008; Hu et al. 2008). Bolli (1994) asserted that it possesses enough distinctive characteristics to warrant the recognition of a new family, the Sambucaceae. Except for some rare cases (Gasson 1979; Gustafsson 1995), this proposal has not been pursued. However, the genus was recently withdrawn from the Caprifoliaceae and placed in the Adoxaceae (Backlund and Bremer 1997; Donoghue et al. 2001; Donoghue et al. 2003), an affiliation supported by plastid gene sequencing (Savolainen et al. 2000) but not supported by Fourier transform infrared spectroscopy analysis (Hao et al. 2007). The exact taxonomical position of the genus Sambucus is likely to be continually debated as new methods are developed and more specimens are submitted to genetic analysis.
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B. Distribution 1. Sambucus canadensis. The American elderberry is native to eastern North America, and fossilized seeds can be traced back more than 16,000 years (Kneller and Peteet 1999). It is found from Florida, 25 N (Deam 1924; Bailey 1930; Allen et al. 2002; Wunderlin and Hansen 2008), in the United States to the northern part of the Gaspe coast of Quebec in Canada, 49 N (Environnement Canada 2002), which marks the northern limit of its natural distribution. Experimental plots have been maintained in Normandin Qu ebec (USDA hardiness zone 2; see National Land and Water Information Service Agriculture and Agri-Food Canada 2000 for correspondence between the Canadian and the USDA hardiness zones), where the wild type and some cultivars grow well but the fruits barely reach full maturity due to a short growing season. It has also been distributed by humans beyond its native range and can be found in Central Mexico and most Mesoamerican countries, such as Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua, and Panama (Plant Gene Resources of Canada Agriculture and Agri-Food Canada 2007). Patches of S. canadensis can be found growing as far west as Manitoba in Canada (Hosie 1979) and Minnesota in the United States (Martin and Mott 1997; Small et al. 2004) and can be found up to an altitude of about 1,500 m (Little 1980). The distribution along the eastern coast of North America is probably limited by its relative sensitivity to salt (Hightshoe 1988; Griffiths 2006). Sambucus canadensis has been reported to grow in the Himalayas at an altitude of 2,200 m (Mehra and Bawa 1968). However, it is unclear from this paper if European elderberry was mistaken for American elderberry or if the specimens studied had escaped from culture. European elderberry has long been used as an ornamental plant in North America (Marie-Victorin 1935). It is also possible that the early settlers brought with them cuttings and seeds of European elderberry and that some might have become naturalized in North America. A thorough genetic analysis would be needed in order to validate this hypothesis. 2. Sambucus nigra. The European elderberry is widely distributed in Europe with an eastern limit near 55 E (Atkinson and Atkinson 2002). Distribution extends farther north than its American counterpart, reachen and Fries 1986). It has been ing 63 N in Norway (Lid 1979; Hult reported to grow to 470 m in the British Isles (Halliday 1997) but probably reaches higher altitudes elsewhere on the European continent and in North Africa (Atkinson and Atkinson 2002). European elderberry reaches its latitudinal and altitudinal limits where the mean October
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temperature is around 7 C, which is probably limiting for seed maturation (Atkinson and Atkinson 2002). It has been introduced in various parts of the world, such as North America, East Asia, New Zealand, and South Australia (Hult en and Fries 1986; Kabuce 2007). A detailed distribution map can be found in Atkinson and Atkinson (2002). C. Habitat American and European elderberries are usually found in open or semiopen areas and along habitat edges (Martin and Mott 1997) where conditions are suitable for seed germination and plant growth. Their seedlings compete poorly with more aggressive species (Hayes 1987) and thrive best in full sun or partial shade (Grime et al. 1988). Examples of such areas are along streams in floodplains (Schnitzler 1997), in wooded areas where they will take advantage of openings in the canopy (Hankla 1977), in abandoned farm fields, in disturbed sites, and along roadsides where they are sometimes used as a windbreak. European elderberry has been shown to be relatively light demanding (Kollmann and Reiner 1996). American elderberry can, however, be found under a closed canopy (Rossell and Rossell 1999). Elderberry does best with ample moisture and will grow in swamps and bogs and in transition zones between wetland and upland (Conner et al. 1990). In North America, elderberry is often found in roadside ditches that provide a moist environment and adequate light. It will thrive under poor drainage (Himelrick and Galletta 1990; McLaughlin et al. 2008), but will not tolerate long periods of flooding. Elderberry’s adaptation to a wide variety of climatic conditions has allowed it to develop an extensive distribution range. As with many plants, it is at risk in winter, after its chilling requirement has been met, when warm spells trigger deacclimation and the beginning of budbreak when freezing temperatures are still common. This can result in leaf death if the plant is subjected to subsequent severe frosts (Grime et al. 1988). In the southmost part of its range, American elderberry grows in areas with no definite winter season and where summer temperature can easily reach 40 C, and therefore it may not undergo a dormant phase. In the northern part of its range, the winter temperature can dip as low as 40 C. All exposed parts are then susceptible to winter kill, and the amount of snow cover will determine the extent of damage. Temperatures as low as 20 C down to root level have been observed in Quebec in a snow-free orchard resulting in some plant death; however, most of the genotypes evaluated survived with various levels of damage (D. Charlebois, unpubl.).
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American elderberry is sometimes mistaken for red elderberry (S. racemosa ssp. pubens (Michx.) House syn. S. pubens Michx.); the two share the same habitats in southern Quebec, but red elderberry ranges only as far south as Tennessee in the United States (Fernald 1970). The red elderberry flowers earlier than the American elderberry, with flowers appearing in April and May, at the same time as the leaves. It also has a much more pyramidal inflorescence compared with the generally flat-topped inflorescence of American elderberry. The berries of the red elderberry are red when ripe. D. Morphology The American elderberry is a deciduous, fruit-bearing multistemmed shrub or small tree that can reach up to 3 m tall in the northern part of its range and as tall as 4.5 m in more southerly regions (Elias 1980; McLaughlin et al. 2008). Exceptionally, plants can reach a height of up to 9 m (Maisenhelder 1958; Vines 1960; Hankla 1977; DeGraaf and Witman 1979) and up to 10 m in European elderberry (Atkinson and Atkinson 2002; Wilczyn´ski and Podlaski 2005). An elderberry seldom develops a spread of more than 3 m. American and European elderberries form shrubs with numerous straight canes growing closely together from the base where numerous branches arise, giving these plants their bushy appearance (Atkinson and Atkinson 2002). Certain cultivars may develop a main trunk from which shoots emerge a few centimeters above the ground. New shoots usually appear from second- or higher-order branching but sometimes can arise directly from the base as a reaction to low temperature (Barnola 1972) or removal of the aboveground part of the plant. As it reaches 20 to 30 years of age, European elderberry will stop producing branches from the base and assume a more treelike form (Bolli 1994). European elderberry can easily live up to 25 years (Atkinson and Atkinson 2002) but rarely more than 35 years (Wilczyn´ski and Podlaski 2005). The longevity of either cultivated or wild American elderberry is unknown but is assumed to be similar to European elderberry. The canes are weakly lignified, with the white pith in the center accounting for most of their diameter, and consequently are somewhat brittle; a heavy load of snow or ice may cause canes to break. Small lateral branches often arise late in the growing season; these usually die at the onset of winter (Metcalfe 1948). Because of this natural dieback, some annual maintenance (see Section III.E, “Pruning”) usually is required in spring with a positive effect on fruit production (DeGraaf and Witman 1979). The bark is light brown, yellowish, or grayish and covered with prominent lenticels (Hankla 1977; DeGraaf and Witman 1979; Foote
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and Joes 1989), and is more deeply furrowed and corky in European elderberry. The cone-shape buds are medium size and slightly pendulous (Harlow 1954). The leaves are stipulate, opposite, and odd-pinnately compound with 5 to 11 leaflets, usually 7 (American; Lawrence 1951) or 3 to 9 leaflets, usually 5 to 7 (European; Atkinson and Atkinson 2002). Leaves
Fig. 4.1. Flowering in American elderberry (Sambucus canadensis): (A) 4-year-old plants in bloom; (B) close-up of flower clusters.
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range in color from bright green to medium green and yellow, are from 10 to 30 cm long (Vines 1960), and are nearly hairless on the upper side but hairy on the underside, especially along the veins. Selections, particularly of S. nigra, have been chosen for their ornamental value. They have a range of leaf colors from lime green to deep purple and a range of dissection to the leaves such that many appear similar to the finely divided leaves of Acer palmatum Thunb. Leaflets are short stalked, finely serrated, lanceolate to elliptical in shape, from 6 to 15 cm (American) or from 3 to 9 cm (European) in length, and from 2.5 to 6 cm in width; the lower leaflets are frequently tripartite (Foote and Joes 1989). The petiole reaches 3 to 10 cm (American) or 3 to 4 cm (European) in length (Vines 1960; Radford et al. 1968; Atkinson and Atkinson 2002). The roots extend into the soil near the surface at a depth of some 20 cm. They are lateral, fibrous and fasciculate, and not extensively ramified. On 2-year-old plants from cuttings, roots may attain a length of over 2 m. E. Reproductive Biology Reproduction is sexual, by means of seeds that are dispersed by birds and mammals (Brinkman and Johnson 2008) eating the fruits and later regurgitating or defecating the seeds (Thompson 1981), and asexual, by root suckering, rhizomes, and rooting (layering) of procumbent stems where they touch the soil surface. Flower and the subsequent fruit clusters arise mainly on the terminal portion of 1- and 2-year-old canes (Stang 1990). The divergent stamens tend to prevent self-pollination (Robertson 1892; Marie-Victorin 1935; Hickey and King 1981). In southern Canada, flowering begins toward the end of June, well after the leaves have appeared, and continues through the first two weeks of July. In the United States, blooming starts in late April and also extends through July in the Carolinas (Radford et al. 1968). The date of full flowering is usually in mid-June in Missouri and a bit later, in late June, in the Pacific Northwest (Finn et al. 2008). Over its entire distribution range in North America, American elderberry’s main blooming period probably extends from June through August. A few new flower clusters usually appear sporadically throughout late summer and early fall (Maisenhelder 1958; DeGraaf and Witman 1979; Hightshoe 1988). In areas where no definite dormant season exists, such as Florida, year-round flower and fruit production can be observed (Cerulean et al. 1986). Because of this late flowering habit, and because they do not produce their floral primordia until shoot elongation has started in the spring (Philipson 1946), elderberry is rarely affected by late spring frost,
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even in the northern part of its distribution range. Thus elderberry is an excellent choice for both flower and fruit production. The flat-topped flower clusters, corymbs (Lawrence 1951) often described as cymes (Marie-Victorin 1935; Fernald 1970), can range from only a few centimeters up to 35 cm in diameter; the largest clusters are usually found on new canes. On unpruned plants, cluster size tends to diminish as the number of clusters increases (D. Charlebois, unpubl.; P. L. Byers and A. L. Thomas, unpubl.). Clusters are made up of 2,000 or more small (6 mm) creamy white flowers. Offshoots arising from old canes often bear small clusters of only a few flowers. The flowers, which are faintly perfumed in S. canadensis but more so in S. nigra, are complete (pentamerous) but contain no nectar gland (Marie-Victorin 1935); however, extrafloral nectaries are present in American (Radford et al. 1968; Fahn 1987) and European elderberry (Dammer 1890). In European elderberry, transpetal veins are absent (Gustafsson 1995). The ovary is inferior and may be trilocular, tetralocular, or pentalocular (Bailey 1930; Marie-Victorin 1935). 1. Pollination. According to Marie-Victorin (1935), the stamens of elderberries are so divergent that self-fertilization is virtually impossible. While some claim that two or more cultivars are needed for optimal fruit production (Way 1965; Bailey and Bailey 1976; Poincelot 1980; Grauer 1990), a planting of a single cultivar will produce good results. Extensive observations of isolated wild plants that consistently produce fruit would seem to further the claim that American elderberry is self fertile (P. L. Byers and A. L. Thomas, unpubl). Such observations cannot, however, completely rule out the contribution of a pollenizer within pollinator flight distance. Because the flowers do not have nectaries, they are attractive to pollinating insects seeking pollen only (Robertson 1892). Field observations made over 3 years in several orchards in Quebec indicate that insects probably play a minor role in the pollination process (D. Charlebois, unpubl.). This is surprising considering that elderberries have showy flower clusters, a characteristic usually associated with the coevolution of pollinators. American elderberry is among the plant species found in Florida that are not visited by apioid insects (Pascarella et al. 2001). A similar lack of interest from this insect group has also been observed in Quebec (D. Charlebois, unpubl.). However, Way 1981 stated that honeybees, as well as wind, are responsible for pollination in American elderberries. The exact determination of insect involvement in the pollination process is difficult, considering the confounding action of the wind and passive
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self-pollination (Vaissi ere 2005). In contrast, European elderberry is believed to be routinely insect pollinated (Grime et al. 1988). Observations made on wild and cultivated plants of various ages seem to indicate that wind and plant density probably are the most important factors responsible for successful pollination (Guilmette 2006; Guilmette et al. 2007). Elderberry pollen grains often are found in traps from various observatories (J€ ager 1989), indicating that they are easily carried by the wind. This contradicts observations made by Bolli (1994) suggesting that elderberry pollen grains would not normally travel much farther than the inflorescence from which they originate. In view of the likely importance of wind as a vector in elderberry pollination, planting density will have a measurable impact on yield, especially when the planting is young and the bushes are small, with few flowers. 2. Fruit Ripening. Elderberry fruits are considered berrylike drupes (Fernald 1970; Cram 1982; Brinkman and Johnson 2008) but are most often referred to as berries. When they appear, they are green, relatively compact, and oblong. As they ripen over a period of 6 to 8 weeks from July to September in most of the distribution range, they enlarge until they are spherical. They then gradually turn red and finally black with a hint of purple and a glossy appearance. The peduncles and pedicels can also turn red during the ripening process. Individual berries, which may range from 5.0 to 6.5 mm in diameter (Brindza et al. 2007), contain 3 to 5 oblong tan to yellowish one-seeded stones (Radford et al. 1968; Brinkman and Johnson 2008). Finn et al. (2008) reported individual ripe berry weights ranging from 46 to 135 mg with means of 81 to 90 mg across multiple cultivars in Missouri and Oregon. Larger fruits were observed in Qu ebec on wild-type and cultivars with individual ripe berry weights ranging from 70 to 186 mg (D. Charlebois, unpubl.) reflecting regional variations. If aboveground tissues in American elderberry are damaged or pruned, vigorous new shoots will arise from the root crown. These new canes flower a few to several days later and produce single fruit clusters that ripen 14 to 21 days later than those on secondary stems (A. Thomas et al., 2009). Individual fruits usually remain attached to their pedicels for up to several days after becoming fully ripe, allowing for timely harvest and processing. The stalks tend to bend under the weight of the ripe berries, and fruit clusters occasionally become detached from the plant by the wind or the weight of birds feeding on them (Bir 1992). In such a case, individual canes should be identified and the larger clusters used for flower production. Fruits from bushes grown in less than full sunlight, as is often the case with wild plants, usually
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ripen later than those in full sunlight (Hill 1983). Cultivars do not ripen at the same time (Koll anyi et al. 2005; Mathieu et al. 2008b); thus cultivar selection can be exploited to manipulate harvest window and maximize harvest efficiency. Elderberries go through important biochemical changes during ripening. Cultivars of American and European elderberries follow similar trends from fruit set to harvest. For instance, titratable acidity and total amino acid content decrease while total soluble solids, anthocyanins and phenols, and antioxidant capacity all increase (K€ unsch and Temperli 1978a; Kaack 1990a; Mathieu et al. 2007; Mathieu et al. 2008a,b). Such knowledge allows a more efficient harvest schedule and a better use of the fruits by the processing industry. The fruits of the native wild American elderberry not only ripen later than those of the various cultivars (Hayes 1984; Mathieu et al. 2008b) but also ripen less uniformly. This heterogeneity in the ripening process is attributable to a number of factors, including the age of the fruit-bearing canes, the amount of sunlight the fruit clusters receive, and possibly genetics. Berries on older canes that are exposed to the sun will ripen first. Uniformity of ripening is an important factor in elderberry cultivar development. The American and European elderberries are endozoochorous, as has been reported for S. ebulus L. (Czarnecka 2005). Because the fruits are eaten by a variety of birds and mammals (Brinkman and Johnson 2008; Stiebel and Bairlein 2008), it is expected that their dispersal can be over long distances (Czarnecka 2005) even in less favorable environments such as woodlands, where the light availability is not ideal for the optimal development of the species. F. Plant Development Because American and European elderberries occur naturally over wide areas, it is difficult to describe their development using universal temporal references. Both species are among the first woody plants to leaf out in spring. For example, leaf emergence in American elderberry can occur in late February in Missouri (P. L. Byers and A. L. Thomas, unpubl.) to early April in southern Qu ebec (D. Charlebois, unpubl.), while European elderberry will do so in February or March in the United Kingdom (Atkinson and Atkinson 2002). When both species were grown in the same environment in Oregon, S. nigra broke bud much earlier than S. canadensis and flowered over 3 weeks earlier (Finn et al. 2008). Despite widely different flowering times, fruit ripening is rather synchronous for both species, reaching full maturity in early August to
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mid-September, depending on where they are grown (Atkinson and Atkinson 2002; Mathieu et al. 2007; Finn et al. 2008; Mathieu et al. 2008b). Little information is available about the development of elderberries over their entire distribution range, and it is to be expected that these general patterns will vary to some extent. For example, in Florida, elderberries have sometimes been known to retain their leaves (Little 1980; Cerulean et al. 1986; McLaughlin et al. 2008) and to bear flowers and fruits all year (Little 1980), thus probably spreading harvest over a long period of time and negatively impacting production. Annual variations in weather patterns will also affect the date of occurrence and the duration of the various developmental stages, as described by Atkinson and Atkinson (2002). While Guilmette et al. (2007) demonstrated that flowering is independent of heat accumulation in American elderberry, full fruit maturity is likely to be delayed if unfavorable conditions occur (D. Charlebois, unpubl.).
III. HORTICULTURE The first report of American elderberry cultivation in North America dates back to 1761 (Ritter and McKee 1964). Either as an ornamental or as a fruit-producing plant, elderberries can be used singly, in groups, as hedges, as living fences or as screens (Galletta and Himelrick 1990). The use of elderberry in a variety of agroforestry production systems is also promising (A. Thomas et al., unpubl.). A. Winter Hardiness 1. Sambucus canadensis. The American elderberry can be grown from USDA hardiness zone 2 to 10. Zone 2 is harsher than that of the northern limit of its natural range, but even in this zone, American elderberry has vigorous vegetative growth and the bushes frequently grow to a height of more than 1.5 m (D. Charlebois, unpubl.). However, in areas with significant annual snow accumulation, the rather brittle canes tend to break under the weight of the snow. The plant will benefit from being carefully wrapped up with burlap or string in fall and probably will need corrective pruning in spring to remove broken canes. Fruit ripening can also be an issue in northern climates where the growing season is too short even for the most precocious cultivar to fully ripen the crop (D. Charlebois, unpubl.). Under such climatic conditions and considering the vegetative growth potential of the plant, flower production might be a better choice than fruit production.
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2. Sambucus nigra. According to Wilczyn´ski and Podlaski (2005), European elderberry is less sensitive to winter temperature than many other woody species. Its natural distribution range suggests that it is probably as winter hardy as the American species canadensis. Both species can, however, be cultivated in colder climates. However, S. nigra has performed poorly in Missouri (A.L. Thomas and P.L. Byers, unpubl.), and it is uncertain if this is due to winter or summer hardiness. Ornamental genotypes of S. nigra often are described as being hardy to USDA zones 5 to 7.
B. Site Selection and Preparation Although American and European elderberries are not demanding plants, care must be taken when selecting a location. For ornamental purposes, the tendency of this species to form thickets through suckering should not be overlooked, and sufficient space must be available. In commercial plantations, fruit production will be compromised in sites with less than full sun. For fruit or flower production purposes, a location away from woods and other obstructions should be selected in order to allow free air movement; to reduce the incidence of disease, insect, bird problems (Stang 1990); and to promote pollen dispersion. 1. Soil Preference. Elderberry can be grown on a wide variety of soils. Excellent growth and yield can be expected in organic (muck) soil. Mineral soil will also provide good conditions for elderberry production. Sandy soils, while capable of supporting limited growth and production, offer few nutrients and insufficient water retention. Elderberry can tolerate imperfect drainage; however, repeated flooding will reduce growth and productivity. Air temperature and rainfall had a significant effect on vascular cambium growth in S. nigra (Wilczyn´ski and Podlaski 2005). The impact of overly wet conditions will vary depending on when they occur; damage may be minimal if the plantation is flooded during dormancy. Growth begins as soon as the ground thaws (in the northern part of its distribution range) and ceases with the first frosts. An accumulation of water during dormancy will be much more harmful if it is accompanied by alternating cycles of freezing and thawing. Ice formation can cause serious injury to young cuttings and seedlings. An excess of water during the growing season, if prolonged, may cause asphyxiation of the roots, delayed growth, and reduced productivity and can encourage root-rot diseases and fungi, and even death. However, an excess of water of not more than
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a day or two is unlikely to do much damage. Elderberry plants respond favorably to planting on berms at sites with less than ideal soil drainage. While no systematic studies have been conducted to assess optimal soil pH for elderberry production, European elderberry has been shown to grow in soils with a pH ranging from 4.2 to 8.0 (Atkinson and Atkinson 2002). 2. Site Preparation. Seedlings and newly planted elderberry cuttings do not compete well if surrounded by other vegetation (Roper et al. 1998). However, allelochemicals from European elderberry bushes have been held responsible for important crop losses in Italy (D’Abrosca et al. 2001). In preparation for planting, perennial weeds should be killed, pH adjusted between 5.5 and 7.5 (Coastal Zone Resources Division 1978; Hightshoe 1988) if necessary, and tile drainage or berms installed if excessive field moisture has been identified as being a problem. While the elderberry’s adaptability to a diversity of sites makes it an attractive option for growers with sites that are not well suited for other crops, good agricultural practices will enhance production. Sites where strawberries, mint, alfalfa, potatoes, or tomatoes have previously been grown are not desirable, as those crops are frequently associated with the presence of Verticillium. Any practices designed to enhance soil fertility and organic matter content will be beneficial to the establishment and development of an elderberry plantation. Excellent results have been obtained on sites freed of weeds and sown with a mixture of slow-growing grasses and clover the year before planting (S. Mercier, person. commun.). When compared to bare soil, such ground cover prevents soil erosion, moderates soil temperature and moisture fluctuations, improves water penetration, and requires less maintenance by suppressing weeds. The use of plastic or organic mulches such as wood chips, sawdust, and bark is an attractive option to limit weed growth. Elderberries are shallow rooted, and the use of plastic mulch conserves soil moisture and promotes root growth near the surface of the soil. While such roots might be perceived to be at a greater risk of cold-temperature damage, data gathered over a 3-year period at Agriculture and Agri-Food Canada’s experimental farm in L’Acadie, Qu ebec, have not shown any negative impact on the growth or survival of elderberry bushes with black plastic mulch (D. Charlebois, unpubl.). 3. Irrigation. Elderberries possess an extensive, shallow root system that can take advantage of any nearby moisture. T€ okei et al. (2005)
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demonstrated that water uptake in elderberry was rather insensitive to soil water content and that transpiration was mainly governed by atmospheric conditions. When the cuttings are first planted, it is essential that they receive enough water to get them off to a good start. Hand watering may be useful in the absence of an irrigation system. The young cuttings should receive between 1.5 and 2.5 cm of water weekly. Warmer and drier sites probably will need additional moisture. Elderberries have done well when irrigated following the general guidelines for most perennial crop species—that is, 2.5 cm water per week during the growing season with higher levels during fruit ripening and times of drought. However, no research has been done to accurately determine moisture needs. The effectiveness of various irrigation systems has not been experimentally investigated for elderberry. While trickle systems are effective in Missouri (P.L. Byers and A.L. Thomas, unpubl.) and other production areas, systems may need to be adjusted in response to root system development as plants age. Elderberries are not very drought tolerant (Atkinson and Atkinson 2002), and drought will cause damage that may range from slower growth, yellowing of foliage or premature leaf fall, to the death of the bush. European elderberry tolerates moderate drought by keeping a low maximum leaf water conductance (Vogt 2001). While it is rated as highly vulnerable to cavitation and drought-induced embolism, it has developed survival strategies to compensate (Vogt 2001). Mulching and proper weed management are helpful in minimizing the adverse effects of an occasional shortage of water, but irrigation might be essential for commercial production of high-quality fruit in some areas. In Missouri, fruit ripening occurs in August and is usually accompanied by very hot, dry weather, which can cause rapid deterioration of fruit quality and yield if water is insufficient. In Mediterranean climates, such as in Oregon’s Willamette Valley, with almost no summer rainfall, irrigation is essential for elderberry production. C. Orchard Establishment A new plantation can be established from seeds, seedlings, or cuttings. One-year-old rooted cuttings are the type of stock that is most commonly selected, but older stock will also yield good results. The type of stock selected, its age, and consequently its size are all factors that will directly affect the cost. One-year-old stock raised in plug trays facilitates mechanical transplanting but does not establish as quickly as older and larger transplants. While 1-year-old cuttings are expected to produce a sizable crop as early as the second year in the field, seedlings will not do so until the third or fourth year (Bolli 1994).
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The genetic variability inherent to seed propagation is not desirable from a commercial production perspective but may be preferred in situations such as wildlife plantings, where genetic diversity is a consideration. In a breeding program, seedling populations are generated from which selections may be made for potential future cultivars. Seeds require stratification before they will germinate (see Section IV.B.1, “Seed Germination”). If bare-root seedlings/cuttings are used, roots should be soaked in water a couple of hours prior to planting (Martin and Mott 1997). When the rooted cuttings/seedlings are to be planted in bare soil, one needs only to open a furrow approximately 15 to 20 cm deep with a harrow or disc and place the plant material in it. Regardless of the type of stock, it is essential to ensure that each plant is planted upright with the root system completely buried. This precaution is particularly important in the case of plug cuttings that are at risk of being uprooted by frost heaving. The furrow may be left open to promote rainfall catchment. If the plantation is small with no more than a few 100 elderberries, a metal rod may prove to be a practical method of making holes to receive the cuttings or seedlings. A mechanical strawberry planter or the like may also be used if a large number of cuttings are to be planted. However, it is important to ensure that the cuttings are set at a depth slightly above their collar and that the earth is properly tamped down around them. No research on different planting dates for a single site has been conducted, but it seems that elderberries can be planted at any time of year, provided that they can be irrigated after planting. In general, planting during the dormant period yields the best results. Planting in the spring, even late spring, has produced excellent results in southern Qu ebec and Missouri. Planting late in the fall (in November) has reportedly yielded excellent results in southern Ontario (R. Geier, person. commun.). Since American elderberry is hardy up to zone 2, fall planting may be advantageous in areas with well-defined seasons by enabling growth to resume as soon as the ground thaws in the spring. Decisions on planting density should consider the increased growth in diameter of the bushes that will occur as the fruits mature and ripen. A common practice in commercial blueberry and primocane-fruiting raspberry production that should work with elderberry is to erect a simple t-trellis made from rebar and strung with baling twine or wire that catches the fruit-laden canes and keeps them from falling into the row middles. Appropriate pruning should enable the grower to keep the aisles between rows reasonably clear without adversely affecting fruit production.
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Under most of its natural distribution range, cuttings set 1.5 m apart or less will form a nearly solid hedgerow before they reach full production capacity; if they are set 2.0 m apart or more, each bush should be accessible from all around even when fully grown. Wider spacing ensures better air movement, which can reduce the incidence of fungal diseases but allows more weed growth between plants. Sambucus nigra bushes spread more than S. canadensis and usually require more space between them. Spacing between rows will depend on the equipment at the grower’s disposal (Kaack 1988). To determine row spacing, 2.0 to 2.5 m should be allowed for bush development, adding the width of the equipment that will be used to maintain the aisles. Roper et al. (1998) recommend 2.1 to 2.4 m between plants and 3.0 to 3.6 m between rows of American elderberries. To illustrate: Spacing cuttings 2.0 m apart in each row and leaving 4.0 m between rows will result in a maximum density of approximately 1,200 bushes/ha. D. Fertilization and Mycorrhizae In an English study, Atkinson and Atkinson (2002) found that European elderberry can grow in soils with a broad spectrum of nitrogen, phosphorous, and potassium content ranging from 18 to 354 mg/g, 71 to 192 mg/g, and 24 to 610 mg/g, respectively. Under favorable conditions, elderberries grow at an impressive rate. New stems may add nearly 2 m to their length in the course of a single year. Growth of this order requires large amounts of nitrogen (N). To meet the needs of an elderberry plantation, Craig (1978) proposed a simplified fertilization method: apply 0.10 kg of 10N-10P2O5–10K2O fertilizer for every year of the plant’s age, up to a maximum of 0.45 kg. Alternatively, KCl (potassium muriate) may be used and applied every year or every second year. Good results have been reported from an application of approximately 220 kg of KCl/ha every second year (R. Geier, person. commun.). Fertilizer should be applied early in the spring, around leaf-out time, but no sooner than budbreak. As with all perennial fruit crops, since phosphorus (P) moves so slowly into the soil, it should be adjusted prior to planting if a site is low in this element. Nitrogen can be applied in any form. When the cuttings are set out, all that is required is to apply the equivalent of 0.30 kg N by hand near, but not touching, the base of each cutting. Where the cuttings are being planted through plastic mulch, an equivalent quantity may be applied immediately before the mulch is laid down. In the second year, application of 0.60 kg N around each plant should be adequate. The fertilizer should be applied in strips in the case of elderberries planted on plastic
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mulch, as their roots will already have spread beyond the mulch. In subsequent years, a spring application of approximately 60 kg N/ha should suffice. Depending on how vigorous the bushes are, this may be followed by a second application of 20 to 24 kg N/ha in late May or early June. In accordance with Craig’s (1978) recommendations, the maximum application rate should not exceed 0.45 kg ammonium nitrate per plant per year. Yearly supply varying from 200 to 400 kg N/ha have been proposed for S. nigra (Strauss and Novak 1971; Groven 1975; K€ unsch and Temperli 1978b; Kaack 1988). For both species, planting density, vigor of the plants, and the age of the plantation will have a direct effect of N requirement. Elderberry roots associate readily with mycorrhizal fungi when treated with a commercial inoculant for trees (D. Charlebois, unpubl.); however, the effect of such an association has not been evaluated to date. Hyphae from unidentified fungi have also been observed in roots of wild and cultivated American elderberries. No effort was made to identify the species present or to assess their relationship (mycorrhiza, pathogen, or other). A few authors have reported the presence of vesicular-arbuscular mycorrhizae in European elderberry (Harley and Harley 1987; Grime et al. 1988; Atkinson and Atkinson 2002). E. Pruning Under normal conditions, individual elderberry canes usually die between the third and fifth year (Deam 1924). Pruning is essential to control plant growth, to remove dead or diseased branches, to stimulate growth of new branches and canes, and to promote fruiting (Stang 1990). 1. Maintenance. Maintenance pruning should be done every year to remove dead or broken branches and manage growth. Removing dead branches not only facilitates harvesting but also helps reduce the incidence of diseases caused by insects, fungi, or bacteria. Branches that are less than 30 cm tall often are removed, which facilitates passage of equipment and eliminates branches that produce fruit that is inefficient to harvest and often of lower commercial value. In some cultivars, such as ‘York’, the fruit load may be such that some branches will bend until they touch the ground. Problematic canes should be removed; ideally a better alternative would be to harvest the flowers from such canes and avoid overload. 2. Rejuvenation. Fruit yields will increase steadily during the first 3 years following establishment of cuttings. However, while the total
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quantity of fruit will increase, the fruit clusters will become smaller over that period (D. Charlebois, unpubl.; P.L. Byers and A.L. Thomas, unpubl.). Usually around the fourth year, productivity will decline due to a number of factors, with aging of the canes probably being the main one. Accordingly, the bushes should undergo some rejuvenation pruning in about the fourth year, or later if growth has been slow. In elderberries, inflorescences form mainly at the terminus of branches. The vigor of the branch will have a direct effect on the size of the fruit cluster. Less vigorous branches will produce small fruit clusters that will be among the first to ripen. As a rule, new shoots and 1-year-old canes bear large inflorescences that produce slightly larger berries, and those berries ripen usually less than a week later. A healthy elderberry bush will withstand extensive pruning without difficulty. Pruning it to ground level will cause it to send up numerous vigorous shoots. However, while this is the simplest of all methods, it can result in substantially lower fruit production in the year that the pruning is done. Alternatively, pruning to the ground can be done every other year. The impact of various pruning methods on plant characteristics and productivity was documented by Thomas (2009). The method that probably has the most positive impact on fruit production is the selective removal of wood that is more than 3 years old. Another advantage of this method is that pruning can be adapted to individual cultivars. ‘Kent’ and ‘Victoria’, for example, tend to form a well-defined trunk; for those cultivars, it is preferable to prune old branches right back to the trunk while leaving 2 to 9 branches that are 1 to 3 years old (Stang 1990). However, erratic branching can make it difficult to clearly establish the age of individual canes. ‘York’ does not usually form a well-defined trunk and sends up large numbers of new shoots; it should not be pruned in the same as ‘Kent’ and ‘Victoria’. ‘Scotia’ might be described as intermediate in terms of its ability to form a well-defined trunk. The next step, for all cultivars, is to prune back the lateral and terminal branches to enhance the rigidity of the plant. This is labor intensive and requires a high degree of familiarity with the cultivars on the part of the grower. If the plants are widely spaced and vigorous, and if they are being grown under favorable conditions, with good pest control, fertilization, and irrigation, more canes can be left unpruned. An intermediate approach is to prune all the branches to a height of somewhere between 60 cm and 1 m above ground level. This method is quick, does not entail any decision making about the age or number of branches, and can be mechanized. Provided enough old wood is left, this type of pruning will promote the development of shoots that will grow
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into vigorous flower-bearing canes. With some cultivars, new shoot production will be stimulated as well. 3. Corrective. In a dense elderberry plantation, water stress during or after flowering may cause fruit abortion. Pruning out nonfruiting canes is a way of minimizing the impact of such stress. Canes that are infested with cane borers or other insect pests may also have to be pruned out in order to limit any further infestations (see Section III.G, “Pest and Diseases”). All removed branches should be disposed of in such a way as to avoid spreading disease and insect pests and keeping the plantation clean. If branches may be diseased or insect infested, they should be burned. Simply shredding the pruned canes that have been left in the aisles is not sufficient to eliminate many insect pests that may be infesting them (Stokes 1981). However, from a practical standpoint, commercial elderberry growers often flail canes in the aisleway. F. Weed Control Elderberry plantations, especially new ones, should be kept weed free. During the establishment period, competition from other vegetation will adversely affect the growth and survival of cuttings and seedlings. Once the bushes have become well established, however, they become competitive. Plastic mulch may be a useful option for weed control within rows of elderberry bushes. A cover crop is useful in the aisles; a species that is an undemanding, slow-growing perennial that requires minimal mowing, water, and fertilizer, and one that provides a favorable environment for organic matter accumulation and reduces soil erosion by minimizing water and wind action should be selected. Proper site preparation before the elderberry cuttings are planted, including application of a nonselective postemergent herbicide, should serve to minimize weed growth until the selected ground cover has had time to become established. Once established, the ground cover will have to be mown frequently enough to keep the seedlings/cuttings clearly visible. Plant debris should be raked away from the elderberry plants in order to discourage rodents from overwintering and feeding on the plants (Martin and Mott 1997). Since elderberries are shallow rooted, mechanical activity in the orchard, including mowing, tillage, and harrowing, should be reduced to a minimum to avoid soil compaction and root damage. On small plantations, weeds may be eliminated by cultivation. Elderberries are considered a minor crop with the result that few herbicides are labeled for either pre-emergent or postemergent weed
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management. Nonselective, postemergent herbicides should be used very cautiously because the herbicide may be taken up by suckers emerging some distance from the parent plant, which will then show symptoms and be injured. G. Pests and Diseases 1. Insects. Few insect pests were identified in small elderberry plantings consisting of 240 four-year-old bushes in southern Quebec (D. Charlebois, unpubl.). However, some species have the potential for producing a measurable economic impact in larger-scale plantations. The currant borer, Ramosia tipuliformis (Clerck), attacks currants and elderberries (Pirone et al. 1960). Insects and mites that may be pests on elderberries include the elder shoot borer, Achatodes zeae (Harris) (Silver 1933; Buriff and Still 1972), of which the larvae feed on canes in which they hatch; the elder borer, Desmocerus palliatus (Forster), which in its adult stage eats elderberry pollen and leaves, and lays its eggs in canes near ground level; and Aphis sambuci L., common in Europe (Sansdrap 2000). Larval feeding by the elder borer causes the dieback of branches and sometimes the entire shrub (Pirone et al. 1960). Infested twigs should be pruned promptly and burned. Eriophyid mites (Eriophyidae) feeding on leaves (Schooley 1995) and flowers and causing flower abortion can significantly impact yield in the midwestern United States (Finn et al. 2008). Vaneˇ ckov a-Skuhrava (1996) reported that the eriophyid mite Epitrimerus trilobus (Nalepa) overwinters within and beneath leaf buds of S. nigra in the Czech Republic. However, very little is known about eriophyid mite species that may infest elderberry in North America, including their life cycles. The larvae of the cecropia moth, Hyalophora cecropia L.; the eastern tent caterpillar, Malacosoma americanum (Fabricius); the forest tent caterpillar, Malacosoma disstria H€ ubner; sawflies such as Langium atroviolaceum (Norton) (Eaton and Kaufman 2007) and Macrophya trisyllaba (Norton) (Amett 2000) in North America and Macrophya ribis (Schrank) in England (Atkinson and Atkinson 2002); the fall webworm, Hyphantria cunea (Drury); and the rusty tussock moth, Orgyia antiqua L., all eat elderberry leaves. Gall mites and the two-spotted spider mite, Tetranychus urticae (Koch), suck sap from the leaves. Sap beetles feed on the sap of the bush and juice from the fruits. Adult European snout beetles, Phyllobius oblongus L., eat the margins of leaves and buds of elderberry bushes while their larvae eat the roots. Potato flea-beetle, Epitrix sp.; green stink bug, Acrosternum hilare (Say); omnivorouslooper, Sabulodes aegrotata (Guen); grape mealybug, Pseudococcus
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maritimus (Ehrhorn); San Jose scale, Quadraspidiotus perniciosus (Comstock); and madrone thrips, Thrips madronii (Moulton), are all considered of minor importance (Pirone et al. 1960). Management strategies include hand removal, sanitation, and application of labeled insecticides at timely intervals. Care must be taken when using insecticides in order to avoid contaminating flowers (Guedon et al. 2008) or fruits. Tingle and Mitchell (1986) have shown that leaf extract from S. simpsonii was effective in reducing egg deposition from the tobacco budworm, Heliothis virescens (Fabricius). The insect repellent potential of European elderberry leaves has been known for centuries (Smith and Secoy 1981). It has also been reported for American elderberry leaves by Durand et al. (1981). According to Shahidi-Noghabi et al. (2008), a type 2 ribosome-inactivating protein confers European elderberry its insecticidal activity. 2. Mammals and Birds. American and European elderberries possess many features, such as fall ripening, small seeds, and short retention time on the plant when ripe, that are considered adaptations to maximize seed dispersal (Stiles 1980). Elderberries are considered to be fairly digestible (Short and Epps 1976). In some regions, mammals such as chipmunks, deer, rabbits, raccoons, squirrels, opossums, and woodchucks may eat elderberry leaves and fruits (Van Dersal 1938; Plummer et al. 1968; Hankla 1977). Some of these pests will even eat unripe fruits (Hankla 1977; Schaefer and Schmidt 2002). Browsing by mammals can sometimes be severe with serious reduction in yield, but often it is insufficient to seriously affect growth. An electric fence will keep deer out but will be ineffective against smaller animals. European elderberry leaves are thought to be toxic to mammals (Grime et al. 1988). Various farm animals will also feed on elderberries. Despite a claim made by Hankla (1977), no documented proof that elderberry vegetation can be fatal to wild or farm animals could be found. American and European elderberries are also attractive to birds (Martin et al. 1951; Wyman 1969; Rajchard et al. 2007; Brookes 2008; Stiebel and Bairlein 2008), and a number of species eat the berries (Martin and Mott 1997). The presence of amygdaline, a cyanogenic glycoside in the fruit, has no bird deterrent effect (Struempf et al. 1999). If not harvested, European elderberries are usually stripped of their fruits by early November (Atkinson and Atkinson 2002). Netting, while effective, is expensive to put in place and to maintain. Various bird-scaring systems are available, such as noise cannons and distress calls, but unless a grower is vigilant about managing the frequency and placement
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of the various bird alarms, they rapidly become ineffective. Birds of prey are the elderberry grower’s natural allies. Territorial birds like the eastern kingbird (Tyrannus tyrannus L.) can sometimes help discourage unwanted bird species in eastern North America. Trap crops may also be useful. Millet, rye, and wheat have been reported to produce good results in attracting birds away from elderberries. If these crops are harvested early, grain residue should be left on the ground and disposed of only after the elderberries have been harvested. The efficacy of this approach is limited with bird species that feed mainly or exclusively on fruits. Depending on the size of the plantation and the seriousness of the bird problem, it may prove simpler for growers to resign themselves to the loss of a percentage of the crop than to install a bird-scaring system. As a last resort, prompt harvesting of ripe fruits should be considered (Stang 1990). 3. Fungal, Viral, and Bacterial Diseases. The following pathogenic fungi have been reported on Sambucus species in landscape or fruit production uses (Pirone et al. 1960). Cankers. Cytospora leucosperma (Pers.: Fr.) Fr. [syn. Cytospora sambucicola Tehon & Stout], C. chrysosperma (Pers.: Fr.) Fr., Diplodia sp., Nectria cinnabarina (Tode) Fr., Neonectria coccinea (Pers.: Fr.) Rossman & Samuels [syn. N. coccinea Desm.], Sphaeropsis sambucina (Cooke) Sacc. Girdling of the infected twigs is usually followed by the death of its terminal portion. The infected material should be pruned and destroyed. Leaf-Spots. Ascochyta wisconsina Davis, Phaeoramularia catenospora (Atk.) [syn. Cercospora catenospora Atk.], Cercospora depazeoides (Desm.) Sacc., Cercosporella prolificans (Ellis & Holw.) Sacc., Phyllosticta sambuci Desm., Mycosphaerella sp., Ramularia sambucina Sacc., Septoria sambucina Peck. Infection is usually moderate requiring no particular intervention. Powdery Mildews. Erysiphe penicillata (Wallr.:Fr.) Link [syn. Microsphaera alni (D.C. ex Wallr.)], Erysiphe grossulariae (Wallr.) de Bary [syn. M. grossulariae (Wallr.) L ev.], Phyllactinia guttata (Wallr.:Fr.) Lev. [syn P. corylea (Pers.) Karst.], Podosphaera macularis (Wallr.) U. Braun & S. Takam [syn. Sphaerotheca humuli (DC.) Burrill]. Other Fungal Diseases. Thread blight caused by Corticium koleroga (Cooke) H€ ohn. [syn. Pellicularia koleroga Cooke] (Pirone et al. 1960;
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Hightshoe 1988); root-rots cause by Helicobasidium purpureum Pat., Phymatotrichum omnivorum (Duggar) Hennebert, and Xylaria multiplex (Kunze) Fr.; and wilt caused by Verticillium albo-atrum Reinke & Berthier have also been reported (Pirone et al. 1960). Verticillium wilt attacks weakened bushes and sometimes kills isolated canes, but as a rule the affected bush survives the infection. However, it is advisable to avoid establishing an elderberry planting on a site where a sensitive species, such as a member of the Solanaceae, has recently been grown. Puccinia bolleyana Schw. [syn Puccinia sambuci Arthur] have been reported on American elderberry (Kellerman 1904; Byers and Thomas 2005) and Hyphodontia sambuci (Pers.) J. Erikss [syn. Corticium sambuci Pers.] on European elderberry in northern Europe. No description of the symptoms was, however, provided by the authors. Proper spacing and alignment of the plants usually help reduce the appearance and spread of such diseases. Viruses and Bacteria. Elderberries seem to be particularly good hosts for viruses (T. Jones, pers. comm.). Viruses infect various elderberry species in many countries in Europe and North America (Jones and Murant 1971; Uyemoto et al. 1971 and references within; Mamula and Mili ci c 1975; Van Lent et al. 1980 and references within). Tomato ringspot and Cherry leaf roll viruses infect American elderberry (Jones 1972; OEPP/EPPO 1996). It is impractical to control the vectors for elderberry viruses (nematodes, leafhoppers, aphids etc.); therefore, the best approach to control is to plant virus-free, clean stock. Filippin et al. (2008) recently reported for the first time the presence of phytoplasma in S. nigra, but their presence was not correlated with any specific symptoms. 4. Abiotic Stress. Elderberry is not salt tolerant, an important point to consider if elderberries are to be planted along roadsides where salt is used in the winter, or if they are to be irrigated with poor-quality water. American elderberry tolerates air pollution and can be used as an ornamental in urban areas (DeGraaf and Witman 1979; Beaudry et al. 1982). European elderberry withstands various anthropogenic pollutants, such as fluoride and sodium (Heinrich and Schaller 1987), ozone (Davis et al. 1981; Kline et al. 2008), sulfur dioxide (Rachwal 1983), and various heavy metals, such as lead (Rachwal 1983; Novikova and Kosheleva 2007). However, ozone injuries have been frequently found in field-grown European elderberries in Poland (Godzik 1998) and in Ukraine in a closely related species, S. racemosa (Blum
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et al. 1988). Sambucus racemosa and S. mexicana have also been used as bioindicators for monitoring ozone (Campbell et al. 2007). Reduced growth will occur under deficient water supply, poor drainage, and soil compaction. Care must be taken to avoid exposure to herbicides and some plant growth regulators since reduced growth, leaf scorching, or death may occur from exposure to these chemicals (Marshall 1989). H. Harvest While mechanical harvesting is a possibility (McKay 2001) elderberries are not well suited for such a practice because the fruits do not separate readily from the pedicels. In the case of American elderberry, the crown is wide, spreading the catcher plates on currently available mechanical harvesters and causing considerable fruit to fall to the ground. While it is likely that elderberries could be mechanically harvested, modifications in training systems and in existing mechanical harvesters will be necessary. At present, most of the crop is harvested by hand. Between 25 and 40 kg can be handpicked in an hour (Sansdrap 2000). Extensive, structured pruning to enhance light exposure throughout the canopy will allow fruit ripening to be more uniform and will also increase harvest efficiency by fostering the formation of fewer but larger fruit clusters. The berries should be harvested when a majority of them are dark blue, almost black, in color. An individual plant can usually be harvested in two to three passes at 5- to 7-day intervals over a period of 2 to 3 weeks. Typically, the entire cluster is collected at harvest. This operation is more easily accomplished in the morning, when the peduncles are engorged with water and consequently tend to break more readily. The fruit clusters are collected into containers of capacity suitable to allow rapid cooling. Elderberries that are not frozen immediately should be refrigerated (Sansdrap 2000) and processed shortly after harvest, as fruit quality rapidly declines at room temperature. Considering their rather small size and lack of appeal as a fresh product (Skirvin and Otterbacher 1977), elderberries are unlikely to be sold fresh. Elderberries do not form a consistent abscission zone between the pedicel and the fruit, and many fruits tear and leak when removed from the cluster, making marketing of the fresh cluster impractical for anything more than immediate local sales. Much of the crop is frozen immediately after harvest, which facilitates long-term storage until processing. Alternately, the fresh fruits can be pressed and the resulting juice frozen.
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If the stems are to be removed before the berries are frozen, the fruit clusters are simply shaken rapidly over a screen that will allow the berries to fall through while intercepting the stems. Cleaning is done by dumping the berries into a container of appropriate size until it is half filled. Enough water is then poured in to cover them. The container is gently shaken, causing stems, leaves, green berries, and any insects that may have been gathered along with the berries to float to the surface of the water, while the ripe berries remain at the bottom. More water is then added, and all this unwanted material is poured out of the container. After this rinsing operation, the berries are poured out on to a screen, to form a thin layer. A fine water spray can be used to remove any sand and soil particles that may still cling to them. In addition, the berries are inspected at this stage, and any foreign bodies or unsatisfactory specimens are eliminated. After being left to drain for a few minutes, they may be packaged and immediately chilled and stored, either fresh or frozen. Removing the fruit from the clusters is difficult when the fruit is fresh but simple once they are frozen. After the elderberries are frozen, the stems can be removed readily simply by mechanical agitation of the fruit clusters over shaking wire mesh or a similar device, such as a blueberry destemmer. Fruit quality can then be evaluated and plant debris and below-grade fruits eliminated. The peduncles represent approximately 10% of fresh corymb mass. I. Yield 1. Sambucus canadensis. Yield data from wild populations are lacking, although fruit has been harvested for thousands of years by native peoples. In one study, Caisse (1998) measured the productivity of wild American elderberries located in the Acadian peninsula (New Brunswick, Canada). She reported very low yields, ranging from 0 to less than 250 g/plant. Considering the natural density of the plant over the studied area, this author evaluated the potential yield to be less than 12 kg/ha (0.012 t/ha). Under natural conditions, the yield is likely to show large annual variations owing to the lack of control over the production parameters. The natural low density of the plant and the lack of control over predators seriously limit the plant from reaching its full production potential in the wild. Even with these limitations, large quantities of American elderberry are harvested from wild plants in the Midwest U.S. (P.L. Byers and A.L. Thomas, unpubl.). Large quantities of European elderberries are also harvested from wild plants throughout Europe (Sˇisˇ ak 2006).
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In managed plantings, significant fruit production will not occur in the year that the cuttings are planted (Stang 1990). This juvenile (nonreproductive) period can extend to 3 years if seedlings are used (Bolli 1994). During planting establishment, removing flower clusters as they appear will encourage vegetative growth. Way (1965) estimated a production of about 6.7 and 8.3 t/ha on a good site. These values are in agreement with those of Skirvin and Otterbacher (1977) who estimated a production varying between 7.5 and 15.5 t/ha. In USDA hardiness zones 5 and 7, production of between 1 and 3 kg per bush was obtained from cuttings in the second year in the field (Finn et al. 2008). However, in hardiness zone 8 in Oregon, yields as high as 6 kg/plant were achieved the year after planting and nearly 13 kg/plant two years after planting (Finn et al. 2008). Average yield may amount to as much as 9 kg per bush in the second production year (third year in the field), peak at 11 kg the fourth year, and slightly decrease the fifth year if no pruning is performed (D. Charlebois, unpubl.). These yields are very close to those reported by Adams almost 100 years ago (Adams 1915). Unfortunately, increased fruit production is accompanied by smaller fruit clusters that results in higher harvesting costs. As the bushes age in subsequent years, productivity may be expected to decline gradually. Pruning to encourage vigorous growth is essential to keeping the elderberry plantation productive. Little is reported in the literature on the long-term productivity of American elderberry; plants in trials in Missouri remained productive for 7 years (P.L. Byers and A.L. Thomas, unpubl.). 2. Sambucus nigra. As with American elderberry, harvesting fruit from wild elderberry populations has probably been going on for thousands of years in Europe. In a survey conducted from 1999 to 2004, Sˇisˇak (2006) reported an average of 32.8 kg/ha of fruits collected from wild elderberries in the Czech Republic. In a study conducted between 1997 and 2003 in Poland, Wa zbin´ska et al. (2004) reported yields varying between 1.3 kg/bush for wild-harvested genotypes and 16.6 kg/bush for cultivated ‘Sampo’ and ‘Samyl’. Yield was dependent on site and cultivar with a 40% difference directly attributed to site. Kollanyi et al. (2005) reported yields varying between 5.2 and 23.0 kg/bush for various cultivars of S. nigra in another study conducted in Hungary between 2003 and 2004. Maximum yields for ‘Sampo’ and ‘Samyl’ were superior to those reported by Wa zbin´ska et al. (2004). The average yield for the wildgrowing European elderberry was much higher than that reported by Caisse (1998) for American elderberry, likely because the former was maintained under controlled conditions while the latter was evaluated in the wild.
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IV. PROPAGATION A. Selection and Breeding European and American elderberries are grown throughout large areas of Europe, northern Africa, eastern Asia, and North America. Their hardiness and attractiveness, as well as their ecological, ornamental, and commercial potentials, have spurred interest in developing cultivars that meet the demands of consumers. It is most likely that naturally occurring forms, such as viridis and laciniata (European and Mediterranean Plant Protection Organization 2008), or large-fruited types (Way 1965), have been used in the past to develop new cultivars. Efforts in cultivar development to satisfy the needs of the ornamental plant and commercial fruit industries (Kaack 1989a) go back no further than the early 20th century (Stang 1990) with a peak in the second half of that century (European and Mediterranean Plant Protection Organization 2008). Breeding programs conducted around 1920 in the United States by the New York State Agricultural Experimental Station in Geneva and around 1960 in Canada by E.L. Eaton (Agriculture and Agri-Food Canada, Kentville, Nova Scotia research station), developed interesting cultivars for fruit production still used today. The following are among the better-known cultivars: ‘Adams’, ‘Johns’, ‘Kent’, ‘Nova’, ‘NY21’, ‘Victoria’, ‘Scotia’, ‘York’ (Skirvin and Otterbacher 1977; Craig 1978). ‘Haschberg’, ‘Korsør’, ‘Samdal’, ‘Sampo’, and ‘Samyl’ are some of the better-known European elderberry cultivars. About 35 cultivars of European and American elderberries are described in the literature (Vines 1960; Wyman 1969; Bailey and Bailey 1976; Craig 1978; Krusmann 1986; Hightshoe 1988; Griffiths 1994; Hillier and Coomes 2002), and probably several hundreds have been evaluated. While European elderberry was dominating the market (Stang 1990), nowadays both species are about equally represented in the backgrounds of the commercial cultivars. In some cases, such as ‘Acutiloba’, ‘Aurea’, ‘Chlorocarpa’ and ‘Laciniata’, the relationship of the genotypes to the two species was unclear. Considering the extensive distribution range of both species, the information provided by nurserymen about growth, yield, and hardiness of any given genotype should be seen only as general information, and important differences are likely to be observed in the various hardiness zones. American elderberry has been described as a species that can vary in appearance by Deam (1924) and some rare, naturally occurring variants have been reported (Schneck 1880). Only a few cases of natural or induced interspecific Sambucus hybrids have been reported, but
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Small et al. (2004) believe that hybridization is widespread in this genus. Most known interspecific hybrids concern European elderberry (B€ ocher 1941; Winge 1944; Chia 1975; Nilsson 1987; Simonovik et al. 2007). Such hybrids are usually sterile and therefore of limited horticultural interest. Ourecky (1970) also mentioned a few cases of interspecific crosses involving S. canadensis and S. nigra from breeding programs. Published information on Sambucus concerning the available and potential parents for specific traits and information on inheritance patterns is scarce. Breeding objectives for elderberry include large fruit size, firmer fruit texture, large fruit cluster size, small seeds, self-fruitfulness, increased productivity (number and size of corymbs and fruit size), vigorous and strong canes, uniformity of ripening within and among clusters, attractive color (glossy, dark), better fruit and juice quality, increased nutraceutical content, resistance to shattering and diseases, immunity or tolerance to virus diseases, wider adaptation, and pendulous fruit clusters less prone to bird damage (Darrow 1975; Lee and Finn 2007; Kaack et al. 2008). The Danish breeding program is seeking plants that are low growing with strong upright shoots from the root or lower part of the bush, characteristics that improve harvest efficiency (Kaack 1989a). In addition to the characteristics just mentioned, the Missouri State University/University of Missouri development program is seeking plants with tolerance to a species of eriophyid mite that causes a significant economic impact. The usual practices of pollen collection, emasculation of the female parent, and controlled pollination are followed. Emasculated blossoms are best isolated from chance pollen before and after pollination; this can be accomplished by protecting the cluster with a paper bag. Fruit clusters resulting from controlled crosses must be protected from bird depredation. Fruit is harvested when all berries in a cluster are fully ripe. Germinated seedlings can be transplanted to individual containers and later planted into selection rows in the field. Seedlings frequently flower and fruit in the second season, allowing for rapid selection for a number of traits of interest. Advanced selections in the Missouri State University/University of Missouri program are further evaluated for three harvest seasons in replicated test plots (P.L. Byers and A.L. Thomas, unpubl.). Elderberries generally can be multiplied by seeds or one of these vegetative methods: layering; suckers; micropropagation; and softwood, hardwood, and root cuttings (Laurie and Chadwick 1931; Mahlstede and Haber 1957). Seedling production is usually not used to establish orchards for fruit production but is useful for producing large numbers of plants for wildlife habitat or in breeding work. Thanks to their vigorous vegetative growth of up to 2 m in a single year, the use of
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cuttings is the most efficient propagation method. In some situations, where it is desirable to produce large numbers of a specimen in a short period of time, propagation by cuttings may not be adequate. In vitro or micropropagation may be necessary in these instances. In vitro propagation also allows for meristemming or a combination of meristemming after heat therapy to eliminate viruses from the planting stock. Regardless of the source of material used, it will take between 3 to 5 years to attain full fruit production (Stang 1990). Sources of certified pathogen-free tested material are limited at present; as the elderberry industry develops, this may become a serious problem. Whether from seeds or from cuttings, appropriate procedures must be followed in order to produce certified pathogen-free material (European and Mediterranean Plant Protection Organization 2008). Although elderberry seeds, seedlings, and cuttings are commercially available, elderberry nurseries and distributors are uncommon, and care must be taken to ensure that cultivars remain true to type. Finn et al. (2008) have determined that there was definitely a genotype environment interaction for phenological, reproductive, and vegetative traits for a group of American elderberry genotypes grown in Oregon and Missouri. Their results suggest that, at least in these diverse environments, the performance of a genotype in one environment is not predictive of how it will perform in the other. This means that it is important to trial cultivars in the region where they will be grown to determine if they will be commercially viable. B. Seed Propagation A mature American elderberry plant may produce several hundred corymbs, each with up to 2,000 fruits containing from 3 to 5 seeds. A single plant may thus supply several tens of thousands of seeds each year. American elderberry produces between 79,000 and 511,500 seeds/kg (Vines 1960; Stiles 1980) with an average of about 105,000 seeds/kg (Hankla 1977). Extracting seeds from elderberries is a relatively simple matter, and it may prove advantageous for the prospective grower to obtain seeds from ripe berries harvested from healthy, productive bushes. The easiest way to extract elderberry seeds is to lightly mash the fruits in water with pectinase added to the slurry. In 24 to 72 hours, the skin and flesh will be completely degraded. Water should be added, and the remains of the flesh and skin and any floating nonviable seed poured off. The seeds should then be allowed to dry. This process avoids the risk of damage that a blender or food processor may inflict if not carefully managed. Seeds can also be extracted mechanically. If pectinase is
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unavailable, the ripe berries can be carefully pureed by hand or in a food processor or blender (Morrow et al. 1954); enough water must be added to ensure that the berries are reduced to a pulp, and then the seeds can be extracted. The processor or blender should be run long enough to separate the seeds from the pulp; depending on the number of berries and the quantity of water used, a few seconds should be adequate. Some seeds will be observed floating on the surface of the liquid. These are probably empty or unlikely to germinate and should be discarded. The pur ee can be strained through a sieve fine enough to ensure that the seeds, which are approximately 1 mm in diameter, will not pass through it. The residue should be rinsed with water several times and, if necessary, run through the food processor or blender again to eliminate the remaining fruit pulp. Filtration must be done after each rinse, and the seeds then allowed to dry. Finally, the seeds should be shaken through a sieve to eliminate any remaining residue. The fruits can also be crushed, dried, and later planted with minimal processing with good results (Brinkman and Johnson 2008). Seeds will remain viable for several years if kept in a closed container at a low temperature (4 C) (Young and Young 1992; Brinkman and Johnson 2008). As a rule, the fresher the seed, the higher the germination rate. Brinkman (1974) found that American elderberry seeds retain most of their viability after 2 years. Fresh European elderberry seeds are reported to have a germination rate of 62.5% following a stratification treatment (Clergeau 1992). The germination rate of various American elderberry cultivars varied between 40% and 60% (D. Charlebois, unpubl.). Rates as high as 70% and 95% have been reported by Davis (1927) and Adams (1927), respectively, with American elderberry seeds sown soon after collection. 1. Seed Germination. Elderberry seeds will not germinate readily, contrary to what Bailey (1930) reported. They contain a dormant embryo and thick but water-permeable teguments (Young and Young 1986; Martin and Mott 1997; Hidayati et al. 2000; Brinkman and Johnson 2008), and consequently require a period of stratification at low temperature. The extent of the pretreatment needed has been reported to vary considerably across the distribution range of the species (Bir 1992) and might not be necessary for seeds from southern sources (Dirr and Heuser 1987). Untreated seeds can take up to 2 years before germinating. While inexpensive and simple, this material yields poor results. Scarification with sulfuric acid can be used prior to the stratification treatment (Heit 1967; Hankla 1977; Young and Young 1986). This treatment weakens the teguments and enables the grower to omit the initial period
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of storage at room temperature. Barring the use of sulfuric acid, the following technique is successful. Seeds are placed in a sealed plastic bag containing a sterile and moist but not wet medium. Adding gibberellic acid to the watering solution increases germination rate (Hidayati et al. 2000). Peat moss is usually satisfactory, but sand can also be used. Sixty to 90 days at room temperature followed by cold (4 C) storage for approximately 90 days will yield good results (Cram 1982; D. Charlebois, unpubl.). After that period, the bags may be placed in light at room temperature until the seeds germinate. This method offers the advantage of selecting only viable seedlings but requires their manipulation during transplantation. Alternatively, seeds can be sown in late fall or spring directly on a raised bed at a density of about 100 seeds per meter and thinned as necessary. 2. Planting. Seedlings may be transplanted into plug trays containing a commercial potting mix. Direct exposure to sunlight should be avoided, and care must be taken to ensure that the potting medium is kept moist. A starter fertilizer for woody plants may be used, according to the manufacturer’s recommendations. Elderberries do not grow as well in pots as they do in the field and should be transplanted to their final location as soon as possible. When the seedlings have attained sufficient size, they may be transferred to the field. A good way to assess seedling development is to examine the root system. Depending on how well advanced they are, it may be advisable to keep them in containers for another year. C. Vegetative Propagation Elderberries are exceptionally well suited for propagation by means of cuttings. Mother plants for cuttings should be true to type and healthy. In particular, care must be taken to ensure the identity of mother plants, since many cultivars cannot be distinguished solely on morphological features of the vegetative parts, and their tendency to produce suckers sometimes can be a source of confusion in nurseries when cultivars are planted too close to one another. Cuttings can also be removed from wild plants when elite specimens are found or for breeding purposes (DeGraaf and Witman 1979). Once the planting is well developed, cuttings may be taken during maintenance pruning operations. Elderberries are easily propagated from hardwood (lignified cuttings, taken in winter), softwood (immature, succulent cuttings, taken in summer), root cuttings, or suckers (Stang 1990; Schooley 1995).
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1. Hardwood Cuttings. Hardwood cuttings commonly include 3 to 5 buds. In most cases, the taking of cuttings can be judiciously timed to coincide with the pruning of the bushes. Hardwood cuttings should be collected in November, after the leaves have fallen, to avoid the risk of harvesting material that has been winter damaged. Cuttings taken in the fall need to be stored properly to retain their quality until they are stuck later in winter or early spring. The cuttings should be placed together in bundles, set upright in coarse sand or peat moss, in which they are buried to half their height, and stored in a cold room or cellar (around 0 C). Cuttings can also be harvested in late winter or early spring, while the elderberries are still dormant, and stuck directly into propagation beds. If harvested in April or May (after budbreak), hardwood cuttings should be treated as softwood cuttings (see the next section) or set out directly in the field. If cuttings are taken in spring, the physiological condition of the canes cannot readily be determined, resulting in a variable percentage of successful cuttings. In very cold climates, the tips of canes may suffer winter damage. To address this problem, woody sections of cane, located several centimeters down from the apex, should be selected from vigorous canes. Soaking the bases of the cuttings in a solution of indolebutyric acid may be beneficial in stimulating rooting, although it is not essential. The cuttings are set upright in a trench, spaced between 7 and 10 cm apart, and covered with a medium, with the upper buds left protruding above the soil surface. The medium used should possess good water-holding capacity but without allowing excessive water to accumulate; for that reason, sand is often selected as the planting medium for field and greenhouse rooting. A media with 50% to 75% perlite and 25% to 50% peat works well in greenhouse environment. New roots will appear within the first 2 weeks and cease to emerge after about a month (Wilson and Wilson 1977). According to these authors, the presence of leaves is necessary for the production of roots. Another method is to lay down a strip of plastic mulch and push the cuttings into the soil through the plastic, approximately 15 cm apart, with 2 to 4 cm of cane protruding. Alternatively, they can be set in their permanent location as just described. The great advantage of this last approach is that the cuttings need not be transplanted; the disadvantage is that not all the cuttings will root, leading to gaps in the row. One way to minimize this problem when cuttings are in sufficient number is to place up to three cuttings at the same location and thin out successful cuttings that might be in excess. During the 2 months after the cuttings have been set out in the field, they will produce foliage, followed by the appearance of new
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roots. The planting medium should be kept moist during this period. Growth of the new canes may be anywhere from 15 cm to 100 cm in the first year. If larger plants are required, the cuttings may be kept under these conditions for an additional year. Given favorable weather conditions and a suitable location, the success rate may be in excess of 95%; under more adverse conditions, such as a dry year, the rate may be as low as 20%. 2. Softwood Cuttings. Softwood cuttings are taken during the growing season and usually comprise the terminal portion of a new green branch. A softwood cutting containing between 2 and 3 nodes will normally be satisfactory. Each node bears 2 opposite buds in the axils of the compound leaves. The first cutting taken from a cane ends in a nonwoody portion that is frequently green, consists of a number of telescoped internodal spaces, and may include flower buds. Ideally, the basal end of the cutting should not be more than 10 mm in diameter, in order to maximize rooting. Cuttings larger than this tend to root less satisfactorily, and their abundant foliage makes them more sensitive to rot. They should always be taken from bushes that are healthy and vigorous. The optimal period for softwood cutting is between the time the bushes are at the flower bud stage and the end of their flowering or the beginning of fruit set in southern Qu ebec and in early summer before flowering in the central United States. In southern Quebec (USDA hardiness zones 4 and 5), that period extends from late June to late July; in Missouri (USDA hardiness zones 5 and 6), that period is late May to early July. As cuttings are collected, care must be taken to protect against overheating and desiccation. It is unlikely that taking too many cuttings from any particular bush might cause damage as elderberries are well able to withstand drastic pruning and only the ends of canes are used. Early removal of flower stalks on the parent plants may be one way to promote more vigorous vegetative growth. Techniques to improve rooting success of softwood cuttings include: avoiding desiccation or overheating of cuttings during collection; removing all but the base 2 leaflets of each retained compound leaf, which reduces transpirational loss of water during the rooting period; and providing intermittent mist during the rooting period. 3. Root Cuttings. Collect root cuttings in early spring before growth begins. Root segments that are 15 to 20 cm in length and 3 to 5 mm in diameter are ideal. Place root segments in shallow pots of sterile media, cover with 2.5 to 3.0 cm of media, and keep warm and moist. Each segment will produce at least 1 plant.
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4. Micropropagation. Elderberries can readily be propagated by means of in vitro culture, and the propagation medium may also be used for rooting (Brassard et al. 2004). Low mortality rates are observed during the acclimatization phase, and acclimatized plants adapt well to field growing conditions (D. Charlebois, unpubl.). Moreover, micropropagation is sometimes the only way to obtain virus-free material. In view of the cost of this propagation method and the technology involved, it is not within most growers’ reach. However, a number of commercial laboratories could propagate exceptional individual plants on a large scale in a short time on a contract basis.
V. USES Almost every part of the elderberry plant has some uses: fruits, flowers, leaves, roots, pith and bark (Vall es et al. 2004). Information related to human exploitation of Sambucus can be traced as far back as the Ancient Rome. Dioscorides (40–90 CE) mentioned the use of S. ebulus to color hair in his treatise De materia medica (Osbaldeston and Wood 2000). Pliny the Elder (23–79 CE) reported that numerous wind instruments and popguns were made out of elderberry (Grieve 1931). Report of the medicinal uses of elderberry flowers and bark were already mentioned in the 17th century by Agustı (1617). The elderberry is primarily valued as a food and medicinal plant, and description of such uses are part of the long history of the Native American people and European culture. These characteristics have been documented by Gunther (1945), Vines (1960), and Moerman (1998). The species nigra, in particular, has been the subject of many traditions, some of which are current to this day. While the Native Americans had a long history of using the native Sambucus species, the European immigrants quickly recognized the similarity between S. canadensis and S. nigra and then used it similarly for folk medicine. Because of the similarities between these two species, the information presented next is to be taken as applicable to either one. Where possible, the name of the species referred to has been indicated. A. Folklore Elderberries appear frequently in European (Chrubasik and Chrubasik 2008) and North American folklore. This is apparent from the numerous uses to which elderberries have been put through the ages. Duke (1985) and Moerman (1998) provide excellent surveys of this field. Elderberries
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have fueled numerous legends and superstitions. According to a Scots verse, the Christ would have been nailed to a cross made of elderberry (Mabey 1996). Grieve (1931) reported different sources alleging that Judas hanged himself on an elderberry tree. In Scotland, elderberries were often planted near old crofts and cottages to protect from witches (Vickery 1995). It is also believed to be imprudent to stand under the shade of an elderberry as its narcotic properties can put you to sleep (White 1876). An English saying states that English summer is not there until elderberry is in full bloom and that it ends when the berries are ripe (Grieve 1931). Elderberries have also caught the attention of numerous writers. In his play Cymbeline (ca. 1609), Shakespeare associated elderberry with grief (Grieve 1931). Probably the most famous reference to elderberry comes from the 1939 play Arsenic and Old Lace by the American Joseph Kesselring in which lonely old men are murdered by poisoning with a glass of elderberry wine laced with arsenic, strychnine, and cyanide. In the 1975 movie Monty Python and the Holy Grail this famous insult was coined: “Your mother was a hamster and your father smelt of elderberries.” More recently, we find Harry Potter, the well-known hero created by the English author J. K. Rowling, sipping a glass of elderberry wine in the company of his friends in the fourth novel in the series that bears his name. B. Utilitarian Leaves, flowers, but particularly berries have been used by North American and European people to produce dyes for a wide variety of objects, such as artifacts and leather (Stang 1990; Moerman 1998). The fruits give a brown dye, but using alum as a mordant gives a pale blue (Thompson 1969). The bark of elder can be used as a mordant as well as the source of a black dye when mordanted with iron (Thompson 1969). The flowers are still used by craftsmen to produce a yellow dye (Allen et al. 2002), and in the perfume industry (Durand et al. 1981). Leather was also tanned using tannin from the bark and the roots. Pigments from berries were used to produce a natural dye to stamp meat. Similarly, berries and leaves of S. simpsonii Rehder (syn. S. canadensis var. laciniata A. Gray) have been used to produce dyes for the wool industry (Smith 1993). Stems of American elderberry were used to make flutes, whistles, and spouts for collecting sap from sugar maple (Durand et al. 1981; Stang 1990). Twigs were also used to build pieces for looms (Durand et al. 1981). The leaves are said to have insect-repelling properties (Durand et al. 1981). Elderberry pith has long been used as
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an easy-to-cut support to prepare histological sections (Marie-Victorin 1935; Hickey and King 1981). More recently, S. nigra agglutinin extracted from the bark (Broekaert et al. 1984; Greenwood et al. 1986) has been used in numerous biochemical and histological studies dealing with various forms of cancer (Dall’olio et al. 1996; Lekka et al. 2006). Folk wisdom has discovered many uses for elderberries. Whistles, chanters, and pop-guns can be made of the young shoots after the pith has been removed (Vickery 1995). Large, hollowed-out stems were crafted into blowguns by the Houma for hunting and fishing and by many people to make medicine blowing tubes. The Seminole people used root bark as a ritual purification emetic after funerals and by their doctors after the death of a patient. Acjachemen Indians from California have been using S. mexicana branches to make clappersticks (Walker et al. 2004). The pith can be removed from the canes to turn them into reproduction sites for solitary bees, especially in the vicinity of alfalfa fields. C. Food Nearly every part of the American and European elderberries has some culinary use. The berries are used in the preparation of pies, jelly, punch, wine, or liqueurs. The flowers can be added to the batter used to make various items, such as pancakes, muffins, or waffles. The flower clusters are made into fritters. Elderberry flowers soaked in water with citrus make a delightful nonalcoholic cordial (Hibler 2004). Elderberry flower wine is a lovely pale yellow color and is reported to be delicious, and tea can be made from the flowers as well. The marinated flower buds are sometimes used as a substitute for capers (Lightfoot 1777; White 1876; Sansdrap 2000; Bubenicek 2002). The young shoots, when cooked, are similar to asparagus, although the green older parts are toxic. The pith from the canes can be used in soups as a thickener. The fruits were used by Native American tribes and settlers as food source and as a fermentable fruit (Allen et al. 2002). In Europe and in North America, a number of commercially available products contain elderberry juice or pur eed or dried elderberries. They are used as a food colorant (Zafrilla et al. 1998; Walker et al. 2006; Kammerer et al. 2007) and to enhance the nutritive value of some common foods. In particular, they are an ingredient in various juices, snack bars, condiments, and drinks. Europeans and Native Americans have long made wines, spirits, syrups, jellies, jams, and pies out of elderberries, and harvesting from wild bushes is still practiced today in many countries (Ghirardini et al. 2007; Łuczaj and Szyman´ski 2007).
252
Table 4.2.
D. CHARLEBOIS, P. L. BYERS, C. E. FINN, AND A. L. THOMAS
Nutritive values for various small fruits (content per 100 g fresh fruit).
Composition
Elderberry
Grape
Raspberry
Blackberry
Strawberry
Cranberry
Blueberry
Water (%) Energy (kcal) Amino acids (mg) Calcium (mg) Carbohydrates (g) Fat (g) Fiber (g) Iron (mg) Phosphorus (mg) Protein (N 6.25) Sodium (mg) Vitamin A (IU) Vitamin B6 (mg) Vitamin C (mg)
79.8 73 0.645 38 18.4 0.50 7.0 1.60 39 0.66 6 600 0.230 36.0
80.5 69 0.574 10 18.1 0.16 0.9 0.36 20 0.72 2 66 0.086 10.8
85.8 52 ND 25 11.9 0.65 6.5 0.69 29 1.20 1 33 0.055 26.2
88.5 43 ND 29 9.6 0.49 5.3 0.62 22 1.39 1 214 0.030 21.0
91.0 32 0.563 16 7.7 0.30 2.0 0.42 24 0.67 1 12 0.047 58.8
87.1 46 0.862 8 12.2 0.13 4.6 0.25 13 0.39 2 60 0.057 13.3
84.2 57 0.497 6 14.5 0.33 2.4 0.28 12 0.74 1 54 0.052 9.7
Source: Adapted from www.nal.usda.gov/fnic/foodcomp/cgi-bin/measure.pl.
1. Chemical Composition and Nutritive Value. The oldest published chemical composition analysis of American elderberry probably dates back to 1941 (Wainio and Forbes 1941). More recent comparative data are presented in Table 4.2. Kislichenko and Vel’ma (2006) found 16 amino acids, including 9 that are essential for humans, in S. nigra flowers, leaves, and flower extract. Kaack et al. (2006) provided a comprehensive study of volatile compounds in S. nigra flowers and their relationship with sensory quality, emphasizing differences between cultivars. Commercial elderberry juice concentrate is among the richest in total phenolics and highest in antioxidant capacity compared to other red fruit juice concentrates (Bermu´dez-Soto and Tomas-Barberan 2004). European and American elderberries are rich in anthocyanins and phenols (Rimpapa et al. 2007; Mathieu et al. 2008a). Elderberries are noteworthy for their fiber, calcium, iron, phosphorus, vitamin B6, and vitamin A content. They also score high in terms of vitamin C content. One hundred grams of elderberries contain 60% of the recommended daily intake of vitamin A and vitamin C and 12% of the recommended daily intake of vitamin B6 (USDA ARS 2008). These figures are likely to change for the various available cultivars, the management practices used, and the environment they were grown in; however, they illustrate the nutritious quality of elderberries. The two major pigments found in European elderberry are cyanidin 3-sambubioside and cyanidin 3-glucoside (Bermu´dez-Soto and Tom as-Barber an 2004). They also contain quercetin and flavonols but no ellagic acid derivatives (Bermu´dez-Soto and Tomas-Barberan 2004;
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Lau et al. 2004). Elderberry flowers are also rich in quercetin, kaempferol (Brand-Garnys et al. 2007), and other glycosylated flavonoids (Lin and Harnly 2007). About 80 different chemicals have been isolated from elderberry flower extracts and essential oil (Toulemonde and Richard 1983; Merica et al. 2006). Elderberries are a good source of high-biological-value protein (K€ unsch and Temperli 1978a). Kaack (2008) presented an extensive study of European elderberry aroma composition and sensory quality of flower and fruit juices processed from various cultivars. Marked differences were observed between cultivars that could be used to guide the processing industry. The characterization of seed oils of S. canadensis, S. nigra, and S. racemosa has been reported by Schuette and Brooks (1936), Gigienova et al. (1969), and Johansson et al. (1997), respectively. The amount of extractable oils is significant (ca. 30% dry weight) for this last species, and wastes from various manufacturers could probably be used as food supplements or cosmetic agents (Johansson et al. 1997). Wastes from American and European elderberries processing could likely be used in a similar fashion. In fact, the oil content of European elderberry press residues can reach up to 12%, and these residues are particularly rich in tocopherol (Helbig et al. 2008). Important amounts of anthocyanins can be extracted from elderberry pomace, an agroindustrial waste traditionally transformed into animal feed or organic fertilizer, which can advantageously be used by the food, cosmetic, and pharmaceutical industries (Seabra et al. 2008). Various N-phenylpropenoyl-L-amino acid amides have been identified in European elderberry leaves (Hensel et al. 2007). Their possible role in human health is currently under study. Different phenolic acids have also been isolated from European elderberry bark (Turek and Cisowski 2007) and flowers (WaksmundzkaHajnos et al. 2007). 2. Toxicity. The canes, roots, and leaves are not hazardous if properly prepared. The leaves contain hydrogen cyanide (HCN) and should not be used to make alcoholic beverages if their HCN content exceeds 25 ppm. Children who play with elderberry canes are potentially at risk of alkaloid or cyanide poisoning. Sixty mg of cyanide is enough to kill a man (Duke 1985). The berries, for their part, may be eaten raw in reasonable quantities without inconvenience; if consumed to excess, they may cause discomfort and vomiting (Li 2000). Cooking the fruits will eliminate these drawbacks. Most plant parts but particularly leaves (Bourquelot and Danjou 1905) are thought to contain various cyanogenic glycosides and to be somewhat toxic (Hardin and Arena 1974; Tull and Miller 1991; Allen et al. 2002; Atkinson and Atkinson 2002). They can induce
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D. CHARLEBOIS, P. L. BYERS, C. E. FINN, AND A. L. THOMAS
stomachaches, nausea, and vomiting if consumed in large enough quantity. Release of hydrogen cyanide has been reported during berries processing from European elderberry (Pogorzelski 1982). The presence of cyanogenic compounds is quite variable between populations of European and American elderberry (Jensen and Nielsen 1973; DellaGreca et al. 2000a,b; Bradberry and Vale 2007). They are even absent in many cases (Buhrmester et al. 2000). Some of the degradation compounds resulting from the oxidative degradation cleavage of cyanogenins found in European elderberry are thought to be harmless (Seigler 1976; DellaGreca et al. 2000b). The transformation of cyanogenic glycosides is performed by hydroxynitrile lyases to produce HCN, which has a role as a defense mechanism against herbivores and microbial attacks (Hickel et al. 1996). While the toxicity of S. nigra has been reported to be rare and low (Brunneton 2001), Vigneaux (1985) indicated that their fruits can cause bloody diarrhea and mydriasis. Hankla (1977) mentioned that new growth can be fatal to cattle and sheep. Lectins found in the bark of various Sambucus species are thought to be responsible for its toxicity (Van Damme et al. 1997; Lehmann et al. 2006). The gene encoding for the type-2 inactivating protein of European elderberry has been expressed in transgenic tobacco, where it produced an enhanced resistance to some insect species, emphasizing the protective role of such protein (Rapisarda et al. 2000). Similar toxicity of the aphid Aulacorthum magnoliae Essig et Kuwana feeding on S. sieboldiana to the predator Harmonia axyridis Pallas has been reported (Fukunaga and Akimoto 2007). Lectins and ribosome-inactivating protein composition of the bark and fruits of elderberries is complex, and their role is not well understood (Atkinson and Atkinson 2002). The allergological potential of elderberry pollen has not been determined, although its presence in the air was not considered a health problem in Vienna three decades ago (Horak et al. 1976). Because Sambucus pollen concentration has been constantly on the rise between 1976 and 1989 (J€ ager 1989) and may have increased even further since, its impact on allergies must probably be reevaluated. The toxicity of some chemicals found in European elderberry has been put to good use in the field of micropropagation. Kuhn et al. (2007) successfully demonstrated the antifungal property of elderberries and leaf extracts on the fungus Microdochium nivale (Fr.) Samuels & Hallet. D. Traditional Medicine Amerindian and European peoples made use of the American and European elderberry, respectively. In both cases, the leaves, flowers,
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and fruit have long been used to alleviate or cure various ills. American elderberry is prominent in traditional medicine. A poultice made from the leaves reportedly relieves pain and promotes the healing of contusions and sprains, and can be used as a disinfectant to wash sores to prevent infection. The dried leaves are combined with mint leaves and used to treat dyspepsia. An infusion from dried branches was used to cure severe headaches. An infusion made from the flowers is said to have soothing and laxative properties and was used to “sweat out fever.” A fruit decoction is still used in Croatia to reduce fever (Pieroni et al. 2003). The juice of the fruit with some added honey is reportedly a highly effective cough syrup. The same mixture with the addition of some extract of sumac (the fruit of Rhus glabra L.) can be gargled to treat a sore throat. Infusions of the fruit were consumed as an antirheumatic. The inner bark is used to prepare ointments. Bark scrapings were used as an emetic and laxative. The pith was infused by the Iroquois to treat heart disease and venereal disease. Meskwaki women used elderberry to assist childbirth. The Choctaw decocted seeds and roots for liver troubles. Dried flowers were used to treat colic in infants by the Mohegan. Elderberry has been considered to possess calming, carminative, cathartic, cooling, cyanogenic, depurative, diuretic, emetic, exciting, laxative, stimulant, sudorific, and toxic properties, and it has been used in folk medicine to treat abrasions, asthma, bronchitis (K€ ult€ ur 2007), bruises, burns, cancer, chapping, chills, dropsy, epilepsy, fever (Kaileh et al. 2007), gout, headache (Passalacqua et al. 2007), neuralgia, psoriasis, rheumatism, rashes, sores, sore throat, swelling, syphilis, and toothache. Other elderberry species have been popular in folk medicine wherever they grow, as in Brazil where S. australis (de Barros et al. 2007), in Mexico where S. mexicana (Adame and Adame 2000), and in Iran and Turkey where S. ebulus are still in use (Ebrahimzadeh et al. 2007; K€ ult€ ur 2007). The antioxidant activity of this last species has been shown to be high (Hosseinimehr et al. 2007). A number of studies have been conducted with a view to identifying molecules that might account for the fruit’s medicinal properties. To date, however, most research on elderberries has focused on the European species nigra. Unfortunately, few of the claims made about the medicinal properties of elderberries are supported by scientific research or clinical studies (Schapowal 2007), and they must be regarded as the stuff of popular tradition, not solid fact based on rigorous experimentation. The elderberry, in fact, is so firmly rooted in folk medicine and popular traditions that some scientists have attempted to determine whether these claims have any basis. Yesilada (1997), and Yesilada et al. (1997), for example,
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D. CHARLEBOIS, P. L. BYERS, C. E. FINN, AND A. L. THOMAS
investigated the anti-inflammatory and anti-arthritic properties of elderberry (S. ebulus). They conducted in vitro studies on the inhibitory effects of extracts from a number of plants frequently used in Turkish folk medicine, including European elderberry. Their findings reportedly validated some of the latter’s traditional uses. E. Modern Medicine The American Botanical Association (2004) provided a good historical review about elderberry uses as a medicinal plant with references going as far back as the 14th century. Despite a few reported cases of poisoning in animals and humans, European and American elderberries have acquired an impressive reputation as a medicinal plant, and their medicinal value has been recently reviewed by Charlebois (2007). A number of studies have been conducted with a view to identifying molecules that might account for the fruit’s medicinal properties. 1. Leaf. The leaves are ground up and applied to wounds or contusions to relieve pain. Even today, S. canadensis or S. mexicana leaves are utilized in Central America to treat measles (Folliard 2008). 2. Flower. The flowers of European and American elderberries are used, mainly in infusions, to relieve the symptoms of rashes of allergic origin and intestinal problems. They are reported to be effective as a diuretic and laxative as well (Beaux et al. 1998; Uncini Manganelli et al. 2005) and are even recommended by the German Commission and the European Medicines Agency for upper respiratory tract infections (Blumenthal et al. 1998; European Medicines Agency 2008). They can also show some anti-inflammatory properties (Mascolo et al. 1987). 3. Fruit. However, the fruit of the elderberries has always been most widely used. Not only are these berries an effective diuretic and laxative but, like the flowers, they are also used to treat various disorders, including colic, sinus congestion, constipation, diarrhea, sore throat, colds (Schapowal 2007), and rheumatism (Novelli 2003; Uncini Manganelli et al. 2005). They are known to show anti-inflammatory (Barak et al. 2002; Gorchakova et al. 2007), antiviral (Zakay-Rones et al. 1995; Zakay-Rones et al. 2004), antioxidative (Pool-Zobel et al. 1999), and antibacterial (Chatterjee et al. 2004) actions. However, juice concentrate had no effect on kidney stone–inducing ions solubility (Walz and Chrubasik 2008). Antibacterial activity on two strains of
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Streptococcus pneumoniae was also reported for S. mexicana by Molina-Salina et al. (2007). Research has shown that elderberries contain a number of active substances (Bermu´dez-Soto and Tom as-Barberan 2004). We now know that they are rich in tannins, which relieve diarrhea and nasal congestion. They also contain valeric acid, which eases breathing, and hence their usefulness in the treatment of asthma (Novelli 2003). In addition, soluble compounds that can stimulate insulin secretion and enhance glucose absorption, are found in elderberries suggesting that they may be a potentially valuable weapon in treating the symptoms of diabetes (Gray et al. 2000; Goetz 2007). 4. Antiviral and Antimicrobial Properties. European elderberry flower extract can inhibit prokaryotic neuraminidase in vitro (Schwerdtfeger and Melzig 2008). Other interesting curative properties are attributed to Sambucol , a commercial product containing a standardized extract from the European elderberry (Zakay-Rones et al. 1995). These authors found that the compound possessed the property of deactivating hemagglutinin, a protein found on the surface of some viruses that enables the virus to attach itself to a host cell. Viruses with hemagglutinin include those in the group known as the myxoviruses, which cause influenza, among other disorders (Anonymous, 2005). In light of this observation, Sambucol was tested as a treatment for influenza. The results are suggestive: 93% of the patients who were given Sambucol experienced relief of their symptoms after 2 days, whereas 92% of those who received a placebo took up to 6 days to recover. The authors reported that Sambucol possessed the property of inhibiting the replication of 11 strains of the influenza virus and hence expedited recovery (Barak et al. 2001, 2002). In addition, Sambucol appears to possess the capacity to activate the immune system by increasing cytokine production. The investigators suspect that it may act as an immunoprotector or immunostimulant and that it may be advantageous to give it in conjunction with chemotherapy in treating immunodepressive cancers or AIDS (Barak et al. 2001). This latter hypothesis was formulated after two cases had been observed in which patients with HIV used an elderberry-based decoction in conjunction with chondroitin and glucosamine sulfate (Konlee 1998). In both cases, the number of cancer cells declined substantially. In a recent study, Fink et al. (2009) reported that flavonoids and A-type proanthocyanidins found in European elderberry extracts blocked HIV entry and infection in GHOST cells. Roschek et al. (2009) also isolated and identified two antiviral flavonoids from European elderberry that bind to and prevent H1N1 infection in vitro.
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Uncini Manganelli et al. (2005) conducted an in vitro study on the antiviral activity of three plants, including the European elderberry, on the feline immunodeficiency virus (FIV). FIV and HIV share many characteristics, making FIV a useful animal model for AIDS research. Their findings suggest the elderberry may potentially be highly useful in treating HIV. However, further research will be required in order to identify the specific substance that possesses the antiviral activity (Uncini Manganelli et al. 2005). Another study has confirmed that elderberry bark contains a nontoxic ribosome protein deactivator. The use of these proteins in conjunction with monoclonal antibodies appears to be a promising tool in the field of cancer therapy (Girbes et al. 2003). Rutin and chlorogenic acid are found in the fruit (Lee and Finn 2007) and plant parts (Thomas et al. 2008). These two compounds have antioxidant and antimicrobial activities (Basile et al. 2000; Grace and Logan 2000; van der Watt and Pretorius 2001; Zhu et al. 2004). Additionally, chlorogenic acid has antiviral activity (Chiang et al. 2002) and may have some cancer preventive activities in rodents (Conney et al. 1991; Mori et al. 2000). Thomas et al. (2008) quantified rutin and chlorogenic acid levels in flowers, green stems, woody stems, and green leaves of S. canadensis. The levels of both compounds varied among the various parts, among cultivars, among harvest times, and depended on where the plants were grown. The authors felt that these plant parts could be viably harvested to provide these compounds as phytochemicals. 5. Anthocyanins and Antioxidant Capacity. Elderberries contain abundant quantities of anthocyanins, the pigments that give them their purple color (Fossen et al. 1998). This abundance of anthocyanins and other polyphenolics is especially valued in today’s markets for their potential health benefits (Strack and Wray 1994; Wang et al. 1996; Hollman 2001; Lee 2004). The antioxidant capacity of the anthocyanins in elderberries has been reported to exceed that of vitamins C and E (Anonymous, 2005). Sambucus nigra extract has been shown to protect low-density lipoprotein against oxidation (Abuja et al. 1998). Most of the anthocyanins contained in the berries are metabolized before entering the bloodstream (Frank et al. 2005). Lee and Finn (2007) examined the anthocyanins and phenolic composition of elderberry genotypes that represented S. nigra and S. canadensis backgrounds. While they found that the levels of the various compounds varied among genotypes and years, the most striking differences were between the two species. Sambucus nigra has no acylated anthocyanins whereas S. canadensis contained the more stable acylated
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anthocyanins (Brønnum-Hansen and Hansen 1983; Inami et al. 1996; Malien-Aubert et al. 2001; Turker et al. 2004). Lee and Finn (2007) found that the same 11 anthocyanins were present in each of the S. canadensis genotypes that they tested: cyanidin 3-sambubioside-5-glucoside (second major pigment present), cyanidin 3,5-diglucoside, cyanidin 3-sambubioside, cyanidin 3-glucoside, cyanidin 3-rutinoside, delphinidin 3-rutinoside (trace levels present), cyanidin 3-(Z)-p-coumaroyl-sambubioside5-glucoside, cyanidin 3-p-coumaroyl-glucoside, petunidin 3-rutinoside (trace levels present), cyanidin 3-(E)-p-coumaroylsambubioside-5-glucoside (major pigment present), and cyanidin 3-p-coumaroyl-sambubioside. This was the first time delphinidin 3-rutinoside and petunidin 3rutinoside had been reported in S. canadensis. Cyanidin-based anthocyanins were the major anthocyanins present in S. canadensis, and all of these samples had more acylated anthocyanins (>60% of the total pigment present) than nonacylated anthocyanins (Lee and Finn 2007). The S. nigra genotypes ‘Korsør’ and ‘Haschberg’ had five and seven individual anthocyanins, respectively. These genotypes contained cyanidin 3-sambubioside-5-glucoside, cyanidin 3,5-diglucoside, cyanidin 3-sambubioside, cyanidin 3-glucoside, and pelargonidin 3-glucoside (present in trace levels). ‘Haschberg’ had two additional peaks (trace levels of cyanidin 3-rutinoside and delphinidin 3-rutinoside). This was the first report to identify delphinidin 3- rutinoside present in S. nigra (only detected in ‘Haschberg’). ‘Korsør’ examined by Kaack and Austed (1998) also had cyanidin 3-glucoside as the major pigment. The S. nigra samples examined by Watanabe et al. (1998) and Inami et al. (1996) were found to have slightly more cyanidin 3sambubioside than cyanidin 3-glucoside. Bridle and Garcıa-Viguera (1997) reported cyanidin 3-sambubioside5-glucoside as the major anthocyanin in the S. nigra sample they tested, but Brønnum-Hansen and Hansen (1983) reported cyanidin 3-glucoside as the major pigment of S. nigra. As in previous research with S. nigra, Lee and Finn (2007) found there were no acylated pigments in ‘Korsør’ and ‘Haschberg’. Both species contained 3-sambubioside-5-glucoside, 3,5-diglucoside, 3-sambubioside (second major pigment present), and 3-glucoside (major pigment present) of cyanidin. Sambucus nigra also had cyanidin-based anthocyanins as the major anthocyanins. Wu et al. (2004) identified three additional minor anthocyanins in S. nigra (cyanidin 3-rutinoside, pelargonidin 3-glucoside, and pelargonidin 3-sambubioside)—the first time a non–cyanidin-based anthocyanin was reported in elderberries. ‘Korsør’ and ‘Haschberg’ contained trace levels of pelargonidin 3-glucoside, but pelargonidin 3-sambubioside was not detected. In conclusion, S. canadensis would be a better choice to use
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when processing fruit as the acylated anthocyanins will have greater color stability and maintain a better antioxidant capacity compared to S. nigra. Lee and Finn (2007) also found that both species had three cinnamic acids and five flavonol glycosides but that the proportion of the individual polyphenolics differed between them. Neochlorogenic acid (3-caffeoylquinic acid), chlorogenic acid (5-caffeoylquinic acid), quercetin 3-rutinoside, and isorhamnetin 3-rutinoside were the major polyphenolics present in S. canadensis. Chlorogenic acid and quercetin 3-rutinoside were the major polyphenolics in S. nigra. Isorhamnetin 3-glucoside was present at low levels in S. nigra. Neochlorogenic acid, cryptochlorogenic acid, kaempferol 3-rutinoside, isorhamnetin 3-rutinoside, and isorhamnetin 3-glucoside were identified for the first time in S. canadensis and S. nigra berries. In an evaluation of the antioxidant potential of European elderberries to inactivate free radicals in human plasma, Halvorsen et al. (2002) surveyed a wide variety of fruits, berries, vegetables, and grains in a typical Norwegian diet for their total antioxidant levels. While the study did not allow for statistical differences to be assessed between the fruit crops, they found that antioxidant capacity of ‘Samdal’ elderberry (3.37 mmol/100 g) was comparable to wild Rubus idaeus L. (3.97 mmol/ 100 g), cultivated ‘Veten’ raspberry (3.06 mmol/100 g), ‘Hardyblue’ (syn. 1613A) blueberry (Vaccinium corymbosum L.; 3.96 mmol/100 g), and ‘Corona’ strawberry (Fragaria ananassa Duch ex Rozier.; 2.34 mmol/ 100 g). However ‘Samdal’ tended to have lower levels than those for wild strawberries (F. vesca L.; 6.88 mmol/100 g), wild blackberry (Rubus nemoralis M€ ull; 6.13 mmol/100 g), genotypes of black currant (Ribes nigrum L.; 7.35 mmol/100 g), and bilberry (V. myrtillus L.; 8.23 mmol/ 100 g). Frank et al. (2005) concluded that the anthocyanins contained in European elderberries have a low bioavailability. More studies are needed to fully understand the relationship between elderberry chemical composition and the various effects reported. F. Ecological Value and Ornamental Potential American and European elderberries continue to have value in ecosystem management and restoration. The shallow, aggressive root system and hardiness of the wild species make elderberry ideal for riverbank stabilization or shelterbelt establishment. They are also praised for their qualities as suitable plant materials for wildlife and habitat management programs, providing shelter and food to countless species of animals, birds, and insects (Hankla 1961; Worley and Nixon 1974; Coastal Zone
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Resources Division 1978; DeGraaf and Witman 1979; Elias 1980; Martin and Mott 1997; Rajchard et al. 2007). Of the various elderberry species found in North America, S. canadensis and S. cerulea (Raf.) probably possess the greatest value for wildlife (Coastal Zone Resources Division 1978). Some mammals will also feed on twigs and leaves. Their tendency to form dense thickets makes them good candidates as windbreaks along roadsides and farm fields (Paquet and Jutras 1996). The attractive appearance, flowers, and fruits of the European and American elderberries, their ease of cultivation, and their numerous cultivars have earned them a good reputation as an ornamental. Consumers appreciate the color and shape of the foliage, and various cultivars are commercially available. Their hardiness makes them suitable as ornamentals well outside their natural distribution range. G. Markets and Production Costs Very little information has been published on the market potential and the production volumes and costs of elderberries, and only general information is available (Charlebois and Richer 2005). Fruit and flower production are known in Canada and the United States (S. canadensis); in the Russian Federation, Poland, Hungary, Portugal, Bulgaria (Brinckmann and Lindenmaier 1994), Chile (Finn, person. commun.), Denmark, Germany, Italy, and Switzerland (S. nigra). Milliken and Bridgewater (2001) reported Sambucus as having a potential for cultivation in Scotland. These authors also reported that Sambucus fruits, flowers, and leaves were commercially available in Scotland with seven known traders and a trade price varying between 3.25 and 10.10 £/kg with an estimated harvest for elderberry flowers of 100 tons (Milliken and Bridgewater 2001). Elderberry flowers are one of the most important wild plant resources commercially exploited in England (Sanderson and Prendergast 2002). According to Murray and Simcox (2003), a growing number of companies in the United Kingdom are harvesting elderberries. Moreover, Prendergast and Dennis (1997) believe that future development in the elderberry flower industry might head for cultivation rather than collecting from wild stands with an emphasis on organic product lines. In 2004, about 11 ha were dedicated to elderberry production in Switzerland (P. Rusterholz, person. commun.) while between 150 and 180 ha were in production in Hungary (T€ okei and Dunkel 2003). Ferencz (2005) studied the costs associated with elderberry production in Hungary. He concluded that producers underestimated their production costs. As pointed out by Way (1965), the North American elderberry market has an interesting potential with an estimated 2,000 tons processed
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annually in the Lake Erie area at that time (Way 1967). McKay (2001) forecasted that the demand for elderberry was expected to grow. In comparison with many fruit crops, the market for elderberry is still in development. It is recommended that a prearranged market be located to insure profitability (Way 1965; Skirvin and Otterbacher 1977). Numerous products derived from the elderberry fruit and flowers are currently available in various parts of the world. However, these few examples are not adequate to enable us to estimate the actual quantities of flowers and fruits that the market might be able to absorb. Accordingly, an economic study will be required in order to obtain a clearer picture of the quantities of elderberries processed worldwide. The nutrient value and the medicinal potential of elderberries can advantageously be compared to those of better-known fruits, such as strawberries, blueberries, and cranberries. Moreover, elderberry production is not as demanding as any of these fruits. As pointed out by T€ okei et al. (2005), the market should be able to absorb an increase in elderberry production. With the introduction of new cultivars and the publication of production guides, it is to be expected that new products will be introduced in the years to come. H. Processing Few studies have addressed the potential effects of processing on elderberry derived product quality, and many of them deal with the European species. Nakatani et al. (1995) and Inami et al. (1996) have demonstrated that acylation confers a better light and heat stability to anthocyanins extracted from American elderberry compared to those extracted from European elderberry. Juice processing from European elderberry was judged unsatisfactory (Kaack 1989b), and improvements to increase juice yield and lower turbidity were proposed (Landbo et al. 2007). Repeated pigments extraction from elderberry pomace with 0.1 M aqueous hydrochloric acid gave good results (Brønnum-Hansen et al. 1985). Freezing the berries prior to pressing resulted in less pomace with only a marginal reduction in its anthocyanin content (Brønnum-Hansen et al. 1985). Pigment extraction can be optimized by adding citric acid to the extraction solvent, which increases the efficiency of the extraction process and helps stabilize the pigments (Kaack 1990b). Selection of cultivars with high vitamin C content along with reduced air exposure of the juice extracted should be considered as a means to maintain pigment integrity during processing (Kaack and Austed 1998). As a rule, processing can impact negatively on phytonutrients such as anthocyanins and polyphenolics (Lee et al. 2002). This fact further emphasizes the need
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to select cultivars with high phytochemical content and fruits that are ripe since variety and maturity can affect anthocyanin concentration (Brønnum-Hansen et al. 1985). According to Brønnum-Hansen and Flink (1985), minimum anthocyanin degradation and maximum product stability occur with undiluted extract at pH 3 with 2.5% of maltodextrin added as a structure stabilizer freeze-dried at a temperature of 75 C and 60 C for the tray and the product, respectively. In a detailed study on aroma composition and sensory quality of fruit juices processed from European elderberry cultivar, Kaack (2008a) and Kaack et al. (2005) showed the complex chemical composition and transformation of such juices. Similarly, chemical analysis of aqueous extracts from S. nigra flowers revealed their complex chemical composition and the importance of cultivar selection (Jørgensen et al. 2000; Kaack et al. 2006; Christensen et al. 2008). Kaack (2008) also investigated the effect of temperature, liquid phase composition, and extraction time on the extraction of various chemicals from European elderberry flowers. From the results obtained with his analytical technique, Kaack (2008a,b) proposed cultivar selections better suited for specific market segments. The effect of packing materials and storage time on volatile compounds in tea processed from flowers of European elderberry was also investigated. Kaack and Christensen (2008) demonstrated that the aroma of elderberry flowers is complex and that its chemical composition is affected by the packing material used and storage time.
VI. CONCLUDING REMARKS Elderberries have been intimately linked to human culture for millennia as the source of numerous superstitions, as an important part of the medicine chest, and as a multipurpose food source. Natural populations, long the only source available, are now being supplemented by wellmanaged orchards of selected cultivars. Despite the conservation of traditional harvest from wild populations, plant breeding, horticulture, and modern chemistry are guiding the development of elderberry into a viable multipurpose crop with customized cultivars better suited for specific market segments. The production and processing of elderberry fruit and flowers are well established in Europe. The publication of a growing number of studies on the chemical characterization of various plant parts from different elderberry species is likely to increase elderberry production and consumption in North America. Such studies are necessary to orient clinical
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and epidemiological research needed to defend the numerous health claims made about elderberries. Elderberries are easy to grow and offer a wide range of applications. With the release of new cultivars, as well as additional basic horticultural research, they offer a huge potential to horticulture and food industry alike. As pointed out by Luther Burbank close to a century ago “The elderberry has qualities of its own that will commend it strongly” (Whitson et al. 1914).
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5 Modified Humidity Packaging of Fresh Produce Victor Rodov, Shimshon Ben-Yehoshua, and Nehemia Aharoni Department of Postharvest Science of Fresh Produce Institute for Technology and Storage of Agricultural Produce Agricultural Research Organization The Volcani Center Bet Dagan 50250, Israel Shabtai Cohen Department of Environmental Physics and Irrigation Institute of Soil, Water and Environmental Sciences Agricultural Research Organization The Volcani Center Bet Dagan 50250, Israel I. INTRODUCTION II. BASICS OF POSTHARVEST WATER RELATIONS A. Air Humidity and Its Measures B. Water Vapor Diffusion C. Water Potential D. Water Potential versus VPD: A Comparison III. WATER IN POSTHARVEST LIFE OF FRESH PRODUCE A. Condensation and Postharvest Diseases B. Senescence and Ripening C. Physiological Disorders IV. THE CONCEPT OF MODIFIED-HUMIDITY PACKAGING V. PRACTICAL MHP APPROACHES A. Individual Shrunk-Seal Packaging B. Compromise Approaches 1. Package Perforation 2. Packaging Materials with Enhanced Water Vapor Permeability 3. Hygroscopic Additives and Humidity Buffering 4. Liquid Absorption
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C. Mathematical Modeling of MH Packaging VI. SUMMARY ACKNOWLEDGMENTS LITERATURE CITED
I. INTRODUCTION Water is the major constituent of fresh fruits and vegetables, usually accounting for 80% to 95% of their mass. It is vital to biological functions in fresh produce, affecting mechanical properties, providing a medium for all biochemical processes, and being a reactant itself (e.g.,in hydrolytic reactions). Harvested produce remains fresh only as long as it retains water (Patterson et al. 1993). Water relations between plants and their environment (the so-called soil-plant-atmosphere continuum) have been extensively investigated (Kramer and Boyer 1995). However, the specific situation of harvested commodities has been surveyed from this viewpoint in few publications (Ben-Yehoshua 1987; Joyce and Patterson 1994; Van Doorn 1997; Ben-Yehoshua and Rodov 2003). The specific problem of water status in harvested organs stems primarily from their detachment from the mother plant whose root system is in contact with the soil. Therefore, moisture loss from a harvested organ typically cannot be replenished by acquisition of water from an external source.
II. BASICS OF POSTHARVEST WATER RELATIONS A. Air Humidity and Its Measures Water status of harvested commodities is predominantly determined by their interaction with the atmosphere. This interaction is based on the same universal physical principles that govern meteorological phenomena such as fog and cloud formation, dew and rainfall (Brutsaert 1991). Detailed analyses of physical mechanisms underlying plant life and its relationship with the environment have been presented by Nobel (1974, 1991) and Jones (1992). The interaction of liquid water and the atmosphere includes two parallel processes: evaporation when water molecules leave the liquid phase for the atmosphere and condensation when the molecules return to the liquid (condensed) phase. Vapor pressure is a measure of the partial pressure of water vapor in air. Under normal atmospheric conditions, water is continuously evaporating and condensing. If more molecules leave a liquid surface than arrive, there is net evaporation; if more
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Fig. 5.1. Scheme illustrating the relations between liquid and gaseous phases at saturation.
molecules arrive than leave, net condensation takes place. The ratio of condensation to evaporation rates depends on the vapor pressure, the shape of the boundary (molecules escape more readily from highly curved small drops than from a flat surface), liquid purity (dissolved foreign substances diminish the number of water molecules that can escape), and the liquid temperature (at higher temperatures the molecules have more energy and can escape more readily). The situation when the evaporation equals the condensation and air is in equilibrium with a flat surface of water, for example, in a closed jar containing water, is called saturation (Fig. 5.1); the corresponding vapor pressure is denoted as saturation vapor pressure or, more correctly, equilibrium vapor pressure. Saturation vapor pressure varies exponentially with temperature, as shown in Fig. 5.2. The curve can be described by several functions, the most popular of which is an empirical equation introduced by Tetens (1930). One robust version of the Tetens equation, after Buck (1981) as presented by Jones (1992), is: bT esðTÞ ¼ f a exp cþT a ¼ 611:21 b ¼ 17:502 c ¼ 240:97 f ¼ 1:0007 þ 3:46 108 P
ð5:1Þ
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where T ¼ temperature in C es(T) ¼ saturation vapor pressure in Pascal (Pa) P ¼ atmospheric pressure in Pascal Note that at sea level, atmospheric pressure is 100 kPa. Values are also available from tables that appear in many texts, including the Smithsonian Meteorological Tables (List 1971). The word saturation is somewhat misleading. It resembles the same term used for liquid solutions and stems from the erroneous belief that water vapor is “dissolved” in air and that, accordingly, saturation corresponds to a maximal amount of water that can be “held” by air at a given temperature. In reality, as shown by Dalton at the beginning of 19th century, the amount of vapor above a liquid is independent of the existence of other gases. The analysis of popular misconceptions concerning water vapor is presented by Babin (1998). Relative humidity (RH) is probably the most popular term for expressing the moisture of air. It is defined as the ratio of actual vapor pressure
Fig. 5.2. The relationship of saturation vapor pressure to temperature. For 30 C, the line AC represents saturation vapor pressure, or 100% relative humidity. Line AB represents the vapor pressure for approximately 55% relative humidity, corresponding to a dew point temperature of approximately 20 C (point D). The vapor pressure deficit (VPD) is represented by line BC.
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in the air to the saturation vapor pressure at a given temperature, expressed in percent. An example is shown in Fig. 5.2, where if the temperature and ambient vapor pressure are presented by the point B, the ratio (in %) of the lengths of lines AB to AC is the relative humidity. RH values can be correctly compared only if they relate to the same temperature. Using RH without considering temperature can result in grave errors in interpretation of horticultural data, in particular concerning produce storage conditions (Lipton 1993). Because RH is relative to saturation above a flat surface, water evaporation from a curved surface may bring RH values to above 100%. For example, inside clouds, where water is present in a form of tiny droplets (typically 5 to 20 mm in diameter), the stable RH level is normally about 102% (so-called supersaturation). Although theoretically air humidity can increase higher, ubiquitous condensation nuclei (aerosols including dust) normally prevent this from occurring (Brutsaert 1991). More relevant to the postharvest sphere, modern air humidifiers may provide similar droplet size and thus allow very high RH levels without precipitation of condensed water (Afek et al. 2000). Vapor pressure deficit (VPD) is the difference between the actual vapor pressure in air and the saturation vapor pressure at the same temperature. It is measured in pressure units, or Pascal (Pa or Newton m2) in the International System of Units (SI) system. VPD gives an absolute measure of the difference between ambient vapor pressure and that at saturation. Referring to Fig. 5.2, and taking temperature and ambient humidity represented by point B, VPD is represented by the length of line BC. As will be shown, in many cases, VPD is proportional to the rate of evaporation and therefore can be taken to represent the “effective” dryness of the atmosphere. Knowing actual temperature and relative humidity, one can easily calculate the VPD using equation 5.2: VPD ¼ esðTÞ ð1RH=100%Þ
ð5:2Þ
where es(T ) is computed from equation 5.1. Alternatively, VPD values can be determined graphically using psychrometric nomograms or the handy nomogram of Williams and Brochu (see Ryall and Lipton 1979). Using VPD rather then relative humidity (RH) was recommended for accurate characterization of plant/ atmosphere water relations (Anderson 1936; Ben-Yehoshua 1987; Lipton 1993). Still, in this chapter, we often refer to RH, since it is most frequently provided in publications and used in postharvest practice.
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Dew point is yet another important characteristic of air humidity. It is definedasthe temperature towhich moist air mustbe cooled, with pressure and absolute humidity held constant, in order to become saturated. In the case in Fig. 5.2, the dew point is at point D, or 20 C. A net condensation occurs on a surface when its temperature is at or below the dew point. The content of water vapor in air may also be expressed as absolute humidity, measured as mass of water vapor per unit volume of moist air. However, the actual absolute amount of water vapor in air, when considered independently of other factors, is practically meaningless for interpreting evaporation/condensation phenomena. As illustrated by Anderson (1936), the very “dry” atmosphere of Death Valley, California, contains in July almost the same average amount of water vapor per unit volume as does the “moist” atmosphere of Duluth, Minnesota, at the same time of the year. Concludes Anderson: “Very obviously, the importance of atmosphere moisture as a factor affecting the rate of evaporation lies not in the absolute quantity of moisture present but in the relation between the amount present and the amount that could exist under the same conditions without condensation.” For this example, the VPD under typical summer conditions of Duluth, MN (temperature 18 C, 72% RH), would be 0.58 kPa, while at the same time in Death Valley, CA (35 C, 25% RH), the VPD would reach about 4 kPa (i.e., about seven times higher). Therefore, the climate in Death Valley is indeed much drier than in Duluth in spite of the similar absolute humidity under the conditions referred (8.8 and 9.3 g vapor per kg dry air, correspondingly). For the same relative humidity, VPD increases exponentially with temperature, as is implied in Fig. 5.2. For example, at the same RH of 80%, the VPD value at 10 C is almost twice as high as at 1 C (25 versus 13 kPa, accordingly), which can result in higher water evaporation rates. B. Water Vapor Diffusion Loss of water from a plant organ (e.g., fruit or vegetable) to the atmosphere is termed transpiration. The transpiration may be considered as a particular case of gas diffusion through a barrier (the organ’s surface). Therefore, it is described by Fick’s law: J ¼ ðei ea ÞAt =ðRD TÞr
ð5:3Þ
where J ¼ vapor flux ea and ei ¼ vapor partial pressures in the atmosphere and in the organ’s intercellular spaces respectively
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At ¼ organ’s surface area RD ¼ gas constant per mass unit T ¼absolute temperature r ¼ surface resistance to vapor diffusion Stomatal or lenticel openings are present in the surface of some fruit and vegetables but are absent in others (Ben-Yehoshua and Rodov 2003). Surface resistance r depends on stomatal opening, resistance of the cuticle and other surface components, as well as aerodynamic resistance. The latter depends on air movement (or wind speed) and turbulence. Air movement and turbulence are also influenced by temperature, and aerodynamic resistance can be large when air movement is inhibited, as frequently occurs in storage conditions, but rigorous treatment of these influences is beyond the scope of this chapter. The interested reader is referred to Monteith and Unsworth (1990). It has been demonstrated, both empirically and theoretically, that intercellular water vapor in the tissues of fresh succulent organs is very close to saturation throughout the organ’s volume, with RH approximately 99.5% (Nobel 1974; Ben-Yehoshua and Rodov 2003). Consequently, for the same r, if the temperatures of the organ and of the surrounding air are the same, the expression (ei ea) in equation 5.3 is practically equal to the difference (es(T) ea), that is, to the vapor pressure deficit (VPD). In this case, the rate of transpiration from fresh produce is proportional to the VPD of the surrounding atmosphere at a given temperature. In real postharvest practice, the temperatures of the produce and of the surrounding air are not always equal. Temperature differences may enhance water loss, for example, in the case where warm produce is placed in a cold store without proper field heat removal. Another factor causing temperature differences between stored produce and the surrounding atmosphere may be fluctuations in air temperature in a storage room because the flow of refrigerant is turned on or off by a thermostat. Efficient produce precooling and omitting fast temperature fluctuations during storage are needed in order to minimize moisture loss from produce. Another diffusion phenomenon relevant to this review is gas or water vapor exchange between the atmospheres inside and outside a plastic package containing fresh produce. This process may also be described by equation 5.3. In this case, ei and ea are partial pressures of a relevant gas (vapor) across the packaging material, At is the plastic film area, and r is the packaging material’s diffusion resistance inversely related to its permeability toward the specific gas.
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C. Water Potential Water potential, denoted by Y (psi), is the most useful quantity for expressing water status in plant physiology. Water potential is a measure of the free energy of water in a given system, compared with the free energy of pure water. In thermodynamics, free energy is defined as the potential for performing work. Several forces act on any molecule affecting its ability (potential) to do work. These factors are concentration, pressure, electric force, and gravity; added together, they make up the chemical potential. Accordingly, the chemical potential of a species j is represented by equation 5.4 (Nobel 1987): mj ¼ mj þ RT ln aj þ Vj P þ zj FE þ mj gh
ð5:4Þ
where m ¼ chemical potential R ¼ gas constant T ¼absolute temperature aj ¼ activity (“effective concentration”) of the species j linearly related to its actual concentration Vj ¼ its partial molal volume nearly equal to the volume of one mole of the species P ¼ pressure exerted on the system in excess of the atmospheric pressure zj ¼ electric charge of the species j F ¼ Faraday’s constant E ¼ electric potential mj ¼ molar mass of the species j g ¼ the gravitational acceleration h ¼ vertical height above the zero (sea) level Note that the elements of equation 5.4 represent contributions of each of the aforementioned factors (concentration, pressure, electricity and gravity) to the overall chemical potential. Since chemical potential is a relative quantity, equation 5.4 includes an additive constant term (reference level) mj . As a result, the difference of chemical potentials between two states can be determined, rather than the absolute values of these potentials. Turning from chemical potential in general to the situation of water in the soil-plant-atmosphere continuum, equation 5.4 can be modified. First of all, one can exclude the electrostatic component since the water molecule is uncharged. The gravitation component may play a
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significant role in soil water status, but for water in plant tissues, it is usually negligible except in tall trees. Obviously, it is unimportant for postharvest systems. The remaining influences that reduce water activity in the system are solutes and the interaction of water with the surface of colloids on liquidsolid interfaces. Therefore, the activity-related component of equation 5.4 may be transformed in accordance with Nobel (1987) in this way: RT ln aw ¼ Vw ðp þ tÞ
ð5:5Þ
where Vw ¼ partial molal volume of water p ¼ osmotic pressure t ¼ matrix pressure resulting from the water-solid interactions at the surfaces of the colloids. The practical interpretation of the matrix pressure is associated with water binding on the surface of soil particles or cell wall matrix. The biological meaning of the pressure-related component Vw P in equation 5.4 is associated in plant tissues with hydrostatic pressure (turgor) exerted on cellular water by rigid cell walls. Transforming equation 5.4 gives the next expression for the chemical potential of water (i.e., water potential Yw) in plant systems: Yw ¼ ðmj mj Þ=Vw ¼ Ppt
ð5:6Þ
In agreement with equation 5.6, water potential in a plant system is comprised of three elements: (1) the pressure, or turgor potential that pushes via the cell wall on the contents of plant cells; (2) the osmotic potential of the cell solution, which pulls water into the cell; and (3) the matric potential, due to capillary and molecular imbibitional forces associated with cell walls and colloidal surfaces that bind some of the water. Thus, equation 5.6 can be rewritten as: Yw ¼ YP þ Yp þ Yt where Yp ¼ osmotic potential YP ¼ pressure potential (turgor) Yt ¼ matric potential Yw ¼ overall water potential
ð5:7Þ
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Except for YP , these values are negative or equal to zero. Water potential is expressed in pressure units, that is, J m3 ¼ N m2 ¼ Pa. In a container with two compartments that share a semipermeable membrane, and each contains water at different potentials, water will move spontaneously in the direction of decreasing potential. In fully turgid tissue, osmotic and turgor pressure are equal and opposite, and the matric potential approaches zero as the colloids and matric surfaces become saturated, resulting in Yw ¼ 0. As an organ dries, turgor and water potential decrease. If water at higher potential is hydraulically available, it will be drawn into the organ. When the tissue is under water stress, turgor is further reduced; the contribution of osmotic and matric effects may increase, and water potential drops farther below zero. As relative water content is further reduced, the wilting point is reached where turgor approaches zero and plasmolysis may occur. For atmospheric water vapor, the equation of chemical potential normally contains only the activity-related element; and the gravitational element is negligible at altitudes less than 1000 m above sea level (Nobel 1987). The activity of water vapor in air awv may be approximated as %RH/100. Accordingly, the atmosphere water potential Ywv is equal to Ywv ¼ RT=Vw ln ð%RH=100Þ
ð5:8Þ
Note that the partial molal volume of liquid water Vw rather than the appropriate volume of water vapor is used in equation 5.8 in order to allow the comparison of water potentials in different phases. The values of the atmospheric water potential typically observed in nature are very low. For example, at 20 C, the Ywv equals approximately 94 MPa at 50% RH, 6.9 MPa at 95% RH, and 1.35 MPa at 99% RH. Considering that the outdoors atmospheric RH rarely reaches the level of 95% to 99% (even during rain) and that leaf water potential varies from 0.5 MPa in agricultural crops like lettuce to 5 MPa in drought-tolerant desert plants, one can conclude that in a natural environment, plants practically always lose water to the atmosphere. Whole plants can replenish transpired moisture loss by taking up water from the soil, which typically has water potentials in the range of 0.01 to 0.5 MPa. However, for harvested commodities disconnected from external water sources, low atmospheric water potential becomes a critical factor. In postharvest situations, turgor reduction leads to wilting, shriveling, and similar phenomena. Most harvested
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commodities turn nonmarketable due to these disorders after losing just 3% to 10% of their weight through transpiration (Ben-Yehoshua and Rodov 2003). One may expect that fresh produce typically loses its market value before matric potential starts playing a significant role in water potential. The potential life span of a detached plant organ under natural ambient conditions depends on the specific organ. Persistent plant organs such as bulbs, tubers, roots, corms, and many mature fruits have morphological and anatomical peculiarities that may be regarded as preadaptations to prevent postdetachment water deficit (e.g., high solute concentrations and osmotic potential, low surface/volume ratio, thick waxy cuticles and/or other water-barrier layers on the surface, and closure and gradual degradation of stomata with maturation). Plant organs not predisposed biologically to sustaining detachment (e.g., leafy vegetables, cut flowers, and immature fruits) lack most of these mechanisms and are especially sensitive to postharvest water loss (BenYehoshua and Rodov 2003). At any rate, the commercial life span of all commodities under noncontrolled environmental conditions is insufficient. Therefore, preservation of fresh produce demands creation of an artificial environment aimed in particular at reducing the water loss from the produce. One of the elements of this environment should be an atmosphere with relatively high (i.e., close to zero) water potential. Further sections of this chapter describe some practical approaches used to reach this goal. D. Water Potential versus VPD: A Comparison Let us compare the two approaches presented in this section—the Fick’slaw–related VPD and the water potential concept—as means to characterize water relations in postharvest systems. It was shown earlier that when all the components of chemical potential besides the activityrelated element are negligible (as for the atmospheric moisture), the gradient of water potential is equivalent to the concentration gradient (i.e., the water potential concept is implicit in Fick’s law). The basic meanings of atmospheric water potential and of vapor pressure deficit are quite similar. Both parameters indicate how far the air is from saturation, and both can be thought of as the driving force for transpiration. Both are measured in pressure units and equal or close to zero at saturation; their absolute value increases with the decrease of air humidity. Both values can be readily calculated from atmospheric RH and temperature measures. The relationship between VPD and Ywv values of air is presented in Fig. 5.3.
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Fig. 5.3. Relationship between atmospheric water potential and vapor pressure deficit at 20 C.
The interaction of a fresh commodity with the atmosphere may be described by both approaches. As long as produce is conceived as a homogenous body saturated with water and enclosed in a semipermeable casing, there is no significant advantage for the water potential concept. Moreover, Fick’s law seems to be a more adequate way to describe water vapor transport from produce to the atmosphere, in particular because it includes the diffusive resistance component. In other words, it not only describes the driving force of transpiration but also characterizes the rate of the process. For the water potential concept, the diffusion resistance factor may be a cause of aberrations (Zanstra and Hagenzieker, 1977). For the same reason, Fick’s law seems to be a more appropriate basis for considering water vapor flux in packaging systems. The advantage of the water potential approach becomes evident, however, when water relations within plant tissues are considered, including the tissues of a harvested organ. Such phenomena as turgor changes, water translocation within the organ (e.g., due to starch hydrolysis during ripening) can be adequately described using the water potential concept. Good examples of consistent application of the water potential approach for describing mechanical properties of harvested produce are given in the papers of Herppich et al. (1999, 2004) and Landahl et al. (2004). Alferez et al. (2003, 2005), and Alferez and
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Burns (2004) used the water potential concept to explain the development of postharvest peel pitting in grapefruit at nonchilling temperature. While simple RH and temperature measurements are sufficient for determining atmospheric VPD and/or water potential, special activities, often rather tedious, are necessary to know the water potential of plant tissues. Methods of water potential measurement have been reviewed by Boyer (1995). Most of these methods are based on application of either pressure chambers or dew point psychrometers. Both approaches have certain difficulties when applied to fruits and vegetables, especially bulky ones. It should be noted that apparent Yw may vary depending on the measurement method used (Zanstra and Hagenzieker, 1977); therefore, a good understanding of the method used is required for reliable measurement. In particular, if a fruit has no stomata or they are closed and its cuticular resistance is high, psychrometry may not be practical because a steady state in the measurement chamber cannot be reached. In this case, only osmotic potential of solution extracted from the fruit can be measured. A nondestructive method for measuring water potential of fruit and vegetables was proposed by Jobling et al. (1997) based on the measurement of water exchange between the fruit and pads containing a salt solution of known water potential attached to the surface of the fruit.
III. WATER IN POSTHARVEST LIFE OF FRESH PRODUCE Water loss is one of the major factors that contribute to commercial and physiological deterioration of fruits, vegetables, and cut flowers. As mentioned, most commodities lose market value when their water loss reaches 3% to 10% of the initial produce weight; in some cases just 1% to 2% water loss makes produce nonmarketable (Ben-Yehoshua and Rodov 2003). Surveying all available literature on this subject is out of the scope of the current chapter. Instead, we present examples from several specific areas of produce-water interaction, illustrating the importance of water for preservation of harvested commodities. A. Condensation and Postharvest Diseases Not only water shortage but also excess moisture can cause stress in the harvested commodity. Water-excess stress is most evident when moisture is allowed to accumulate on the produce surface, usually as a result of water condensation. Condensation hastens spoilage and considerably shortens storage life (Ben-Yehoshua et al. 1998a,b; Xu and Burfoot 1999; Hemalatha et al. 2000; Kleinhenz et al. 2000).
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Patterson et al. (1993) and Joyce and Patterson (1994) detailed the negative consequences of water condensation on the fruit surface, including leakage of solutes from the damaged areas, inhibition of gas exchange, and enhancement of microbial growth. The latter factor seems to be the most important in the detrimental condensation effect. Germination of fungal spores is promoted by condensation (Pasanen et al. 1993; Fernando et al. 2000). Presence of condensed water on the produce surface favorably affects the development of postharvest pathogens (Will 1975; Eckert 1978; Grierson and Wardowski 1978), including such harmful species as Erwinia carotovora (Lund and Nichols 1970), Botrytis cinerea (Jarvis 1977), and Aspergillus niger and Rhizopus stolonifer (Witbooi et al. 2000). It should be mentioned, however, that desiccation and wilting also increase the susceptibility of vegetables to necrotrophic pathogens such as Botrytis (Eckert 1978). Important factors promoting water condensation in fresh produce storage include temperature fluctuations (Sonneveld van Buchem 1985; Koca et al. 1993), breakage of the cool chain (Jackson et al. 1999), and insufficient ventilation (Xu and Burfoot 1999). Condensation is also affected by package volume (less condensation occurs in smaller packages) and by the degree of ventilation (Sonneveld van Buchem, 1985; Noble 1990; Hemalatha et al. 2000). Xu and Burfoot (1999) developed a numerical model describing the occurrence of condensation in bulk foodstuff stores. The model was able to predict the position of condensation in a typical potato storage facility and allowed the authors to propose a way to control the phenomenon. It should be kept in mind that water condensation on the produce surface is almost inevitable in postharvest practice, in particular at the stage of rewarming when the produce leaves the cold store and is exposed to the ambient atmosphere. Temperature equilibration may take a long time, depending on airflow, package, and produce characteristics. During the entire period when the produce surface temperature is lower than the ambient air dew point temperature, water will condense on its surface (so-called sweating; see Fig. 5.2). In combination with relatively high temperature, this situation creates ideal conditions for disease development. The rewarming situation was simulated in experiments with “Galia”type melons. The melons were packaged in commercial cartons without any preliminary packing house treatment, kept for 14 days at 5 C, and subsequently transferred for 4 additional days to simulated shelf-life conditions (temperature about 20 C and RH ca. 85%). After removal from cold storage part of the melons underwent forced temperature equilibration (FTE) by holding the fruit out of cartons for 10 minutes in a flow of
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Fig. 5.4. Temperature of the fruit surface and of the surrounding in-package atmosphere and readings of the wetness sensor mounted on the fruit surface after transferring meloncontaining packages from the cold storage directly to shelf-life conditions. Lower sensor readings correspond to lower surface electrical resistance due to the presence of condensed water; accordingly, the increase in sensor readings means gradual surface drying.
warm outdoor air. Another group comprising nine cartons of melons from the same batch was transferred to the shelf-life conditions directly from the cold store. These cartons were arranged in three adjacent stacks of three cartons in each; the condensation was measured on the surface of a melon located in the second carton of the middle stack (i.e., the central pack surrounded by other cartons). The condensation was assessed by a custom-made wetness sensor based on the electrical conductivity measurement similar to the sensor described by Wei et al. (1995). The results of temperature and condensation measurement are presented in Fig. 5.4. The figure shows that it took more than 40 hours to reach temperature equilibrium between the bulky fruit directly taken from the cold storage and the atmosphere inside the carton. Accordingly, the fruit surface stayed wet for all that period of time. On the contrary, no condensed water was present during the shelf life on the surface of melons that underwent the FTE treatment. Table 5.1 presents the effect of forced temperature equilibration on the quality of melons. It is clear from the data in this table that the FTE treatment significantly reduced the incidence of fruit decay and the growth of aerial fungal mycelium on the fruit surface.
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Table 5.1. Effect of forced temperature equilibration (FTE) on decay and quality of Galia-type melonsz after storage of 14 days at 5 C and 4 days at 20 C. Treatment Fruit with decay, % Fruit with aerial mycelium, % General appearance index, 1 to 5y
No FTE (control) 55.6 100.0 1.8
FTE 18.8 37.5 2.5
z
The fruit did not receive antifungal packinghouse treatments. 1 ¼ completely deteriorated, . . .2.5 ¼ marketable, . . .5 ¼ excellent.
y
The duration of “wetness period” (i.e., the period when liquid water is contiguous to the plant organ) is accepted in plant pathology as one of the important factors affecting the disease development (see, e.g., Jarvis 1977). Therefore, although the phenomenon of condensation is practically inevitable, one may significantly diminish its negative effect by accelerating the thermal equilibration between the produce and the atmosphere at the rewarming stage (Rodov et al. 1997). The importance of fast produce cooling at the beginning of the cool chain is commonly understood nowadays. The symmetrical process at the other end of the cool chain (“fast rewarming”) is equally important. A similar study was conducted later with stone fruit (sweet cherries and plums) by Linke et al. (2004), leading the authors to the same conclusion about the importance of enhanced airflow at the rewarming stage for improved post–cold storage fruit handling. In this case, two mechanisms could explain the results. First, enhanced airflow increases convective heat transfer from the air to the fruit, thus speeding up temperature equilibration. Second, once fruit temperature exceeds the dew point temperature, increased ventilation reduces the aerodynamic resistance and speeds up evaporative drying of the fruit surface. B. Senescence and Ripening Water deficit has been shown to accelerate senescence in plant tissues (Ben-Yehoshua and Rodov 2003). The common mechanisms that underlie the two phenomena may be related to deterioration of membranes caused by free radical formation. In harvested bell peppers, the development of water stress was accompanied by softening, decreased insoluble pectin, increased soluble pectin, and increased electrolyte leakage, all processes attributed to senescence (Ben-Yehoshua et al. 1983a). When peppers are kept in a water-saturated atmosphere, all these physiological changes are alleviated.
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Similar to senescence, ripening of a number of harvested commodities is hastened by water stress. Littman (1972) found in banana and other climacteric fruit that the time from harvest to the climacteric peak was inversely related to the rate of weight loss. Acceleration of ripening in water-stressed bananas and avocados was later confirmed by other authors (Burdon et al. 1994; Akkaravessapong et al. 1996). In particular, Burdon et al. (1994) showed that water stress affects banana ripening by increasing the ethylene production of the peel through an increase in l-aminocyclopropane-1-carboxylic acid (ACC) content and ACC-oxidase activity. In contrast, keeping bananas at high humidity (95% RH) after ethylene treatment slows down their color change and softening (Blankenship and Herdeman 1995). Fast softening of Japanese persimmon at ambient humidity (40%–60% RH) is induced by the ethylene produced by water-stressed fruit calyx tissues, which in turn induces autocatalytic ethylene production in the flesh (Nakano et al. 2002). Keeping the fruit at high humidity (>95% RH), as well as treating them with an inhibitor of ethylene action, 1-methylcyclopropene (1-MCP), prevents or markedly reduces their softening. The 1-MCP treatment inhibits the secondary ethylene production by the flesh but not the initial ethylene peak originating from the water-stressed calyx. This initial ethylene production is accompanied by the increased accumulation of ACC and expression of the enzyme ACC-synthase. Quite opposite, storage at low humidity (55% and 75% RH) inhibits ripening of Le Lectier pears compared with fruit stored at 95% RH (Murayama et al. 1995). This inhibition is related to the suppression of ACC synthesis, inhibiting in turn the production of ethylene. It can be overridden by exogenous ethylene treatment. In durian, water stress accelerates rind yellowing but does not significantly affect pulp ripening (i.e., changes in starch and sugar contents, softening) (Ketsa and Pangkool 1994). It is obvious that the behavior of each fruit in relation to water stress may vary depending on the response of more than one parameter to this stress. C. Physiological Disorders Both water deficit and water excess may trigger various physiological disorders in harvested fruits and vegetables. In this section we present some examples of such disorders. In citrus fruits, several kinds of blemishes result from suboptimal water status of the peel. A special physiological blemish of Shamouti oranges (Citrus sinensis) known as noxan or superficial flavedo necrosis is the result of collapsed hypodermis cells in the flavedo. This blemish reduces fruit quality and causes
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significant losses, threatening the commercial future of this cultivar. Noxan incidence and severity on Shamouti oranges is markedly reduced by several postharvest treatments that raise the humidity of the atmosphere around the fruit to over 96% RH, such as individual seal packaging, keeping fruit in plastic bags or plastic liners, or even by temporarily holding the fruit in a water-saturated atmosphere. Noxan incidence is much lower at 5 or 6 C than at 20 C. All treatments that reduced noxan also reduce weight loss and maintain the turgidity and firmness of the fruit (Ben-Yehoshua et al. 2001a). These authors suggested that the blemish may be related to disruption of the oil gland compartmentalization leading to leakage of the essential oil components that cause the damage. Similarly, the red blotch blemish of lemons is inhibited greatly by raising the storage humidity from 80 to 85% to 90 to 95% RH. Development of blemishes in various citrus fruits is markedly inhibited under high-humidity conditions provided either by shrunk-seal packaging (Ben-Yehoshua 1985) or by the Humifresh storage technique (Deason and Grierson 1972; Ben-Yehoshua 1987). Another blemish of citrus fruit, called rind-staining or rind breakdown, is also referred to as postharvest nonchilling peel pitting. It affects fruit of Navel oranges, Marsh grapefruits, and Fallglo tangerines and is characterized by sunken colorless areas of the peel that develop into reddish-brown, dry areas partially covering the exposed portion of the mature fruit (Agusti et al. 2001; Alferez et al. 2001; Lafuente and Zacarias 2006). Observation of the damaged areas by light microscopy reveal a collapse in epidermal and subepidermal tissues and flattening of some layers of enveloping cells surrounding the oil gland. At advanced stages of the disorder development, coincident with browning of the flavedo, oil glands became deformed and began to collapse. At this stage, oil droplets may be visibly observed between albedo cells below the deformed oil glands. According to Alferez et al. (2005) this blemish is caused by transient exposure of fruit to low humidity, followed by a transfer to high RH (90%) storage. Only 2 hours at a RH of 30% are sufficient to induce peel pitting in Fallglo and Marsh fruit during subsequent high-RH storage. The authors suggest that the commercial impact of postharvest peel pitting can be reduced by harvesting susceptible cultivars at high RH and minimizing exposure to low RH after harvest. Note that RH is usually high early in the morning and late in the evening. Similar observations with Kiyomi tangor (Citrus unshiu C. sinensis) were made by Fujisawa et al. (2001), who studied the traditional practice of prestorage conditioning (i.e., keeping fruit at ambient
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temperature and humidity for 1 to 2 weeks before prolonged cold storage). The conditioning increases the occurrence of rind injury manifested as brown spotting. On the contrary, Kiyomi fruit, stored at 6 C and >98% RH without prestorage conditioning, remain sound with little or no rind injury for 5 months after harvest. Excessive turgidity and wetness can predispose citrus fruit to a different important physiological disorder, oleocellosis (or oil spotting), a blemish caused by mechanical impact damage that ruptures oil glands and brings their content in contact with hypodermal cells (Knight et al. 2003; Lafuente and Zacarias 2006). For lemons, keeping fruit at ambient conditions for 24 hours before delivery to packing houses has been recommended to reduce the risk of oleocellosis by decreasing fruit turgidity (Wardowski et al. 1998). Similarly, enhancement of moisture loss by prestorage cooling delay suppresses the development of apple storage disorders, such as soft scald and low-temperature breakdown (DeLong et al., 2004). Controlled-atmosphere storage of apples at relatively low humidity (RH >75%) reduced their bruising susceptibility, respiration rate, and titratable acidity loss (Prange et al., 2001). Fruit cracking or splitting is another example of a physiological disorder associated with excessive turgor pressure. Splitting can occur in almost any compact plant organ due to a sudden increase in water supply. In sweet cherries (Prunus avium L.), cracking is related to water absorption through the fruit surface, both preharvest during rainfall (Beyer and Knoche 2002) and postharvest when the fruit is transported in water-filled containers. About 20% of fruit cracked after 6 hours of “wet storage” (Stortzer and Grossmann 1980). Similarly, in cherry tomatoes, cracking occurs both in the field and after harvest, rendering fruit nonsalable and fostering fungal decay. The cracking potential of cherry tomatoes is highest after morning harvest; it declined at noon and was low after evening harvest. Early morning corresponds to low negative water potential and maximum turgor pressure. Water loss from the fruit reduces the cracking potential (Lichter et al. 2002). Splitting of carrot storage roots is one more disorder triggered by a high water status. The disorder is characterized by occurrence of sudden radial longitudinal fractions of the roots at harvest and during handling. Split roots have to be discarded during sorting, but since splitting continues throughout the handling process, the final product still may contain split roots. Splitting develops as a result of water uptake by the root cells, which increases cell volume and in turn causes stress and strain within the root tissues (Sorensen and Harker 2000). Carrot genotypes vary in their susceptibility to splitting (McGarry 1993).
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IV. THE CONCEPT OF MODIFIED-HUMIDITY PACKAGING As mentioned, preservation of fruits and vegetables demands creation of an artificial environment with relatively high water potential in the atmosphere in order to prevent loss of produce freshness. Assuming that the produce had optimal water status prior to storage, ideal conditions for quality maintenance would be when the commodity neither loses nor absorbs water and there is no risk of surface wetting due to water condensation or other reasons. The desirable humidity levels vary for different commodities, depending on water potential of the produce, its recommended storage temperature, surface peculiarities, and sensitivity to disorders. The information regarding optimal storage conditions for various fresh crops may be found, for example, in the recommendations prepared by Hardenburg et al. (1986). For most fresh fruits and vegetables, the recommended conditions are within the ranges of 85% to 98% RH and 1 to 13 C. These ranges correspond to VPD from 0.01 to 0.22 kPa and air water potential from 2.5 to 21.5 MPa. However, much lower values (RH 65%–70% at 0 C corresponding to Ywv of 45 to 54 MPa) are recommended for certain commodities with relatively high dry-matter content and accordingly low water potential, such as garlic and onion. Extended storage of garlic at RH higher than 70% to 75% at positive temperatures results in disorders associated with excessive water absorption (e.g., sprouting, rooting, and mold development). Two major approaches are used in order to create optimal humidity conditions around stored fresh produce. One approach addresses design and operation of a storage facility in order to maintain high atmospheric moisture with minimal temperature fluctuations. The factors important in this context are insulation, airflow, refrigeration regime, and air humidification. The second approach deals with formation of an optimal local microenvironment around the produce by means of appropriate packaging. These two approaches are based on the same physicochemical principles and in real life should be exploited in parallel in order to reach the desired goal. However, this chapter concentrates predominantly on the latter approach (i.e., on packaging design ensuring optimal humidity conditions for maintaining quality of fresh fruits or vegetables). The term modified humidity packaging (MHP) was introduced by Shirazi and Cameron (1987, 1992) and Shirazi (1989) as an extension of the widely used term modified atmosphere packaging (MAP). Resistance of a plastic film for water vapor permeation usually far exceeds that of produce surfaces (Ben-Yehoshua 1978; Ben-Yehoshua et al. 1985).
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For example, permeance of 20 m-thick low-density polyethylene for water vapor is about 70 times lower than that of mango fruit surface and about 20 times lower than that of citrus fruit as calculated from data presented by Ben-Yehoshua et al. (1985) and Fishman et al. (1996a). Therefore, most water molecules evaporated from the produce do not escape through the film and remain within the package space, enhancing the water vapor pressure in the package microenvironment. Saturated vapor density at 20 C is 17.3 g/m3. A simple calculation shows that for a package with a void volume of 500 ml and initial RH of 50%, the addition of just 4.3 mg of water is sufficient to bring the atmosphere to saturation. Modeling the conditions in plastic packages containing fresh produce caused Song et al. (2002) to conclude that with regular commercially available films (such as polyethylene or polypropylene), the in-package RH “could not be controlled below 100%.” Elevated humidity inside the package reduces the water potential gradient between the produce and the atmosphere, diminishing further moisturelossfromthecommodity.Underthesenear-saturationconditions, even minor temperature fluctuation may result in precipitation of condensed water on the inside surface of the film and/or on produce surfaces, causing produce wetting and stimulating pathogen development. Therefore, the major challenge of modified-humidity packaging is finding solutions for reducing the risk of water condensation in the package while still maintaining produce water loss as low as possible. Several practical approaches to achievement of this goal will be surveyed in the next section. In addition to controlling the water loss, packaging fruits and vegetables in plastic film often serves another purpose: creation and maintenance of optimal modified atmosphere composition (oxygen and carbon dioxide levels) due to produce respiration. Although this subject is out of the scope of the present chapter, one should keep in mind that reaching these objectives must be harmonized in order to achieve the ultimate goal of extended produce life. In other words, package design should answer specific produce requirements toward both humidity conditions and atmospheric composition; otherwise its effect on maintaining produce quality will be limited or even detrimental.
V. PRACTICAL MHP APPROACHES A. Individual Shrunk-Seal Packaging The method of individual sea -packaging (sometimes also called shrinkwrap or, rarely, unipack) was developed and promoted to horticultural
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practice by Ben-Yehoshua (1978, 1985) and Ben-Yehoshua and Nahir (1977). According to this technique, each individual fruit or vegetable is sealed in a separate package of heat-shrinkable film and then is passed through a hot-air tunnel. The method is based on using bilaterally oriented polymer films, stretched after extrusion in two dimensions that have a high shrinking capacity at elevated temperature. The resulting shrunk package tightly covers the commodity, following its shape and leaving only a very small air space between the produce surface and the film. The air in this space practically immediately becomes saturated with water vapor diffusing from the produce. Because of the close contact between the produce surface and the film, the respiratory heat is efficiently dissipated via conduction rather than the less efficient convection process. The temperature gradient between the produce and the package surface is negligible, diminishing the chance of water condensation within the inner space of the package. As a result, individual shrunk-seal packaging allows maintaining high RH around the produce without the risk of condensation (Ben-Yehoshua et al. 1981; Joyce and Patterson 1994), especially with objects of regular shape, such as citrus fruit, cucumber, and melon. In addition, the smaller the void volume of a package the less water vapor it contains per surface area unit. At the same time, this cover is relatively gas permeable due to its low thickness as well as minor film ruptures that usually form during heat shrinkage. The method of individual shrunk-seal packaging extends the postharvest life of nonclimacteric commodities (e.g., citrus, bell peppers, cucumbers) as measured by appearance, firmness, shriveling, weight loss, and other keeping qualities, without any deleterious effect on flavor (Ben-Yehoshua et al. 1981, 1983b). Moreover, it reduces chilling injury in various citrus cultivars (Ben-Yehoshua et al. 1981) and thus could be combined with low-temperature storage in order to further extend the life of the fruit. The mode of action of seal packaging in delaying the deterioration of nonclimacteric fruits was shown to be related to alleviating water stress rather than to changes in atmosphere composition (Ben-Yehoshua et al. 1983a,b). Reducing the in-package relative humidity with calcium chloride negated the advantages of seal packaging for bell peppers and lemons (Ben-Yehoshua 1983a). Individual film wrapping delays senescence of cucumbers and Chinese cabbages due to combined effect of increased humidity and altered atmosphere composition (Zong 1991). Individual shrunk-seal packaging allows improvement of keeping quality also with many climacteric commodities, such as persimmon (Kawada 1982), muskmelons (Lester and Bruton 1986), and durian
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(Mohamed 1990). However, in other climacteric fruit, such as mangoes or tomatoes, shrink sealing in nonperforated films causes undesirable effects of impaired ripening and off-flavor development (Miller et al. 1986; Floros et al. 1987). These side effects apparently are related to the composition of the modified atmosphere generated inside the shrunk packages, which was inappropriate for those fruits. Using properly selected perforated films for seal-packaging tomatoes (Floros et al. 1987) and mangoes (Rodov et al. 2003) alleviates postharvest water stress in these commodities without negative effects on their quality. Individual shrunk-seal packaging is commonly used for marketing desiccation-sensitive produce, such as greenhouse cucumbers (Otma 1988). Special machines are available for the application of shrunk-seal packaging to various products. In labor-rich countries, such as China, a similar technique is applied manually, when each individual fruit is tightly wrapped in plastic film. This individual wrapping is routinely applied in China for exporting and for local long-distance transport of various citrus fruits. It is used also in Japan with several commodities, including long-term storage of citrus fruit. Still, the extent of commercial implementation of the individual seal packaging seems inadequate compared with its high efficacy. Some possible explanations of this limited application include difficulty of integrating the method in regular packaging practice (Joyce and Patterson 1994), requirement for special equipment to apply this technology, or consumer reluctance about this type of package due to its association with plastic waste (Morris and Jobling 2002). However, a marketing study conducted in Israel and in Korea reveals a positive attitude of consumers in both countries to seal-packaged citrus fruit, including their willingness to pay a premium price covering the cost of packaging (Lee et al. 1997). Furthermore, this technique is implemented by many supermarkets in order to preserve the produce quality during marketing. The benefits of applying seal packaging immediately would accrue over time after harvest. B. Compromise Approaches The method of individual shrunk-seal packaging prevents water condensation on the produce surface due to the unique package geometry, which follows the shape of individual fruit. This approach controls condensation practically without compromising the high level of inpackage humidity and therefore provides a standard of MHP efficacy (Joyce and Patterson 1994). Most other MHP approaches are based on a
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compromise principle: that is, reducing the risk of condensation by allowing decreased in-package humidity with a trade-off rise in water loss. In this case, the benefit is reached if the humidity level inside the package is low enough to prevent condensation but still is high enough to significantly reduce water loss compared with the produce kept without plastic packaging. For example, at storage conditions of 10 C and RH 99%, the dew point is 9.85 C; that is, a mere 0.15 C drop of temperature will cause water condensation on the inner plastic surface, eventually wetting the produce. If the in-package RH is reduced to 92%, a temperature fluctuation of 1.2 C will not cause condensation. Assuming that the air humidity in the storage facility outside the package is 85%, the MH package will save about half of the produce weight loss, since VPD values for 92% and 85% RH at the given temperature are 97 and 183 Pa, respectively. 1. Package Perforation. The desired reduction of in-package air humidity may be reached by using the relatively low water potential of the air outside the package. For this reason, the permeability of the packaging material to water vapor should be enhanced to a certain extent. Perforation is the simplest way to reduce the diffusion resistance of plastic film. Obviously, the higher the degree of perforation, the more significant is the influence of outside humidity on the in-package conditions. Fig. 5.5 presents RH levels inside polyethylene-lidded model packages with plastic area 0.03 m2 perforated with either 4 or 40 holes of 2 mm in diameter (total perforation areas of 0.04 and 0.4% of the film surface, respectively). Each model package contained two fruits of Keitt mango. The packages were kept at 24 C in thermostatic chambers under humidity conditions stabilized with saturated salt solutions. In the packages with 40 holes, the RH levels reached 96% and 93.2% when the outside humidity was 75% and 60% RH, respectively. The humidity changes inside the packages with 40 holes followed the RH fluctuations of the surrounding atmosphere. By contrast, the RH in the packages with 4 holes was practically independent of external RH fluctuations and remained at a level of around 99% RH with only negligible differences between the two outside humidity levels. As shown in Fig. 5.5, the measured RH levels were in good agreement with the predictions calculated on the basis of the mathematical model (Fishman et al. 1996a). Further experiments showed that such slightly decreased RH levels in highly perforated mango packages was sufficient to diminish condensation and at the same time to prevent shriveling, maintain relatively low weight loss, and allow normal ripening of mango
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Fig. 5.5. Relative humidity inside polyethylene-lidded model packages perforated with either 4 or 40 holes (2 mm in diameter) per film area of 0.03 m2, compared with predicted steady-state RH levels calculated from the model of Fishman et al. (1996). Each model package contains two mango fruit. The packages are at 24 C in thermostatic chambers under humidity conditions stabilized around 75 and 60% RH.
fruit (Morris and Jobling 1990; Ben-Yehoshua et al. 1996; Rodov et al. 2003). Using perforated polyolefin films in bell pepper packages allowed combining satisfactory weight loss control with reduced condensation and low incidence of Botrytis decay (Ben-Yehoshua et al. 1995, 1998;
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Fig. 5.6. The effect of packaging method on weight loss percentage, incidence of Botrytis decay and amount of condensed water in the packages of red bell peppers stored for 2 weeks at 8 C and 4 additional days at 20 C. The fruit are in telescopic cartons lined with either nonperforated polyolefin Cryovac MD (20 mm thick) or perforated polyolefin Cryovac SM60M (25 mm thick, 8 holes 0.4 mm per sq. inch), or not lined with any plastic film (control—regular carton). The plastic sheets are stapled to the inner carton surface. The individually sealed fruit are shrunk-sealed in the nonperforated MD polyolefin. The individually sealed peppers are in nonlined cartons. Each carton contains 4 kg of produce. The condensation was evaluated by determining weight gain of filter paper after wiping the fruit and the plastic surfaces to dryness. Values with the same parameter marked by different letters are significantly different (Duncan’s multiple range test, P ¼ 0.05).
Rodov et al. 1998). Fig. 5.6 presents the results of bell pepper storage trials in various types of custom-made telescopic cartons (Ben-Yehoshua, Rodov, and Perzelan, unpublished). Produce desiccation is the major problem of bell peppers stored in regular carton boxes (control) without plastic lining. Cartons lined with nonperforated polyolefin causes a sevenfold reduction in the water loss; however, the amount of condensed water in the package and the incidence of Botrytis decay increases approximately in the same proportion. Lining cartons with perforated Cryovac SM60M polyolefin film (total perforation area 0.16% of the film surface) greatly reduces condensation and prevents Botrytis decay; at the same time the produce weight loss is approximately half of that in the control. Notably, individual shrunk-seal packaging of peppers in the same polyolefin film as used for nonperforated carton lining reduces condensation and decay without compromising produce weight loss.
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In beetroot storage, plastic packaging is beneficial for maintaining turgor and reducing weight loss and shriveling. Using perforated polyethylene bags prevents root sprouting, which takes place in nonperforated packages (Tessarioli et al. 1998). Similarly, packing corms of cocoyam (Xanthosoma) in perforated plastic bags reduces water loss and maintains better appearance without the increase of decay and sprouting that occurs in nonperforated packages (Mbonomo et al. 1991). However, plastic perforation is not always sufficient as a sole means to prevent decay. In some cases, the perforation has to be combined with additional pathogen-controlling measures. For example, the best results with cocoyam storage are obtained when perforated packaging is combined with curing and washing in chlorinated water (Mbonomo et al. 1991). Sealing in perforated polyolefin film is insufficient for decay control of mandarins and cannot substitute for fungicide treatment (Peretz et al. 1998). Choosing a proper perforation level is critical for achieving desirable results. For example, the amount of condensed water in model polyethylene packages containing two mango fruit is reduced fivefold by increasing perforation area from 0.2 to 0.7 cm2 per package (0.25% and 0.89% of the total film area, respectively) (Ben-Yehoshua et al. 2001b). Ben-Arie et al. (1995) provides an example of empirical optimization of perforation in polyethylene grape packages for simultaneous control of decay, desiccation, berry splitting, and sulfur dioxide (SO2)-caused bleaching. Polyethylene bags of 25-, 35.5-, or 50-micron thickness and 0, 0.2, 0.4 or 0.6% perforation were tested for storage of sapota (sapodilla) fruit (Joshua and Sathiamoorthy 1993). The best spoilage control is reached with bags 25 micron thick and 0.4% perforation, while the highest spoilage takes place in nonperforated bags. It should be kept in mind that resistance of plastic packages toward oxygen and carbon dioxide is normally affected by perforation much greater than their resistance toward water vapor diffusion (Fishman et al. 1996a,b; Chung et al. 2003). This phenomenon may be related to the fact that, when expressed in comparable units, permeability values for water vapor of most plastic packaging materials are usually one to three magnitude orders higher than those for oxygen (Greengrass 1999), while the “permeabilities” of holes for these substances (i.e., their diffusion coefficients in air) are quite similar (Nobel 1974; Chung et al. 2003). Therefore, puncturing a film adds similar values to its permeabilities toward oxygen (O2) and water (H2O), but the relative contributions of these added values are very different. In addition, the in-package levels of RH, O2 and carbon dioxide (CO2) are affected by the fact that the rate of moisture diffusion through the produce surface is a couple of orders of
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Fig. 5.7. Relative contribution of perforations to oxygen and water vapor permeance of model polyethylene packages (20 mm thick, 0.03 m2 film area) containing two mango fruit. Calculations performed on the basis of the model of Fishman et al. 1996a.
magnitude higher than that for the respiratory gases (Cameron et al., 1995). Fig. 5.7 represents relative contributions of holes and of plastic matrix to oxygen and water vapor permeation through low-density polyethylene films possessing different numbers of 0.5-mm holes, calculated using the model of Fishman et al. (1996a). According to the calculation, a single 0.5-mm hole in a package of total area of 0.03 m2 (perforation of just 0.00065% of the total film area) will account for 88.5% of the total oxygen diffusion through the package but only for 11% of the water vapor diffusion. In other words, in this situation almost 90% of the oxygen will pass through the perforations while almost 90% of the water vapor passesthrough the plastic. With 10 holes of the given size, about 99% of the oxygen flux is directed through perforations, but the water vapor permeation is distributed almost equally between the holes and the plastic matrix. This basic phenomenon has important practical consequences for the design of modified-humidity and modified-atmosphere packages of fresh produce. On one hand, it enables omitting undesirable hypoxic conditions that may develop in nonperforated packages while still keeping high humidity in the package and controlling produce desiccation, as shown with mango fruit (Rodov et al. 1997b, 2003; Morris and Jobling 2002). On the other hand, due to the misbalance in perforation effects on water vapor and gas permeabilities, it seems hardly possible to
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use perforation for simultaneous optimization of humidity and modified atmosphere composition in the package. Tiny openings of 50 to 100 mm in diameter produced in microporous or microperforated films for regulating O2/CO2 transmission rates (e.g., P-Plus film currently marketed by Amcor Flexibles, Australia) have a negligible effect on inpackage humidity and do not prevent in-package condensation. In turn, the degree of perforation sufficient for a measurable reduction of in-package humidity and condensation will nullify any respirationrelated modification of O2 and CO2 concentrations in the atmosphere. That is why perforation-based MHP is less suitable for commodities benefiting from reduced O2 and elevated CO2 concentrations. For example, with peeled garlic cloves, highly perforated bags perform worse than nonperforated ones (Lee et al. 2000). The perforated polyolefin Cryovac SM60M (perforation area 0.16%), which considerably improves the keeping quality of bell pepper, gives unsatisfactory results with trimmed sweet corn (Rodov et al. 2000). Packages of sweet corn are especially prone to condensation due to the intense transpiration and respiration of the produce and low storage temperature. The spoilage in the highly perforated sweet corn packages is enhanced, apparently due to the fact that the degree of perforation used does not support the buildup of a beneficial modified atmosphere but still cannot prevent the accumulation of condensed water. At the same time, packaging with lower perforation area that allows the achievement of desirable O2 and CO2 concentrations is beneficial for sweet corn storage (Riad et al. 2002). 2. Packaging Materials with Enhanced Water Vapor Permeability. As shown, plastic matrices play a significant role in water vapor transmission through packaging material. Therefore, the package permeability toward water vapor may be enhanced not only by perforation, as described in the previous section, but also by choosing a relatively hydrophilic plastic material with suitable barrier properties. When moisture control does not rely on film perforation, the improved humidity conditions may be combined with the benefits of the modified atmosphere (MA). Furthermore, in this case, humidity and atmospheric composition inside the package may be manipulated independently, by varying matrix composition to achieve a desirable RH and perforation level to optimize the MA composition. Some polymers possess relatively high permeability toward water vapor, markedly exceeding the transmission rates of polyethylene or polypropylene commonly used for produce packaging. The list of these materials includes, in particular, ethylene vinyl acetate (EVA), polyamide (PA, nylon), polyester (polyethylene terephthalate, PET),
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polystyrene (PS), and polyvinyl chloride (PVC) (Day 1993; Greengrass 1999). Applicability of these films to MH packaging of fruits and vegetables depends on their mechanical properties, cost, barrier properties toward oxygen, and other parameters. Some of these films (e.g., EVA, PS) have high oxygen transmission rate, while others, such as PA or PET, are rather resistant to gas permeation. In the latter case, gas permeability may be enhanced by microperforation. Barron et al. (2002) tested two hydrophilic materials, biodegradable wheat gluten–based film and polyether polyamide copolymer (Pebax , Elf Atochem, France), as packaging materials for mushrooms. The use of Pebax film results in detrimental levels of CO2 and O2. At the same time, packaging mushrooms in wheat gluten film allows attainment of a desirable atmosphere composition (i.e. low levels of both CO2 and O2). However, the possibility of commercial application of this film for produce packaging is limited due to its poor mechanical and sealing properties. Polyamide film was tested by Ben-Yehoshua et al. (1998b) as a lining layer for telescopic cartons used in bell pepper packaging, in comparison with nonlined and polyolefin-lined cartons. Polyolefin liners are most efficient in reducing produce weight loss but characterized by abundant water condensation and high incidence of gray mold caused by Botrytis cinerea (above 12%). Gray mold incidence in polyamide-lined packages and in nonlined cartons does not exceed 1.5%. The polyamide liners delay produce shriveling and allow a twofold reduction in the weight loss compared with regular cartons without plastic lining. A series of plastic films with enhanced water vapor permeability is currently being marketed under a commercial name Xtend (Aharoni et al. 1997, 2007). Xtend (also nicknamed XF), a hydrophilic plastic packaging, was developed in the mid-1990s by StePac L.A. Ltd, Tefen, Israel, in cooperation with Agricultural Research Organization, Israel (Nir et al. 2001). The film is manufactured by coextrusion of proprietary blends consisting of different polyamides with other polymeric and nonpolymeric compounds. The different blends allow manufacturing materials varying in water vapor permeability, in accordance with required in-package RH levels. The water vapor transmission rates (WVTR) of the three most common XF films (20-mm thick) are 6 1010, 19 1010, and 25 1010 mol m2 s1 Pa1, compared with 12 1011 mol m2 s1 Pa1 for low-density polyethylene. The least water-permeable film of the series has a WVTR value close to those of polyvinylchloride (PVC) and to highly perforated Cryovac SM60M polyolefin (7.9 100 and 4.4 1010 mol m2 s1 Pa1, correspondingly), while in more hydrophilic XF films the WVTR
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values are three to four times higher. The barrier properties noted were provided by plastic producers and converted to SI units according to Banks et al. (1995). Oxygen permeance values of the Xtend plastic materials are very low, 24 1014 to 48 1014 mol m2 s1 Pa1 (i.e., about 2 orders of magnitude lower than that of polyethylene). It should be kept in mind that barrier properties of hydrophilic plastics depend on the presence of water in their matrix. In particular, water sorption was shown to reduce the resistance of polyamide toward oxygen and polar organic volatiles such as ethanol (Sfirakis and Rogers 1980). Xtend films are microperforated in order to allow sufficient CO2 and O2 exchange. According to Day (1993), the typical O2 transmission rate of microperforated film is above 70.5 1012 mol s1 m2 Pa1 at 23 C (the data converted into SI units). The degree of perforation of the Xtend packages is typically in the range of 0.00012% to 0.0012%. Note that as shown in the previous section, this perforation level has practically no effect on the in-package RH. Packaging sweet corn in various films of the Xtend series provides RH levels between 95% to 98%, compared with >99% for polyethylene. Suitable Xtend materials can be chosen for either bulk or consumer packages of sweet corn, reducing the produce decay compared with polyethylene or iced control packages without visible denting of kernels (Aharoni and Richardson 1997). Nested packages, including PVCwrapped retail trays and removable external bulk Xtend liners, are proposed for reducing the risk of off-flavor development under nonrefrigerated shelf conditions (Rodov et al. 2000). The performance of Xtend packaging in storage of various vegetables has been presented for a range of examples in a new extensive paper by Aharoni et al. (2007). In this chapter, the performance of the Xtend packaging is illustrated by its effect on the keeping quality of summer squash (Fig. 5.8). Fig. 5.8 compares the effects of Xtend versus polyethylene liners on summer squash storage. The fruit of cocozelle type (cv. Erlica) were packed in commercial cartons lined with microperforated Xtend or polyethylene films or covered with paper (control). The atmosphere composition in polyethylene and Xtend liners is similar. Both films inhibit yellowing of summer squash during storage and reduce its weight loss, compared with control. As might be expected from the WVTR values, polyethylene is more efficient than the Xtend film for weight loss reduction. At the same time, the disease incidence in Xtend packs is five times as low as in polyethylene liners due to reduced condensation and four times as low as in the control due to inhibited senescence and direct antifungal MA effects (Rodov et al. 2004).
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Fig. 5.8. Effect of packaging method on weight loss, color changes, and decay incidence of summer squash after 16 days of storage at 10 C and 3 additional days at 20 C.
The humidity-favoring bacterium Pseudomonas lachrymans prevails in polyethylene-packed squash while the gray mold Botrytis cinerea is one of the major decay causes in the control. The advantages of microperforated Xtend liners over polyethylene packages (either perforated or nonperforated) were reported also for the storage of mango (Pesis et al. 2000), snap beans (Fallik et al. 2002), cherries and nectarines, but not for plums (Lurie and Aharoni 1998). Additional examples of superior performance of Xtend packages in comparison with microperforated polyethylene for storage of broccoli, green onion, parsnip, and cucumbers were presented by Aharoni et al. (2007).
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The Xtend packages are nowadays applied commercially in various regions (North, Central and South America, South Africa, Europe, Middle East) with about 40 commodities, including melons, cherries, bananas, avocado, cucumbers, squash, asparagus, broccoli, sweet corn, green onion, green beans, and other fruit and vegetables. 3. Hygroscopic Additives and Humidity Buffering. Another alternative for reducing in-package humidity, instead of releasing the excessive water vapor to the outside space, may be to entrap it in hygroscopic material located within the package space or in its walls. The attractive feature of this approach is that when needed (e.g., when atmospheric water potential in the system decreases), the moisture may be released back to the atmosphere, thus stabilizing its RH at a desirable level (humidity buffering). The humidity of a package atmosphere can be stabilized with hygroscopic materials, such as salts and polyhydric alcohols (polyols). Shirazi and Cameron (1992) demonstrated the control of RH in tomato packages by using microporous sachets containing sorbitol, xylitol, sodium chloride (NaCl), or other compounds with type III sorption isotherm behavior. This packaging method extends the storage life of tomatoes, mainly by retarding surface mold development. Inserting NaCl-containing mesh cloth bags into package space prevented half of the decay incidence of muskmelons stored in polyethylene-wrapped cartons (Yahia and Rivera 1992). However, the positive effect of sodium chloride is observed only with a relatively short storage duration (10 days at 5 C and 2 additional days unwrapped at 20 C). No significant advantages of adding a hygroscopic material occur with melons stored for 20 or 30 days. Buffering the in-package RH by the use of sodium chloride–containing sachets reduces decay and extends storage life of red bell pepper sealed in low-density polyethylene (Rodov et al. 1995). Humidity level in a package containing 0.5 kg fruit and stored at 8 C is ca. 88% with 15 g NaCl, 92% to 95% with 10 g NaCl, about 97% with 5 g NaCl, and close to saturation (>99%) without a hygroscopic material (Fig. 5.9). The addition of NaCl prevents or significantly reduces the accumulation of condensed water on the fruit and on the inner film surface and reduces decay incidence. Obviously, the hygroscopic material increases the atmospheric VPD and the weight loss of the fruit compared with polyethylene packages without sodium chloride. However, peppers packaged with NaCl still lose less weight and have higher firmness than the control fruit kept in standard cartons. The water regime that develops in the presence of 10 g NaCl improves the balance between reduced fruit desiccation and inhibited pathogen development.
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100
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ADDITION OF 10 g NaCl
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HOURS Fig. 5.9. Effect of hygroscopic insert on relative humidity level in nonperforated retail package (20 mm thick polyethylene) containing 0.5 kg of bell pepper. Reprinted with permission of ASHS from Rodov et al. 1995.
Modified humidity packaging of Agaricus mushrooms in the presence of sodium chloride– or sorbitol-containing sachets was described by Roy et al. (1996). Packages containing 10 or 15 g sorbitol result in better appearance of mushrooms than those with 5 g sorbitol or without any hygroscopic additive. The RH level of 87% to 90% attained in packages with 10 or 15 g sorbitol is considered optimum for mushrooms. Using a silica gel humidity absorber reduces microbial contamination of polyethylene-packaged Agaricus and Pleurotus mushrooms (Popa et al. 1999). However, Villaescusa and Gil (2003) in their study with Pleurotus conclude that hygroscopic materials (sorbitol or silica gel) do not improve the quality of this mushroom sufficiently to justify acceptance of the additives by consumers. DeEll et al. (2006) recently examined the effect of sorbitol-containing sachets on the quality of broccoli stored in modified atmosphere packages in the presence of another type of additive: volatile absorbers containing potassium permanganate (KMnO4). After 29 days of storage
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at 0 to 1 C, broccoli heads in packages with sorbitol have better appearance, firmness, and odor ratings compared with the controls. A slight increase in weight loss ( 1.3%) occurs with the addition of sorbitol, although not at a level that would affect produce marketability. Overall, the use of sorbitol with KMnO4 in MAP enhances the removal of off-odor volatiles and maintains the quality and marketability of the produce. A humidity buffer for maintaining a predetermined RH level in a sealed container was developed and patented by Patterson (1991). The buffer is comprised of a water-swellable, water-insoluble polymer and a mixture of a nonvolatile hydrophilic liquid and water. It may be manufactured in the form of sheets or free-flowing granules. Another humidity-controlling agent for preservation of food products, comprising equal proportions of polyacrylic acid (sodium salt), potassium carbonate, and silica gel, was formulated and optimized by Liu and Chiang (2000). The formulation maintains the RH in polyethylene bags with pak-choi leaves at ca. 87% at 25 C and extends the shelf life of the produce. Water vapor may also be absorbed from the atmosphere by porous mineral materials, such as clays or zeolites. The addition of natural clay adsorbent almost eliminates condensation in raspberry packages and reduces decay (Toivonen et al. 2002). Zeolite-based moisture absorbent prolongs storage life of fresh figs packaged in plastic film (Matteo et al. 1999). A range of humidity-controlling package inserts or packaging materials are manufactured commercially. In particular, available desiccant products include Desi Pak (based on bentonite clay), Sorb-it (silica gel), Tri-Sorb (molecular sieve), Getter Pak (activated carbon) and 2in-1 Pak (silica gel or bentonite clay with activated carbon) manufactured by Sud-Chemie, Germany (formerly United Desiccants, U.S.), as well as MiniPax and StripPax packets, NatraSorb and TranSorb bags, and DesiMax patch from Multisorb Technologies Inc., U.S. (Suppakul et al. 2003). These are only some of the brands available commercially to protect packaged products from moisture. A humidity control device for maintaining a desired humidity inside packages or containers has been patented (Saari 1999; Saari and Esse 2005) and marketed under a commercial name Humidipak (Humidipak, U.S.). The device includes a protective case, a water vapor–permeable pouch, and a thickened saturated salt solution having a suitable humidity control point. The manufacturer claims that it allows humidity buffering by either adding or removing moisture to/from the air (termed two-way moisture control) and maintaining in-package RH at any predetermined level, from 10% to 95% RH under variable temperature conditions.
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Esse (2005) indicates that “Humidipac” sachets stabilize humidity levels inside fresh-cut produce packages, extending their shelf life by up to 20%. Humidity-buffering packaging film has been produced by Showa Denko (Japan) under the trade name Pichit for more than 10 years. The Pichit moisture-removal sheet includes hygroscopic material (presumably propylene glycol) and a carbohydrate enclosed between two layers of plastic highly permeable to water vapor (Rooney 1995). It is marketed for home use as a wrapping material that delays foodstuff spoilage by controlling the RH around the product. Another humidity-absorbing plastic film brand is the Everfresh bag (Aisaika, Japan) made of polyethylene impregnated with volcanic ash containing the moisture absorbent silicic acid anhydride (Laszlo 1991). Packaging in mineralimpregnated bags prevents the accumulation of condensed moisture, reduces decay incidence, and extends life of stored guava fruit, compared with nonimpregnated polyethylene packages (Combrink et al. 1990). However, the positive influence of Everfresh bags on grape storage is inconsistent (Laszlo 1991). No significant positive effects of mineral absorbers incorporated in plastic films were observed in our own studies (Rodov and Ben-Yehoshua, unpublished; Aharoni, unpublished). Another step in controlling humidity during storage of fruits and vegetables is represented by membrane contactors (Dijkink et al. 2004). The contactor is a hollow-fiber membrane through which a desiccant solution (humidity buffer, e.g., glycerol/water) is circulated. The membrane is brought in contact with air and may either humidify or dehumidify it depending on water potential gradient between the desiccant and the atmosphere. The system includes a desorber for regeneration of the used desiccant solution. In green bell peppers, red currants, and pears, the contactor storage system reduces produce losses caused by shriveling and fungal decay. Membrane contactors may be used in stationary storage chambers or in bulk transportation containers. However, their application in smaller packages is difficult to conceive. 4. Liquid Absorption. The approach described in this section is similar to the previous one, with the difference that water molecules are intercepted by a hygroscopic material from the liquid phase, not from the vapor one. Accumulation of liquid on the package bottom may result either from draining condensed water, especially in packages containing antifog (antimist) additives, or from direct dripping from the produce (e.g., from fresh-cut fruits). Several companies manufacture drip-absorbent pads or sheets aimed at preventing liquid accumulation that may foster produce spoilage and hamper marketing appeal.
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A drip-absorbent sheet usually consists of two quilted layers of a microporous or nonwoven material, with granules of superabsorbent polymer between them. Polyacrylate salts often are used to absorb the water, although graft copolymers of starch can also be utilized (Rooney 1995). These polymers are capable of absorbing 50 to 500 times their own weight in liquid. Another way to immobilize water is by using a surface alloy of a hydrophilic polymer on a bulk hydrophobic surface as described by Noda (1991). The examples of drip-absorbent products include Toppan produced in Japan, Thermarite and Peaksorb from Australia (Rooney 1995; Suppakul et al. 2003), Containermat and Flower Dry from the Netherlands (Anonymous 2001), and Fresh-r-Pax from the United States (Gautreaux 2001). In addition to pads and pouches, the latter brand (product of Maxwell Chase, U.S.) is manufactured in the form of trays and cups with liquid-absorbing layers, suitable for fresh-cut fruit and vegetables as well as for meat, fish and dairy products (Brander 2005). Using paper inserts is a simple and cheap solution for absorbing surplus water condensed inside plastic packages of fruit or vegetables (Ben-Arie et al. 1995; Fallik et al. 1995; Meir et al. 1995). Morris and Jobling (2002) reported improvement in visual and microbiological quality of mushrooms packaged in polyethylene bags by using paper inserts. The performance of these packages is further markedly improved by addition of antimicrobial eucalyptus oil. However, the use of paper inserts is not always efficient, in particular because such inserts usually have limited direct contact with water droplets condensed on the package walls. A condensation-control carton capable of collecting the condensed water from the package surface was designed by Patterson and Joyce (1993). The design is comprised of a fiberboard carton with a multilayer structure where water collects in the internal wicklike layer and is released in vapor form in response to lower RH. Therefore, this modified-humidity package combines the principles of liquid absorption and humidity buffering. The structure and performance of condensation-control cartons are described in detail by Patterson et al. (1993) and Rooney (1995). However, currently this development is not applied commercially (Morris and Jobling 2002). C. Mathematical Modeling of MH Packaging MHP reaches its target only if all the elements of the packaging system (i.e., produce amount, film permeability, extent of perforation, hygroscopic inserts) are tuned to produce requirements and expected storage conditions. Otherwise, the effect may be opposite to expectations,
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resulting in either produce desiccation or in accumulation of condensed water and increased decay. Optimization of MH package design can be facilitated by the use of mathematical modeling. As shown in previous sections, the water regime of packaged harvested commodities is based on known physical fundamentals and can be described mathematically. However, in-package humidity modeling has received much less researchers’ attention than modeling oxygen and carbon dioxide dynamics, possibly because it seemed too obvious at first glance. Nowadays, in view of novel modified-humidity approaches, such as hydrophilic films with RH-dependable barrier properties, macro- and microperforation, and humidity buffering and moisture absorbers, this task no longer appears trivial. A numerical model of gas exchange in microperforated packages including water vapor, oxygen, carbon dioxide, nitrogen, and argon was built by Renault et al. (1994) using Stephan-Maxwell and Fick’s laws. The Fick’s law approach was further used by Fishman et al. (1996a,b) in order to mathematically describe the effect of perforation on RH and oxygen concentration in a package containing fresh fruits. In particular, this model theoretically substantiated the fact that in-package oxygen concentration is affected by perforation much more than atmosphere humidity. Practical consequences of this phenomenon have been discussed in previous sections. The model allows prediction of in-package RH dynamics and produce weight loss as affected by produce specificity, package perforation level, and ambient humidity. Further development of the model for gas and water vapor exchange in perforated packages was done by Lee et al. (2000). Validation under controlled experimental conditions showed fairly good agreement between experimental results and theoretical predictions. However, when applying the model to commercial-size packages of highly perforated Cryovac SM60 film containing 0.5 kg of peeled garlic cloves, results deviate considerably from the predicted RH value. Most probably, the vapor flow through part of the perforations in densely packed commercial packages is blocked or hindered by the produce, resulting in higher RH than the model estimation (88% RH instead of the predicted 61%). Not surprisingly, the conditions formed in these packages do not inhibit spoilage of humidity-sensitive garlic, especially in the absence of a beneficial modified atmosphere. The effect of moisture absorbents on relative humidity in modifiedatmosphere packages of blueberry was modeled by Song et al. (2001, 2002). The difference between the experimental and predicted RH was within 2%. Satisfactory prediction of in-package RH may allow
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calculating the expected VPD and Ywv values of the in-package atmosphere in order to optimize the required amount of a hygroscopic additive. Package geometry is an additional factor to be considered in MHP modeling. The performance of perforated polyethylene liners as a means to reduce water loss of apples in multilayer cartons was modeled by Tanner (2001). The model described the conditions in different fruit layers within the carton and showed that humidity and weight loss values are not uniform throughout the package space, in part due to the moisture-absorbing effect of paper-based cushioning trays. Moreover, it revealed the locations within the package where the produce is most vulnerable to moisture loss. The study resulted in recommendations for improving package performance. Probably one of the most detailed models describing gas and water vapor flux within produce-containing packages was developed by Cazier (2000). The model allowed simulation of moisture distribution within the package volume (in particular the formation of a water-saturated boundary layer in the produce vicinity) as affected by stomata and by plastic microperforations. Application of the model may improve the efficacy of perforated MH packages by predicting optimal perforation locations. The next step in MHP/MAP modeling should be integration with produce-keeping quality parameters, not only in terms of weight loss but also condensation-associated decay risk and other spoilage processes. The published integrated model of a modified-atmosphere package (Hertog et al. 1999) describes spoilage as a function of atmospheric composition but ignored the humidity factor in spite of its acknowledged importance (Hertog et al. 1997a, 1997b). Integrating humidity, atmospheric composition, and temperature conditions together with produce quality parameters in one model may be of help for optimization of postharvest technologies. One should keep in mind, however, the limitations of applying mathematical modeling to biological objects due to their variability and complexity (Cameron 2001).
VI. SUMMARY Water availability is critical for the existence of plant organs. In agreement with universal thermodynamic laws, water moves spontaneously in the direction of decreasing free energy, expressed as water potential. The ambient atmosphere normally has a much lower water potential than plant tissues, so plants continuously lose water to the atmosphere by transpiration. In contrast to whole plants, detached organs cannot
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replenish moisture loss by water uptake from the soil. Therefore, water status of harvested commodities is determined by their interaction with the atmosphere. An artificial environment with a relatively high air water potential (vapor pressure close to saturation) is essential for preservation of fresh produce. Packaging in plastic films is one of the ways to diminish the water potential gradient between the produce and its environment. The resistance of most plastic films to water vapor diffusion far exceeds the barrier properties of produce surfaces. As a result, most water molecules evaporated from the produce remain within the package space, enhancing the humidity of the in-package atmosphere. Under near-saturation conditions inside the package, even minor temperature fluctuations may result in precipitation of condensed water, wetting the produce and stimulating pathogen development. The major challenge of modifiedhumidity packaging (MHP) is in finding solutions for reducing the risk of water condensation while still maintaining the produce water loss as low as possible. Individual shrunk-seal packaging provides a yardstick standard of MHP efficacy controlling condensation practically without compromising the high in-package humidity. In this method, the shrunk film tightly covers the produce. The chance of water condensation within the inner space of such packages is diminished due to the very small void volume and negligible temperature difference between the produce and the film surfaces. However, this approach is applicable only to a limited number and type of produce. Other MHP approaches are based on a compromise principle. The benefit is reached if the humidity level inside the package is low enough to prevent condensation but still high enough to reduce water loss compared with produce without plastic packaging. The in-package humidity may be lowered in particular by reducing barrier properties of the package toward water vapor. Perforation is the simplest way to enhance the permeability of a plastic film. However, perforation affects the film’s permeability to oxygen and carbon dioxide to much greater extent than its resistance to water vapor. The degree of perforation sufficient for a measurable humidity reduction in a typical polyethylene package nullifies the formation of a modified atmosphere (MA) in it. The perforation-based MHP is less suitable for commodities requiring reduced O2 and/or elevated CO2. Another MHP approach is based on using a relatively hydrophilic plastic material with suitable barrier properties toward water vapor. This approach allows combining MH and MA advantages. A series of microperforated packaging materials based on polyamide-comprising blends with enhanced water vapor permeability is manufactured commercially. Optimization of humidity
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in these packages is based on selecting an appropriate plastic blend and optimization of atmospheric composition on varying film microperforation level. Instead of releasing the excessive moisture to the outside atmosphere, it can be entrapped in a hygroscopic material located within the package space or in its walls. In case of decreasing atmospheric water potential in the system, the moisture may be released back to the atmosphere, thus stabilizing its humidity at a desirable level (humidity buffering). Substances used for intercepting excessive water vapor from the atmosphere include salts, polyhydric alcohols, porous minerals, hydrophilic liquids (e.g., propylene glycol and water-swellable polymers such as polyacrylate salts). The latter materials, as well as cellulose (e.g., paper) are also used for absorbing liquid water accumulated in the package. The performance of MH packages is based on known physical fundamentals and can be described mathematically. Mathematical modeling of MHP allows optimizing the elements of the packaging system, such as produce amount, package dimensions, film properties, perforation, and hygroscopic additives. Further steps in MHP/MAP modeling should include integration with keeping-quality models and predicting the produce spoilage rate as a function of package parameters.
ACKNOWLEDGMENTS We are grateful to Dr. Svetlana Fishman for the fruitful discussion of perforation effects on the permeability of plastic films for oxygen and water vapor and ways of mathematical modeling of these effects.
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6 Ecological and Genetic Systems Underlying Sustainable Horticulture Autar K. Mattoo and John R. Teasdale Sustainable Agricultural Systems Laboratory USDA-ARS, Animal and Natural Resources Institute The Henry A. Wallace Beltsville Agricultural Research Center Beltsville, MD 20705–2350, USA ABBREVIATIONS I. INTRODUCTION II. ECOLOGICAL SYSTEMS A. Conventional versus Organic: Principles and Distinctions B. Agroecological Principles of Soil Management C. Soil Fertility and Nutrient Availability D. Weed, Disease, and Pest Management E. Crop Rotation F. Cover Crops in No-Tillage Systems III. GENETIC SYSTEMS A. Legume Metabolism and Functional Molecules B. Other Nitrogen:Carbon Interactive Metabolites C. Legume-Arbuscular Mycorrhizal Fungus Interactions D. Molecular Signature of Hairy Vetch–Grown Tomato E. A Working Model Explaining Hairy Vetch–Tomato Interactions F. Genotype Environment and N:C Interactions IV. AN INTEGRATED APPROACH TO SUSTAINABLE HORTICULTURE LITERATURE CITED
ABBREVIATIONS AMF Atxdh1 BP
Arbuscular mycorrhiza fungi Arabidopsis xanthine dehydrogenase gene Black polyethylene
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Bacillus thuringiensis toxin Cytokinin Cytokinin receptor kinase gene Gibberellins Gas chromatography–mass spectrometry Hairy vetch Auxin Substrate affinity constant Nicotinamide adenine dinucleotide phosphate Senescence-associated protein
I. INTRODUCTION Crop production and food security are high priorities on the list of global concerns to meet the food demands of the growing world population. It has been estimated that over the next 20 or more years, agricultural production needs to double from the same area of land (Norman Borlaugh quoted in Smaglik 2006). This poses a higher challenge particularly when a declining trend in crop yields and increasing water shortage is apparent in many nations (Rosegrant and Cline 2003). In the last century, conventional breeding strategies for large-scale farming in concert with fertilizer use and integrated pest management led to higher crop production (Trewavas 2001). Unfortunately, this increase in production impacted the world ecosystems and raised concerns for human and animal health because it relies heavily on chemical inputs of agrochemicals, synthetic fertilizer, and heavy machinery driven by fossil fuels (National Research Council 1989). The high usage of nonrenewable resources in conventional agriculture also resulted in loss of topsoil, reduced soil fertility, and contamination of the two major natural resources, water and air (Smil 1997). Preservation of yield and attractiveness, particularly for fruits and vegetables, continues to rely heavily on the use of pesticides. Thus, agriculture faces unprecedented challenges due to rising energy costs, global climate change, and increasingly scarce production resources. It will become imperative for producers to adopt sustainable systems that rely on natural processes and use inputs as efficiently as possible. Sustainable agricultural systems strive to achieve the general goals of productivity, profitability, and resource conservation while using local applications of these principles depending on climate, soils, and available markets. There are many approaches to achieving sustainability, ranging from organic farming with no synthetic inputs to conventional farming with the latest genetic and technological inputs. In
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this chapter, we highlight the development of production systems based on sound ecological principles as well as on physiological and genetic principles that hold the most promise for addressing the challenges of the 21st century. First we focus on organic farming because the systems approach that relies on ecological processes is most developed and clearly articulated by practitioners and researchers of this form of agriculture. Then, in the next section, the focus is on genetic systems and how these can underlie and supplement ecological approaches for improving agricultural systems. Finally, in the last section, we suggest the importance of integrating ecological and genetic approaches to optimize agroecosystem sustainability. II. ECOLOGICAL SYSTEMS A. Conventional versus Organic: Principles and Distinctions Organic farming is often defined by prohibited substances (e.g., synthetic fertilizers, pesticides, transgenic crops), but organic production can also be defined in positive terms relating to resource cycling, ecological balance, and biodiversity. Most organic farmers would agree that their goal is not simply “input substitution,” that is, substitution of organic forms of fertilizer and pesticide products into production systems that are otherwise unchanged. Instead, the focus is on designing a new production system that builds the means of fertility and pest management into agroecosystem processes that will support crop production (Drinkwater et al. 1995). Thus, conventional inputs are replaced not just by a different set of approved organic products but by the integrated functions of the agroecosystem itself. A major principle of organic agriculture is building soil organic matter as the underlying prerequisite for building the capacity to supply essential resources for crop production (nutrients and water) as well as for building the species diversity needed to maintain manageable pest and weed populations. The adage “feed the soil, not the crop” refers to taking a long-term systems approach to building the fertility and resilience of soils rather than taking a short-term approach to supplying growth requirements to crops. It is often difficult to determine the relative efficacy of these approaches to crop production because of the different time scales involved for optimizing each system. Changes in agroecosystem processes associated with converting from conventional to organic management, especially processes based on soil organic matter, can take many years or even decades to reach a new equilibrium. Thus any assessment of the efficacy of organic production must be conducted over a long-term temporal scale to capture underlying soil dynamics (Drinkwater 2002).
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B. Agroecological Principles of Soil Management Most benefits of organic soil management can be linked with high organic matter inputs to soils. This is accomplished by keeping crops or cover crops continually growing throughout the year and by adding organic amendments from external sources as needed. Soils with a history of organic farming sequester higher levels of soil carbon than corresponding conventional soils, both in horticultural systems (Ciavatta et al. 2008; Melero et al. 2008) and in agronomic systems (Marriott and Wander 2006b). Increased soil organic carbon has been associated with increased productivity of soils resulting in higher crop yield potential in organic than conventional systems after soil carbon (C) has become higher in organic systems (Fig. 6.1). Organic soils with higher organic matter levels often have higher capacity to capture and store essential nutrients, such as nitrogen (N) (Marriott and Wander 2006a), and water resources (Sangakkara et al. 2008). Higher organic matter also leads to higher soil aggregate stability, which is associated with higher microbial and earthworm biomass and mycorrhizal colonization in long-term organic soils (M€ ader et al. 2002). High soil organic matter is also associated with richer food webs and higher biological activity that drive soil ecological services (M€ ader et al. 2002). Conservation tillage practices also promote many of the same goals for soil improvement as organic farming systems, including sequestering carbon, improving soil nutrient and water-holding capacity, resisting sediment and nutrient losses, and enhancing soil biological activity (Peign e et al., 2007). The adoption of conservation tillage systems in conventional agriculture, particularly no-tillage, has been facilitated by the advent of herbicide technology and transgenic crops for control of weeds that otherwise would become more problematic with the elimination of tillage. For example, absence of tillage in organic cropping systems led to lower crop yields due to increased weed competition and lower nitrogen mineralization (Drinkwater et al. 2000). It has been suggested that organic systems cannot attain the same degree of soil stewardship because, without herbicides, weed control and seedbed preparation require tillage operations that oxidize soil organic carbon and destroy soil structure (Trewavas 2004). However, research has shown that organic systems, despite the tillage required, can build soil carbon and yield potential of soils beyond that achieved by conventional no-tillage systems (Teasdale et al. 2007). Organic farmers could potentially reduce tillage and gain additional soil benefits by both diversifying rotations to include perennial crops as well as by combining minimum tillage practices with recent technologies for mechanically suppressing
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Fig. 6.1. Maize yield as a function of total soil carbon (A) or nitrogen (B) in a uniformity trial following nine years comparison of reduced-tillage organic (solid symbols) and conventional no-tillage (open symbols) systems. Data are from Teasdale et al. (2007).
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high biomass cover crops that can substitute for herbicides in suppressing weeds. (These options are discussed later in the chapter.) There also are opportunities for conventional farmers to improve their systems by increasing organic inputs, such as by diversifying rotations with cover crops (Calegeri et al. 2008). C. Soil Fertility and Nutrient Availability Some have suggested that soil fertility is “fundamentally different” in organic systems than in conventional systems (Drinkwater et al. 1995); however, others have concluded that the fundamental processes driving nutrient cycling do not differ but that the primary differences are related to the quantity and quality of inputs (Stockdale et al. 2002). Nutrients delivered in organic forms, either from in situ crop or cover crop residue or from organic amendments, usually are present in lower concentrations than in fertilizers and require large quantities of material either to be grown as a rotational green manure or delivered to fields from off-site locations to meet crop growth requirements. Most organic materials do not contain a large amount of readily soluble nutrients; hence, nutrient availability in organically farmed soils is dependent on soil processes for nutrient mineralization. Substrate decay dynamics and nutrient mineralization are affected by soil microbial activity, which in turn is affected by soil environmental conditions such as temperature, moisture, and aeration as well as soil chemical properties, particularly the ratio of carbon and nitrogen (Gaskell et al. 2006). Soil microbes are carbon limited; organic amendments with higher extractable carbon have been shown to increase microbial biomass, microbial respiration, and nutrient mineralization in organic vegetable production systems (Tu et al. 2006; Melero et al. 2008). In general, mature organic farming soils often have lower levels of soluble nutrients, especially inorganic nitrogen, at any given time but have a greater capacity to mineralize nutrients than conventional soils (Drinkwater et al. 1995; Poudel et al. 2002; Miller et al. 2008). Because soluble nutrients are not readily available and their release depends on microorganism-mediated processes, mineralization is not necessarily synchronized with crop demand (Gaskell et al. 2006, Evanylo et al. 2007). Amendments with a high carbon to nitrogen ratio can immobilize nitrogen into microbial biomass and reduce immediate availability and uptake by crops (Rodrigues et al. 2006) despite the potential long-term impact high carbon amendments can have on nutrient availability. Most reports of inadequate nutrient availability leading to poor crop yields in organic versus conventional systems have been associated with experiments where organic systems have been
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maintained for less than 10 years and there probably was insufficient time to develop adequate mineralization potential (Rodrigues et al. 2006; Cavigelli et al. 2008). Most reports of adequate fertility and equivalent yields between organic and conventional systems are based on systems in place for at least 10 years (Pimentel et al. 2005). In addition to the problem of synchronization, the ratio of nutrients in organic materials may not match requirements of crops. For example, the nitrogen (N) to phosphorus (P) ratio in composted amendments is usually lower than that required by crops, leading to the dilemma whether to fertilize according to crop nitrogen requirement and oversupply phosphorus or apply to phosphorus requirements and undersupply nitrogen. Limited manure and compost application to organic fields because of nutrient management regulations limiting phosphorus application led to lower nitrogen availability in several years of a long-term experiment in Maryland (Cavigelli et al. 2008). However, Evanylo et al. (2007) showed that high annual compost rates could meet vegetable crop nitrogen requirements but would not increase phosphorus loss from fields because of improved soil physical properties leading to increased rain infiltration and reduced runoff volume. Thus, although organic farms may arrive at a new equilibrium with higher soil carbon, microbial activity, and mineralization potential after years of organic inputs, this process will still require careful management to meet the appropriate balance of nutrients required by crops and to avoid the buildup of excess nutrients that can pose an environmental hazard or the depletion of nutrients that could limit yields. D. Weed, Disease, and Pest Management Perhaps the most challenging aspect of organic farming is controlling weeds, pests, and diseases without use of agrichemical products that are the mainstay for crop protection in conventional agriculture. Although biologically based alternatives have been explored and some successes have been recorded, their major limitation has been inconsistency compared to the recommended agrichemical standards. For example, in a review of weed suppression by cover crops, Teasdale et al. (2007) found that suppression of weed biomass ranged from 0% to 99% by several cover crop species grown in different areas of the world. Although progress has been made developing biological agents for control of plant diseases, this approach has also been hampered by inconsistent performance (Compant et al. 2005; Roberts et al. 2005). The most promising approach for control of weeds, pests, and diseases is not through identification of single control tactics but through development of integrated systems that maintain populations of unwanted organisms
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within acceptable bounds (Lewis et al. 1997). This approach seeks to use preventive measures to limit weed/pest populations by a combination of system stresses, or “many little hammers” (Lewis et al. 1997; Liebman and Gallandt 1997). Thus, crop rotation, timing of planting, creating an attractive habitat for natural enemies, tolerant crop cultivars, competitive crop populations, optimizing soil fertility, and avoiding crop stress all may be insufficient alone but together may limit damage from weeds/ pests/diseases to acceptable levels. Since long-term changes in soil organic matter, nutrient mineralization potential, and biological activity are fundamental to the ecologically based management of organic farming, solutions to controlling weed, pest, and disease populations must also be integrated with these basic soil conditions. Drinkwater et al. (1995) have shown that soil nutrient management can have profound implications for plant-pathogen and plant-herbivore interactions, suggesting that the consequences of soil processes in organic systems extend to community-level mechanisms for regulating disease and pest populations. In their study of fresh-market tomato production on 20 organic and conventional farms, reduced corky root disease was associated with increased microbial activity, particularly cellulolytic actinomycetes, and lack of herbivory was associated with greater abundance and species richness of predators and parasitoids on organic farms. Additional mechanisms that involve crop responses can also contribute to crop protection. Induced resistance is a series of plant defense responses to invasion by pests or disease organisms that are mediated by the hormones jasmonic acid, salicylic acid, and ethylene (Walters and Heil 2007; Zheng and Dicke 2008). The specific transcriptional and metabolic events associated with induced resistance have been demonstrated for many crop-pest or crop-pathogen systems. There is generally a metabolic cost to the crop in the form of reduced growth or yield for this induction response; this finding explains the absence of these processes as a constitutive plant defense mechanism (Walters and Heil 2007). Because these costs are associated with reallocation of limited resources in some instances, the cost to crop growth or the expression of resistance can be a function of resource availability to the crop. For example, nitrogen has been shown to modulate the growth and seed yield costs of Arabidopsis to induction of pathogen resistance (Dietrich et al. 2004). These induced responses can also be sensitive to the presence of multiple species of pests and pathogens in an ecosystem that can result in a complex of signaling leading to negative and positive crosstalk between jasmonic acid and salicylic acid pathways (De Vos et al. 2005). Mutualistic symbioses involving mycorrhizal fungi and root nodule forming Rhizobium are highly critical to plant nutrient capture in
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organic systems but also can interact with induced resistance responses to pest or pathogens. These mutualistic organisms have been shown to induce resistance to certain diseases, but their function also may be impaired by resistance induction (Walters and Heil 2007). The important legume-rhizobial symbiosis that provides the plant with nitrogen (N) and the soil rhizobia with carbon is now thought to be mostly a plantcontrolled process (Caetano-Anolles and Gresshof 1991; Kawaguchi et al. 2002); this process appears to be interrelated to resistance induction by invading pests or pathogens as well. Thus, the agroecosystem functions of both nutrient acquisition and regulating crop and pest/pathogen interactions appear to be regulated by important subcellular processes. The linkage of these functions offers exciting management opportunities given greater understanding of these processes in the future. E. Crop Rotation A diverse crop rotation is fundamental to addressing the two major obstacles to the successful transition from conventional to organic farming, namely, weed control and nitrogen sufficiency. Most examples of the importance of rotation come from long-term agronomic studies, but the principles apply equally to horticultural crops. During the first 10 years of the long-term Beltsville Farming Systems Project comparing three organic rotations and two conventional systems, nitrogen availability and weed abundance explained 73% and 23% of the yield difference between conventional and organic maize. However, organic maize grown in a longer, more diverse rotation of maize-soybean-wheat-hay yielded higher, had higher nitrogen availability, and had lower weed abundance than organic maize grown in a standard maize-soybean rotation (Cavigelli et al. 2008). Long-term research in conventional systems showed that first-year maize following alfalfa did not require additional fertilizer nitrogen to optimize yield whereas second- and third-year maize following alfalfa did require fertilizer nitrogen suggesting that alfalfa can substantially meet first-year nitrogen requirements (Stranger and Lauer 2008). Additional research at the Beltsville Farming Systems Project showed that organic rotations with phenologically diverse crops provided a good example of systems-level dampening of soil weed seed populations (Teasdale et al. 2004) as discussed in the previous section. Including a perennial sod or hay crop in an organic rotation has many benefits, including building soil fertility and reducing weed populations, as outlined, but it also can contribute substantially to reducing the tillage frequency in the rotation and thus provide many of the same benefits conferred by reducing tillage. Thus, a rotational hay crop may provide not only nutrients to subsequent crops but also positive long-
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term changes in soil organic carbon, microbial activity, and aggregate structure (Karlen et al. 2006). It has been argued that increases in organic grain crop yield that result from following a rotational soil-building crop are misrepresented because they do not account for the land and time required to grow the soil-building crop (Trewavas 2002). When Olesen et al. (2002) computed the total grain yield across a four-year rotation, the benefit of inclusion of a grass-clover green manure crop in one of four years could not adequately compensate for the yield reduction of leaving one quarter of the rotation out of production of a cash crop. However, Schmutz et al. (2008) showed that fertility from green manure crops incorporated into moderate-intensity organic vegetable production systems without livestock or associated manure amendments could be economical. F. Cover Crops in No-Tillage Systems Many of the benefits of no-tillage and organic agriculture just described can be magnified by incorporating cover crops into rotations (Sustainable Agriculture Network 2007). Cover crops fix carbon that can input substantial amounts of organic matter to soil without requiring hauling expenses associated with soil amendments such as manure or compost. Legume cover crops fix nitrogen that can provide a substantial input of nitrogen for succeeding crops (Sainju and Singh 2008). Cover crops capture excess nitrogen and other nutrients from the soil, thereby preventing potential losses from the soil system. They cover the soil with a vegetative cover that prevents soil losses during heavy rainfall events. Residue remaining after the cover crop is killed can assist rainfall infiltration and prevent evaporation of soil moisture. They can displace or otherwise interfere with weed and pest populations. For example, organic tomatoes intercropped with turfgrass had higher resistance to leaf blight, higher root colonization by mycorrhizal fungi, higher photosynthetic capacity in the late season, and higher yields than when grown in clean tilled soil (Xu et al. 2008). Conversely, cover crops can have negative influences on cropping systems if not managed properly (Sustainable Agriculture Network 2007). They withdraw soil moisture reserves that may be essential to production of subsequent crops. They can tie up otherwise available nutrient resources if the carbon-to-nitrogen ratio is too high. They can interfere with planting operations if excessive levels of biomass remain on or near the surface of fields. And they can enhance certain weed and pest populations by providing resources and environmental conditions suitable for those species.
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A system for no-tillage planting of tomato transplants into a hairy vetch cover crop developed by Abdul-Baki and Teasdale (2007) has been extensively studied at the USDA-ARS Beltsville Agricultural Research Center. This system involves planting a hairy vetch cover crop on beds in fall, mowing the abundant biomass of vetch after danger of frost in spring has passed, and transplanting tomatoes or other summer vegetable crops through the mulch with a no-tillage transplanter. The system is not organic in that it utilizes fertilizer, herbicides, and fungicides, but levels of these are reduced compared to conventional systems. For example, tomatoes grown in the hairy vetch system required approximately half the amount of nitrogen required by those grown in the conventional system to obtain maximum yields (Abdul-Baki et al. 1997). Research over a 10-year period showed higher tomato yields and net returns using the hairy vetch system compared to a conventional black polyethylene system (Abdul-Baki and Teasdale 2007). Tomatoes in black polyethylene mulch initially grew at a faster rate than those in hairy vetch mulch, presumably because of faster soil warming under the black polyethylene. Later in the season, tomatoes produced greater leaf area and maintained that leaf area over a longer period in the hairy vetch mulch than in the black polyethylene mulch (Fig. 6.2). Leaf area duration was correlated to
Fig. 6.2. Extended duration of tomato leaf area when grown in a hairy vetch versus black polyethylene mulch. Week 10 designates the beginning of fruit harvest. Leaf area duration of tomatoes in hairy vetch equaled 2259 dm2 week1 compared to 1486 dm2 week1 in black polyethylene. Data are from Teasdale and Abdul-Baki (1997).
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yield and could explain the higher yield of tomatoes in the hairy vetch mulch. Higher leaf area was associated with delayed leaf senescence and reduced foliar disease in the hairy vetch–grown tomatoes. A molecular basis for delayed leaf senescence and tolerance to diseases in tomato plants cultivated in the hairy vetch mulch has been demonstrated. In hairy vetch–cultivated plants, expression of specific and select classes of genes is up-regulated compared to those grown on black polyethylene mulch (Kumar et al. 2004; discussed later). The expression of the genes associated with efficient utilization and mobilization of nitrogen, higher photosynthetic rates, higher carbon mobilization, sustained reducing power, and defense promotion were at a higher steady-state level in vetch-grown tomato leaves than in plants grown under black polyethylene. The net result was that tomato plants lived longer, delayed leaf senescence, and were more tolerant to diseases. This system will be discussed in depth later as a model system for understanding and designing sustainable horticultural systems in the future. III. GENETIC SYSTEMS The discussion in the previous section suggests that agroecosystems function according to carefully regulated processes at several scales from the population level to the molecular level. A complex system of metabolic cycles and interacting genetic regulation underlies soil microbial functions, nutrient cycling, crop production, and other processes that determine agroecosystem performance. It may be presumed that at each level key factors control cycling, outputs, and communications among system levels and ultimately may influence overall system functioning. Agricultural breakthroughs will most likely result from improved understanding and application of these key regulating and signaling factors. A. Legume Metabolism and Functional Molecules Among the cover crops, legumes are critical for sustainable agriculture systems because of their ability to fix nitrogen in association with N-fixing bacteria such as Rhizobium, providing renewable source of nitrogen and consequently lowering the input of synthetic fertilizer in agriculture. This will become particularly important as fertilizer nitrogen that is dependent on natural gas for production and petroleum products for transportation becomes increasingly expensive. The focus here is on functional and/or signaling molecules that legume cover crops accumulate during growth and development that can profoundly influence the growth and defense potential of succeeding crops. The nutrients
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and bioactive molecules released during decomposition of cover crop residue and their interactions with crop plant roots within the rhizosphere will define the potential benefits to crop production, produce quality, and ecosystem function. Marketable fruit yields were found to correlate with C : N ratio of the cover crop used, the higher the C : N ratio the lower the yield (Teasdale and Abdul-Baki 1998). Nitrogen release from cover crops is considered a major component that not only replaces the input of chemical fertilizer for robust growth of horticultural crops but also signals beneficial attributes in the subsequent crop (Abdul-Baki et al. 1997). Thus, Nresponsive genes, such as NiR, GS1, rbcL, rbcS, and G6PD, featured prominently among genes found up-regulated in hairy vetch–grown tomato leaves (Kumar et al. 2004). Interestingly, the promoters of these genes harbor the NIT2 element, which has been implicated in nitrogen regulation (Fu and Marzluf 1990). Nitrogen signaling is intimately associated with hairy vetch–grown tomatoes (Kumar et al. 2004; Mattoo and Abdul-Baki 2006). Is nitrogen the only contributing factor in legume cover crop-mediated enhancement of longevity and defense properties of the subsequent crop? In their molecular analysis, Kumar et al. (2004) did not find up-regulation of senescence-associated protein (SAG12) or the nitrate transporter CHL1, whose transcripts were found overexpressed in plants that received short-term exposure to external nitrate concentrations (Wang et al. 2000). Similarly, the expression of an antifungal protein osmotin (Liu et al. 1994), which was found up-regulated in hairy vetch–grown tomatoes (Kumar et al. 2004), actually decreased by 2.5-fold in Arabidopsis exposed to high nitrogen levels (Wang et al. 2000). Thus, it would be simplistic to presume that nitrogen is the only driving element for the effects of legumes on crops. As discussed, nutrient release in cropping systems based on input of organic residues relies on degradation processes that are likely to release many compounds in addition to the wellknown macro- and micronutrients. Legumes are known to produce a wide variety of secondary metabolites that, like isoflavones, have a health-promoting effect. Likely there are other factors present in legume foliage residue that are complementary with the subsequent crop and signal longer growth duration and enhance tolerance to disease/pests? Thus, gas chromatographic–mass spectrometry (GC–MS)–based metabolome analysis of the legume Lotus quantified nitrile glucosides, linamarin and lotaustralian cyanogenic glucosides, and terpenoids—compounds suggested to be involved in plant-insect interactions (Arimura et al. 2004; Forslund et al. 2004; reviewed by Udvardi et al. 2005). It is important to obtain an under-
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standing of such interactive biology by investigating legume biology. The thrust for comparative genomics for model legumes including Vicia faba, Lotus, Medicago, and soybean is therefore a powerful approach to develop comprehensive information on physiological, biochemical, and genomic traits of legumes, which should allow knowledge-based application for achieving agricultural goals (Udvardi et al. 2005; Domoney et al. 2006). Analysis of plant organs from diverse legume species and applying high-throughput methods of metabolomics, transcriptomics, and proteomics should generate an understanding of legume biology principles and plant-plant interactions. B. Other Nitrogen:Carbon Interactive Metabolites Legumes interact with rhizobia and develop symbiotic nitrogen fixation in their nodules, a process that is predated by other plant development processes and evolved some 60 million years ago (see Jiang and Gresshoff 2002). This symbiosis that provides the plant with N and the soil rhizobia with C is now thought to be mostly a plant-controlled process (CaetanoAnolles and Gresshof 1991; Kawaguchi et al. 2002). However, relatively more is known about the bacterial involvement of this symbiosis than about the plant genetics involved, because of the complexity of legume biology. The genome initiatives mentioned in the previous section should further our understanding of the legume genetics that has a direct impact on legume-rhizobia symbiosis. During the legume-rhizobial interactions, the ureides allantoin and allantoic acid remain major nitrogenous products as well as polyamines that have been found to regulate a number of processes in plants. These and possibly other functional metabolites present in legume cover crops can be taken up by the succeeding crop, transported from roots to other plant parts, and subsequently influence tissue-specific gene regulation. Some microorganisms play a symbiotic role in not only fixing atmospheric N but also in producing factors that stimulate host plant growth (Steenhoudt and Vanderleyden 2000; Ma et al. 2002; Penrose and Glick 2003). Atkins et al. (1982) provided direct evidence for the transport of ureides and utilization of ureide-N in cowpea plants for the synthesis of amino acids and insoluble N-containing compounds using 15 N and 14 C feeding studies. This study suggested that ureides can be transported via phloem upward to fruits or downward to the roots of the plant and also freely exchanged from xylem to phloem. Therefore, the researchers concluded that ureides constitute a significant source of translocated nitrogen for protein synthesis in phloemfed organs.
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It is now realized that the phloem stream is a conduit for nucleic acids and proteins, some of which by their very nature can upon translocation regulate gene expression (Atkins and Smith 2007). Amides glutamine and asparagine as well as ureides or citrulline, depending on the species, predominate in xylem and represent translocated forms of assimilated nitrogen in nodulated legume roots (Atkins 1991). Further, Rhizobiumlegume symbiosis also involves translocation of unique solutes, including the plant hormone cytokinin, that can modulate plant growth and development (Upadhyaya et al. 1991). It is becoming increasingly clear that xylem and phloem channels carry important molecules that, when unloaded in a particular plant organ, act as molecular signals. Studies with a pumpkin (Cucurbita maxima) phloem RNA binding protein introduced into rice showed a rootward protein mobility in rice sieve tubes. This occurs through transport systems that interact with other proteins, suggesting protein-protein interactions in the phloem sap. In contrast, shootward translocation involved passive bulk flow (Aoki et al. 2005). A critical role for purine catabolism with concomitant accumulation of ureides in delaying leaf senescence has been presented (Brychkova et al. 2008a). That ureides play an important role in dark and senescence-induced purine remobilization was unmasked in the Arabidopsis mutant developed to silence a key gene in ureide biosynthesis pathway, xanthine dehydrogenase (Atxdh1) (Yesbergenova et al. 2005; Brychkova et al. 2008b). The uriedes were shown to serve as reactive oxygen scavengers as well as favorable N:C compounds. These studies provide a new paradigm for developmental senescence. Polyamines are nitrogen-rich compounds with antisenescence property and capacity to scavenge reactive oxygen species (Kaur-Sawhney and Galston 1991; Borrell et al. 1997; Mattoo and Handa 2008). The most common plant polyamines include the di-amine putrescine, triamine spermidine, and tetra-amine spermine. Pretreatment of cucumber cultivars with spermidine and spermine before exposure to chilling stress was found to inhibit cold-induced lipid peroxidation, and nicotinamide adenine dinucleotide phosphate (NADPH) oxidase was suggested to be the likely target (Shen et al. 2000). Later, Cuevas et al. (2004) reported that polyamines modulate NADPH oxidase in Lotus glaber. These and other studies suggest that polyamine metabolism and action respond to oxidative stress in legumes and other plants. Studies on transgenic tomato engineered to have fruit-specific accumulation of spermidine and spermine have shown that these polyamines revive anabolic processes, signal N:C interactions and markedly impact fruit metabolism and gene expression (Mattoo et al. 2006, 2007;
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Mattoo and Handa 2008; Neelam et al. 2008). The fruit that accumulated spermidine and spermine were nutritionally enriched, had higher juice quality and improved organoleptic characteristics (Mehta et al. 2002; Mattoo et al. 2006). Interestingly, hairy vetch mulch–grown tomato plants produced more spermine in the fruit than that from plants grown under conventional black polyethylene (Neelam et al. 2008). Very little is known about polyamine transporters, particularly in plants. The protein product of the PuuA gene cluster in the bacterium Escherichia coli was studied and found to catalyze g-glutamylation of putrescine (Kurihara et al. 2008). PuuA was found to have a high affinity constant (Km) for putrescine, in millimolar levels, which is consistent with the high (12 mM) levels of putrescine that E. coli can accumulate. Mechanisms that allow plants to sense and respond to changes in C:N ratio are emerging (Hellmann et al. 2000; Smeekens 2000; Vidmar et al. 2000; Coruzzi and Zhou. 2001; Mattoo et al. 2006). These multiple C and N signals can serve as effective tools to understand how different sensing pathways cross-talk with one another and send long-distance signals to regulate plant growth, development, and senescence. C. Legume-Arbuscular Mycorrhizal Fungus Interactions Apart from the root-nodule symbiotic relationship of leguminous plants with N-fixing rhizobia, most higher plant roots associate with the arbuscular mycorrhiza fungi (AMF), an association by which plants can acquire phosphate for growth (Smith and Read 1997). Both these associations involve genetic interactions via signaling molecules, for instance, the Nod factors that signal reprogramming of root development (Oldroyd 2001; Kistner and Parniske 2002). Two genes, CASTOR and POLLUX, have been shown to be among the determinants of microbialplant root symbiosis since mutants of these genes in Lotus japonicus affect symbiosis with arbuscular mycorrhiza and, independently, root nodulation process (Ehrhardt et al. 1996; Novero et al. 2002; Harris et al. 2003). Both genes encode proteins that are localized in root plastids and have been shown to be essential for early signal transduction events, such as calcium spiking that leads to successful endosymbioses (Imalzumi-Anraku et al. 2005). These studies concluded that “an ‘ancient’ endosymbiont helps bacterial and fungal ‘newcomers’ to infect their partner.” In addition to helping plants to acquire phosphorus from the soil (Harrison and Van Buuren 1995), AMF can also acquire and transfer nitrogen to the host plant (He et al. 2003). In an elegant study, Govindarajulu et al. (2005) used stable isotope labeling to show that
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inorganic nitrogen taken up by AMF located outside the roots is recovered in amino acids, then moved as arginine to the intraradical mycelium, and from there transferred to the plant without carbon. These flux events were consistent with the expression of N assimilation genes in the extraradical tissue and arginine catabolism genes in the intraradical mycelium (Govindarajulu et al. 2005). The fact that the AMF use arginine as the N carrier is advantageous because of its property to bind polyphosphate (Martin 1985). It has been suggested that polyphosphates are the P form translocated by AMF (Smith and Read 1997), thus enabling AMF to transfer nitrogen simultaneously with phosphorus to the plant roots. For such a scenario to function well, plant roots should be able to metabolize arginine polyphosphates and use them as an alternative energy source for plant growth and development. Also, such endosymbiotic relationships may be significant for enhancing multiple nutrient cycling within an ecological and physiological context. In an exciting breakthrough, studies with pea (Pisum sativum L) ccd8 mutant (Gomez-Roldan et al. 2008) and rice d mutant (Umehara et al. 2008) deficient in carotenoid cleavage dioxygenase (ccd) have revealed the significance of a group of terpenoid lactones, strigolactones, in AMF-plant symbiosis. Strigolactones are root-synthesized molecules that interact with AMF and promote nutrient uptake by plants. These properties as well as their roles in seed germination and shoot branching across the plant kingdom have prompted suggestions to include strigolactones as new plant hormones (Gomez-Roldan et al. 2008; Umehara et al. 2008). It is clear from this discussion that the metabolic function of a legume plant is defined by root-nodule and root-AMF interactions and that these processes should be important considerations in future experimentation for understanding the mechanism(s) and synergism between cover crops and the subsequently grown crop. D. Molecular Signature of Hairy Vetch–Grown Tomato A window into the black box of genetic and biochemical changes associated with the phenotypic characteristics of tomato plants grown in hairy vetch mulch was opened by a molecular analysis aimed at studying differential gene expression in leaves of plants grown in hairy vetch versus those grown in the conventional black polyethylene (Kumar et al. 2004). Surprisingly, a select transcript signature pattern was evident in the leaves of the hairy vetch–grown tomatoes. This gene signature comprised: N-responsive genes such as NiR, GS1, rbcl, rbcS, and G6PD; chaperone genes such as hsp70 and BiP; defense genes such
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Fig. 6.3. A gene transcript expression signature revealed in hairy vetch (HV)–grown tomato leaf in comparison to plants grown in black polyethylene (BP). Shown are the gene classes and respective northern blot analysis of total RNA from BP- and HV-grown tomato leaves harvested on the indicated days after planting. Modified after Kumar et al. (2004).
as chitinase and osmotin; a CK-responsive gene, CKR; and gibberellin (GA20) oxidase. The transcripts of these genes were at a higher steadystate level in the hairy vetch–grown tomato foliage (Fig. 6.3). The transcript signature pattern paralleled protein profiles for photosynthesis proteins—small and large Rubisco subunits, glutamine synthetase-1; defense-related proteins: chitinase and osmotin; and chaperone proteins: heat shock protein-70 and binding protein BiP. Higher and durable accumulation of hsp70 and BiP transcripts in hairy vetch–grown tomato is an indication of their recruitment in keeping the anabolic machinery functional, thereby increasing the life span of these plants. Thus a coordinated molecular basis seems responsible for the phenotypic characteristics observed in these plants: Plants live longer, have delayed foliar senescence, and are more tolerant to foliar diseases. Overexpression of cytosolic GS-1 in transgenic tobacco previously was shown to lead to an improved growth phenotype (Oliveira et al. 2002). Similarly,
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BiP overexpression in transgenic tobacco results in alleviating endogenous oxidative stress (Alvim et al. 2001). Further validation comes from experiments showing that hairy vetch residue taken from the field imparts the delayed senescence phenotype to tomato plants when grown in the greenhouse (Kumar et al. 2005). Interestingly, Lu et al. (2005) demonstrated that the type of N fertilizer, organic versus inorganic, used to grow wheat can bring about a differential gene expression response. Likewise, tomato fruit responds in a specific manner in regulating gene expression in response to accumulation of organic N in the form of polyamines (Mattoo and Handa 2008; also see later). Differential transcript expression profiles for hormone signaling genes—auxin-responsive ACS6, GA20 oxidase, and CKR (Fig. 6.4)—are yet another hallmark of hairy vetch–grown tomatoes, implicating gibberellin (GA) and cytokinin (CK) signaling in delayed foliar senescence and enhanced disease tolerance in hairy vetch–grown plants. CK regulates a myriad of processes in plant growth and development including a role as an antisenescence hormone (Nooden et al., 1979) and an N signaling molecule (Sakakibara et al. 1998; Takei et al. 2001). Initiation of senescence in plant organs is concomitant with a decrease in CK signaling (Hwang and Sheen 2001; Inoue et al. 2001). A direct correlation between the CK level and retention of greenness was demonstrated by expressing the Agrobacterium CK biosynthesis gene, tmr, in
Fig. 6.4. Differential hormonal signaling highlighted in hairy vetch (HV)–grown tomato. Real-time PCR analysis showing expression patterns for auxin (IAA)-responsive ethylene biosynthesis gene (ACS6), GA signaling gene (GA20 oxidase), and cytokinin receptor kinase gene (CKR) in black polyethylene (BP)– and HV-grown tomato leaves harvested on the indicated days after planting. Adapted from Kumar et al. (2004).
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tobacco leaf (Smart et al. 1991). Interestingly, engineered expression of bacterial CK biosynthesis genes in tobacco plants that caused accumulation of CK led to induction of several defense-related genes including chitinase (Memelink et al. 1987) and osmotin (Thomas et al. 1995). Slight but a significant increase in GA20 oxidase transcript levels in hairy vetch–grown tomato foliage compared to that grown in black polyethylene raises the possibility that GA also directly, or through cross-talk with CK, contributes to differential gene regulation in tomatoes cultivated in the hairy vetch mulch. Additional evidence for differential hormonal signaling in tomato plants cultivated in the two mulch systems is also exemplified by up-regulation in the black polyethylene–grown plants of ACS6, a key gene in the biosynthesis of the aging hormone ethylene (Fluhr and Mattoo, 1996), which is also inducible by the hormone auxin (Yoon et al. 1999). Coincident with early and higher accumulation of ACS6 transcripts in the black polyethylene–grown tomato leaves is the accumulation of cysteine protease transcripts, an additional senescence-associated gene. The simultaneous increase in cysteine protease and ACS6 transcripts may not be a mere coincidence. Matarasso et al. (2005) have found that a cysteine protease–like protein binds to the 715 to 675 promoter region of a related tomato ACC synthase gene, ACS-2 gene. They further found that overexpression of the cysteine protease–like protein in transgenic plants harboring the GUS reporter gene under the control of the ACS2 promoter results in the activation of the GUS gene. Thus, early and sustained accumulation of cysteine protease transcript in tomato plants grown under black polyethylene mulch could activate ethylene biosynthesis by induction of ACC synthase transcripts, thereby promoting senescence in these plants earlier than in the hairy vetch–grown ones. Signaling pathways tuned to hormonal cues seem well coordinated in the hairy vetch–tomato system (Kumar et al. 2004; Mattoo and Abdul-Baki 2006), and a detailed molecular examination of such interactions should reveal new insight into regulation of distinct sets of genes in tomato plants that are involved in the fitness of plants and tolerance to diseases. In this context, it is interesting to note that a role for the CK-signaling pathways has been suggested in plant-microbe interactions involving rhizobacteria (Ryu et al. 2003). E. A Working Model Explaining Hairy Vetch–Tomato Interactions The select transcript/protein signature pattern allowed the development of a model (Fig. 6.5) to explain how hairy vetch system can direct beneficial attributes in tomato (Kumar et al. 2004). Features of this
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Fig. 6.5. A model illustrating the concept of two systems working in unison resulting in enhanced longevity, disease resistance, and higher fruit yield in tomato plants grown in hairy vetch residue. See text for details.
model are in consonance with the scheme proposed by Sugiyama and Sakakibara (2002) on N sensing, CK accumulation, and transcription of N-responsive genes. Hairy vetch–based soil management influences root physiology and causes differential hormonal signaling. A robust root growth habit having larger spread of adventitious roots compared to tomato plants grown on black polyethylene (Sainju et al. 2000) favors CK synthesis, thereby enabling more CK available from the root to the shoot. The CK signal would be transduced through the His-Asp phospho-relay system, inducing the transcription of N-responsive genes (Imamura et al. 2003). Does CK level signal leaf longevity as well as defense against pests in hairy vetch–grown tomatoes? Elevation of the cytokinin receptor kinase CKR is interpreted to mean that a continued influx of CK into the leaf occurs (see also Papon et al. 2002). Upon shootward transport of CK, it is perceived at the leaf membranes and enters the cellular pool, in turn signaling processes that keep the leaf from senescing. It can also form a tripartite complex with basic chitinase and osmotin, both of which bind cytokinins in tobacco callus (Kobayashi et al. 2000). As a result of the tripartite combination of CK, basic chitinase, and osmotin, the two
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defense proteins remain stable for a longer duration, which, in turn, keeps the level of free CK to a minimum. This sequestration of CK can achieve the objective of preventing feedback (autoregulatory loop) signaling from the shoot to the root by high free CK levels and thereby allow for continuous flow of CK from the root to the shoot. Also, chitinase and osmotin proteins can bind actin and cause cytoplasmic aggregation, and thereby participate in pathogen defense, as in potato cell suspensions (Takemoto et al. 1997). The high level of endogenous coexpression of chitinase and osmotin transcripts in hairy vetch–grown tomatoes likely contributes to disease resistance (Kumar et al. 2004). This was validated by studies showing sheath blight resistance in rice engineered to co-express chitinase-osmotin double construct (Kalpana et al. 2006). Engineering resistance to a number of fungi has been broadened by introducing more than a single defense gene: chitinase-glucanase combination reduced lesion development in tobacco by Cercospora nicotianae (Zhu et al. 1994), in tomato by Fusarium oxysporum (Jongedijk et al. 1995), in carrot by different Alternaria sps. and Erysiphe heraclei (Melchers and Stuiver 2000), and in rice by Rhizoctonia solani (Sridevi et al. 2008). F. Genotype Environment and N:C Interactions Conventional methods of selection and breeding in the last century coupled to fertilizer and pesticide use, improved irrigation, and integrated pest management led to increased crop production and contributed to the green revolution. Recent advances have utilized molecular markers to assist in the selection process while technological innovations, such as genetic engineering and biotechnology, have provided new knowledge about genes and their function at the cellular and molecular levels (Chrispeels et al. 2002; Razdan and Mattoo 2005, 2007). Environmental impact data obtained from 42 field experiments with cotton and maize engineered with Bacillus thuringiensis toxin (Bt) have verified that genetically modified crops can contribute to sustainable agriculture (James 2005, 2007; Marvier et al. 2007). In light of these advances, it is imperative that genetically engineered crops be developed to be compatible with alternative agricultural practices and that we learn how the two interact to influence plant growth in the field, fruit metabolism, and overall agricultural sustainability. A transgenic tomato line (ySAMdc line 579HO; Mehta et al. 2002; Mattoo et al. 2006) engineered to accumulate polyamines in a fruitspecific manner was field tested alongside the azygous control line (556AZ; Mehta et al. 2002; Mattoo et al. 2006) in hairy vetch mulch and
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conventional black polyethylene. This study, which profiled 20 fruit metabolites such as amino acids, sugars, and organic acids and expression patterns of a number of genes, demonstrated that growth environments created by using hairy vetch mulch or black polyethylene influence the gene expression of a plant (tomato genotypes) in a unique manner and exemplified genotype mulch-dependent interactions on fruit phenotype (Neelam et al. 2008). Since hairy vetch stimulated spermine accumulation in the nontransgenic fruit, a feature genetically enabled in the 579HO fruit by the ySAMdc transgene (Mehta et al. 2002) when grown in black polyethylene, these data suggested a linkage between polyamines and metabolite content in tomato fruit. Notably, synergism was found between hairy vetch mulch and transgenic tomato in upregulating N:C indicator genes PEPC and ICDHc in the fruit. Hairy vetch increases CKR transcripts (Kumar et al. 2004) also in the fruit (data not shown), suggesting that polyamines, in concert with N and CK, orchestrate the N:C metabolism in tomato fruit. The mulchdependent and transgene-dependent changes in fruit metabolism occurred without any apparent qualitative deviation from normal fruit metabolites (Neelam et al. 2008). This observation bodes well for the integration of genetically engineered (transgenic) crops with ecologically based agriculture practices. Given more precise knowledge of the molecular interactions within agroecosystems, a diversity of crop genotypes may be designed with suites of genes that are adapted to local ecological management systems each with unique ecological requirements and constraints.
IV. AN INTEGRATED APPROACH TO SUSTAINABLE HORTICULTURE Twentieth-century agriculture was characterized by the development of agricultural products for fertilizing crops and controlling weeds, pests, and diseases as well as an industry for economically producing and marketing these products. These products could be targeted to very specific requirements, including delivering targeted ratios of nutrients, selective control of specific weed or pest species without injuring associated crop species, and plasticized materials for favorably altering crop environmental conditions. Use of these products provided an unprecedented level of consistency for optimizing crop yields and eliminating detrimental influences of weeds, pests, and diseases. However, rising energy costs threaten to undermine the cheap raw materials from which these products are manufactured as well as the transporta-
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tion for delivery to the farm gate. In addition, issues relating to the environmental hazards associated with use of selected products on farm and during the manufacturing process heighten interest in discovering alternative approaches. In this chapter we have highlighted ecological and genetic approaches that are likely to contribute toward defining future agricultural alternatives. The challenge will be to synthesize knowledge of genetic/metabolic systems with knowledge of agroecosystem structure and function to understand how manipulation and control of specific gene expression will translate into directing processes at the ecological scale. Rapid advances in technology for modifying crop genetic profile and expression will aid in creating plants with traits most adapted to cropping systems based on sustainable ecological management principles. For example, expression of the gene-encoding terpene synthase 23, which produces volatile terpenes that attract entomopathogenic nematodes and/or parasitic wasps in response to damage by rootworms or leaf damaging larvae, respectively, has been bred out of modern maize cultivars (K€ ollner et al. 2008). Restoring this genetic function to maize would enhance the resistance of these lines to both above- and belowground pest damage in conjunction with ecosystem management that provides a suitable habitat for populations of the required entomopathogenic nematodes and parasitic wasps. Thus, solutions would involve both an understanding of genetic mechanisms and the appropriately compatible ecosystem management. The hairy vetch–tomato model system described in this chapter is a composite of two major systems, each of which is interlaced with symbiotic associations, as illustrated in Fig. 6.5. In System 1, interactions of live hairy vetch roots with rhizobia and AMF upload the vetch foliage with functional primary and secondary metabolites. These metabolites remain in the foliage residue until released to become the substrate and signaling molecules for System 2 interactions between the hairy vetch residue and succeeding tomato plant growth processes. The latter system is characterized by a dynamic equilibrium, at a minimum, between longevity and disease resistance genes, enabling a more productive and fit tomato plant within the agroecosystem. Whether legume cover crops with a high N : C ratio, in general, create a universal signaling system controlling ecosystem interactions with succeeding crop species needs to be investigated. But we advocate that multidisciplinary research between crop ecologists and molecular biologists is needed to better understand these linkages between molecular mechanisms and whole plant function within the context of the agroecosystem. Resulting information will serve to refine agroecosystem management and to direct development of improved crop genetics. Although few
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current agricultural ecologists and molecular biologists are trained to engage in integrated research of this type, we encourage educational programs to promote this type of interdisciplinary training in the future. The synergy between on-farm–produced organic inputs and field production of genetically engineered, value-added crops such as tomato is an important step toward future sustainability of horticultural produce. It will be of interest to discover the nature of synergy between other nutritionally enhanced plants, including fruits and vegetables (Shintani and DellaPenna 1998; Valpuesta 2002), and appropriate leguminous cover crop production systems. Integrating genetically modified crops with sustainable agricultural practices would mitigate the impact of intensive practices on environment and simultaneously address the issues of crop productivity, protection, and quality. Such a paradigm for sustainable agriculture provides a system that decreases the disadvantages of conventional agriculture and increases environmental congeniality and economic viability of future agriculture. It shifts the current paradigm toward sustaining future food production and addresses the opportunity of a “second paradigm” (Sanchez 1994, reviewed by Uphoff 2006) that relies on new germplasm that is adaptable to adverse soil conditions, enhanced soil biological activity, and efficient use of nutrient cycling with minimal external inputs. LITERATURE CITED Abdul-Baki, A.A., and J.R. Teasdale. 2007. Sustainable production of fresh-market tomatoes and other vegetables with cover crop mulches. USDA-ARS Farmers’ Bul, 2280. Abdul-Baki, A.A., J.R. Teasdale, and R.F. Korcak. 1997. Nitrogen requirements of freshmarket tomatoes on hairy vetch and black polyethylene mulches. HortScience 32:217–221. Abdul-Baki, A.A., J.R. Teasdale, R.F. Korcak, D.J. Chitwood, and R.N. Huettel. 1996. Freshmarket tomato production in a low-input alternative system using cover-crop mulch. J. Am. Soc. Hort. Sci. 31:65–69. Alvim, F.C., S.M.B. Carolino, J.C.M. Cascardo, C.C. Nunes, C.A. Martınez, W.C. Oto´n, and E. P.B. Fontes. 2001. Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol. 126:1042–1054. Aoki, K., N. Suzui, S. Fujimaki, N. Dohmae, K. Yonekura-Sakakibara, T. Fujiwara, H. Hayashi, T. Yamaya, and H. Sakakibara. 2005. Destination-selective long-distance movement of phloem proteins. Plant Cell 17:1801–1814. Arimura, G., R. Ozawa, S. Kugimiya, J. Takabayashi, and J. Bohlmann. 2004. Herbivoreinduced defense response in a model legume. Two-spotted spider mites induce emission of (E)-b-ocimene and transcript accumulation of (E)-b-ocimene synthase in Lotus japonicus. Plant Physiol. 135:1976–1983. Atkins, C.A. 1991. Ammonium assimilation and export of nitrogen from the legume nodule. pp. 293–319. In: M.J. Dilworth and A.R. Glenn (eds.), Biology and biochemistry of nitrogen fixation. Elsevier Sci. Publ., Amsterdam. Atkins, C.A., J.S. Pate, A. Ritchie, and M.B. Peoples. 1982. Metabolism and translocation of allantoin in ureide-producing grain legumes. Plant Physiol. 70:476–482.
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Subject Index Bean rust, 1–99 Bitter gourd, 101–141 botany, 109–112 breeding, 120–132 horticulture, 111–119
Genetics and breeding, bitter gourd, 120–131 Grape, carbohydrates, 143–211 Modified humidity packaging, 281–329 Momordica charantia, see Bitter gourd
Carbohydrate, grapevine, 143–211 Organic horticulture, 331–362 Dedication: Goldman, Irwin L., xiii–xxi Disease, bean rust, 1–99 Elderberry, 213–280 botany, 215–226 horticulture 226–264 Fruit. elderberry, 213–280 Fruit crops: elderberry, 213–280 grapevine carbohydrates, 143–211 packaging, 281–329 Fungi, bean rust, 1–99
Horticultural Reviews, Volume 37 Copyright 2010 Wiley-Blackwell.
Physiology, gapevine carbohydrates, 143–211 Postharvest physiology, modified humidity packaging, 281–329 Sambucus, see Elderberry Sustainable horticulture, 331–362 Vegetable crops: bean rust, 1–99 bitter gourd, 101–141 packaging, modified humidity, 281–329 Water relations, packaging, 281–329
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Cumulative Subject Index (Volumes 1–37) 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 mango fruit drop, 31:124–125 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 mango fruit drop, 31:113–155 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, see Kiwifruit 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: development, 32:329–378 phytonutrients, 28:156–159 Alkekenge, history & iconography, 34:36–40 Almond: bloom delay, 15:100–101 Horticultural Reviews, Volume 37 Copyright 2010 Wiley-Blackwell.
breeding, 34:197–238 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: Allium development, 32:329–378 apple flower & fruit, 10:273–308 apple tree, 12:265–305 asparagus, 12:71 cassava, 13:106–112 citrus, abscission, 15:147–156 daylily, 35:196–203 embryogenesis, 1:4–21, 35–40 fig, 12:420–424; 34:127–137 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
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366 Anatomy & morphology (Continued ) magnetic resonance imaging, 20:78–86, 225–266 orchid, 5:281–283 navel orange, 8:132–133 pecan flower, 8:217–255 plant architecture, 32:1–61 pollution injury, 8:15 red bayberry, 20:92–96 waxes, 23:1–68 Androgenesis, woody species, 10:171–173 Angiosperms, embryogenesis, 1:1–78 Anthurium, fertilization, 5:334–335. See also Aroids, ornamental 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 cider, 34:365–415 crop load, 31:233–292 fertilization, 1:105 fire blight control, 1:423–474 flavor, 16:197–234 flower induction, 4:174–203 fruit cracking & splitting, 19:217–262 fruiting, 11:229–287 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 pollination, 34:267–268 replant disease, 2:3 root distribution, 2:453–456 scald, 27:227–267 stock–scion relationships, 3:315–375 summer pruning, 9:351–375
CUMULATIVE SUBJECT INDEX 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 Architecture, plant, 32:1–61 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 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 Aubergine, see Eggplant 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 mango fruit drop, 31:118–120 mechanical stress, 17:18–19 petal senescence, 11:31 Avocado: CA & MA, 22:135–141 flowering, 8:257–289 fruit development, 10:230–238
CUMULATIVE SUBJECT INDEX 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: botany, dispersal, evolution, 36:117–164 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 rust, 37:1–99 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 Belladonna, history & iconography, 34:14–19 Biennial bearing, see Alternate bearing Bilberry, wild of Kazakhstan, 29:347–348 Biochemistry, petal senescence, 11:15–43 Bioreactor technology, 24:1–30 Bioregulation, apple & pear, 10:309–401. See also Growth substances Bird damage, 6:277–278 Bitter gourd, 37:101–141 botany, 37:109–112 breeding, 37:120–132 horticulture, 37:111–119 Bitter pit in apple, 11:289–355 Black currant, bloom delay, 15:104
367 Black pepper, 33:173–266 Blackberry: harvesting, 16:282–298 wild of Kazakhstan, 29:345 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 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 industry, 36:1–115 in vitro, 18:87–169; 34:427–445 micropropagation, 18:89–113 root physiology, 14:57–88 virus elimination, 18:113–123 Bunch stem necrosis of grape, 35:355–395 C CA storage, see Controlled-atmosphere 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 Calcifuge, nutrition, 10:183–227 Calciole, nutrition, 10:183–227
368 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 Capsicum pepper, history & iconography, 34:62–74. See also Pepper Carbohydrate: fig, 12:436–437 grapevine, 37:143–211 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
CUMULATIVE SUBJECT INDEX Cell wall: calcium, 10:109–122 hydrolases, 5:169–219 ice spread, 13:245–246 tomato, 13:70–71 Cellular mechanisms, salt tolerance, 16:33–69 Chelates, 9:169–171 Cherimoya: CA & MA, 22:146–147 pollination, 34:266–267 Cherry: bloom delay, 15:105 CA storage, 1:308 origin, 19:263–317 wild of Kazakhstan, 29:326–330 Chestnut: blight, 8:281–336 botany & horticulture, 31:293–349 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 Cider, 34:365–415 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 in vitro culture, 7:161–170
CUMULATIVE SUBJECT INDEX 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 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
369 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 Cucumis melo, see Melon 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 mango fruit drop, 31:118–120 petal senescence, 11:30–31 rose senescence, 9:66 D Date palm: asexual embryogenesis, 7:185–187 in vitro culture, 7:185–187 Datura, history & iconography, 34:44–51 Daylength, see Photoperiod
370 Daylily, 35:193–220 Dedication: Bailey, L.H., 1:v-viii Beach, S.A., 1:v-viii Bukovac, M.J., 6:x-xii Campbell, C.W., 19:xiii-xiv Cantliffe, D.J., 33:xi-xiii Cummins, J.N., 15:xii-xv De Hertogh, A.A., 26:xi-xiii Dennis, F.G., 22:xi-xii Faust, Miklos, 5:vi-xvi Ferguson, A.R., 35: xiii Goldman, I.L., 37:xiii-xxi 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:xii-xv Magness, J.R., 2:vi-viii Maynard, D.N., 36:xiii-xv Mizrahi, Y., 34:xi-xv 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 Sedgely, M., 32:x-xii Sherman, W. B., 21:xi-xiii Smock, R.M., 7:x-xiii Sperling, C.E., 29:ix-x Stevens, M.A., 28:xi-xiii Warrington, I.J., 31:xi-xii Weiser, C.J., 11:x-xiii Whitaker, T.W., 3:vi-x Wittwer, S.H., 10:x-xiii Yang, S.F., 23:xi Deficiency symptoms, fruit & nut crops, 2:145–154 Deficit irrigation, 21:105–131; 32:111–165 Defoliation, apple & pear bioregulation, 10:326–328 ‘Delicious’ apple, 1:397–424 Desiccation tolerance, 18:171–213 Dieffenbachia, see Aroids, ornamental Dioscorea, see Yam
CUMULATIVE SUBJECT INDEX Disease: air pollution, 8:25 aroids, 8:67–69; 10:18; 12:168–169 bacterial, of bean, 3:28–58 bean rust, 37:1–99 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 melon, 36:185–190 mycorrhizal fungi, 3:182–185 ornamental aroids, 10:18 resistance, acquired, 18:247–289 root, 5:29–31 rust, bean, 37:1–99 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 grape physiological, 35:355–395 pear fruit, 11:357–411 watercore, 6:189–251; 11:385–387 Dogrose, botany, breeding, horticulture, 36:199–255 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 Early bunch stem necrosis of grape, 35:355–395 Easter lily, fertilization, 5:352–355
CUMULATIVE SUBJECT INDEX Eggplant: grafting, 28:103–104 history & iconography, 34:25–35 phytochemicals, 28:162–163 Elderberry, 37:213–280 botany, 37: 215–226 horticulture, 37:226–224 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 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 flower longevity, 3:66–75 flowering, 15:295–296, 319 genetic regulation, 16:6–7, 14–15, 19–20 kiwifruit respiration, 6:47–48 mango fruit crop, 31:120–122 mechanical stress, 17:16–17
371 1-methylcyclopropene, 35:263–313 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 Fig: botany, horticulture, breeding, 34:113–195 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 daylily, 35:193–220 dogrose, 36:199–255
372 Floricultural crops (Continued) fertilization, 1:98–104 flower bulb industry, 36:1–115 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 bulb industry, 36:199–255 cactus, 18:325–335 citrus, 12:349–408 control, 4:159–160; 15:279–334 daylily, 35:193–220 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 in vitro, 4:106–127 induction, 4:174–203, 254–256 initiation, 4:152–153 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
CUMULATIVE SUBJECT INDEX 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 industry, 31:47–112 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 crop load, 31:233–292 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 banana, 36:117–164 bloom delay, 15:97–144 blueberry development, 13:378–390 CA storage & quality, 8:101–127 cactus physiology, 18:335–341 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 & pear, 10:359–361
CUMULATIVE SUBJECT INDEX elderberry, 37:213–280 fig, 4:258–259; 12:409–490; 34:113–195 fresh cut, 30:185–251 functional phytochemicals, 27:269–315 grape, 35:355–395 growth measurement, 24:373–431 jujube, 32:229–298 kiwifruit, 6:35–48; 12:316–318 loquat, 23:233–276 lychee, 28:433–444 mango fruit drop, 31:113–155 maturity indices, 13:407–432 melon, 36:165–198 navel orange, 8:129–179 nectarine, postharvest, 11:413–452 nondestructive postharvest quality evaluation, 20:1–119 olive physiology, 31:157–231 olive processing, 25:235–260 pawpaw, 31:351–384 peach, postharvest, 11:413–452 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 pollination, 34:239–275 pomegranate, 35:127–191 quality & pruning, 8:365–367 red bayberry, 30:83–113 ripening, 5:190–205 rose, wild of Kazakhstan, 29:353–360 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
373 Fruit crops. See also Individual crop alternate bearing, 4:128–173 apple bitter pit, 11:289–355 apple crop load, 31:233–292 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 apricot, origin & dissemination, 22:225–266 apricot, wild of Kazakhstan, 29:325–326 architecture, 32:1–61 avocado flowering, 8:257–289 avocado rootstocks, 17:381–429 banana, 36:117–164 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 CA & MA for tropicals, 22:123–183 CA storage, 1:301–336 CA storage diseases, 3:412–461 carbohydrate reserves, 10:403–430 cherry origin, 19:263–317 cherry, wild of Kazakhstan, 29:326–330 chilling injury, 15:145–182 chlorosis, 9:161–165 cider, 34:365–414 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
374 Fruit crops. (Continued) citrus nutrition diagnostics, 34:277–364 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, 37:213–280 elderberry, wild of Kazakhstan, 29:349–350 Ericaceae nutrition, 10:183–227 fertilization, 1:104–106 fig, industry, 12:409–490; 34:113–195 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 physiological disorder, 35:355–395 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 carbohydrates, 37:143–211 grapevine pruning, 16:235–254, 336–340 greenhouse, China, 30:149–158 honey bee pollination, 9:244–250, 254–256 jojoba, 17:233–266 jujube, 32:229–298 in vitro culture, 7:157–200; 9:273–349 irrigation, deficit, 21:105–131 kiwifruit, 6:1–64; 12:307–347; 33:1–121 lingonberry, 27:79–123 lingonberry, wild of Kazakhstan, 29:348–349 longan, 16:143–196
CUMULATIVE SUBJECT INDEX loquat, 23:233–276 lychee, 16:143–196; 28:393–453 melon, 36:165–198 mango fruit drop, 31:113–155 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 physiology, 31:157–231 olive salinity tolerance, 21:177–214 orange, navel, 8:129–179 orchard floor management, 9:377–430 packaging, modified humidity, 37:281–329 pawpaw, 31:351–384 peach orchard systems, 32:63–109 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 pollination, 34:239–275 pomegranate, 35:127–191 pruning, 8:339–380 rambutan, 16:143–196 raspberry, 11:185–228 raspberry, wild of Kazakhstan, 29:343–345 red bayberry, 30:83–113 roots, 2:453–457 sapindaceous fruits, 16:143–196 sea buckthorn, wild of Kazakhstan, 29:361 short life & replant problem, 2:1–116
CUMULATIVE SUBJECT INDEX 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 water stress, 32:111–165 Functional phytochemicals, fruit, 27:269–315 Fungi: bean rust, 37:1–99 fig, 12:451–474 mushroom, 6:85–118 mycorrhiza, 3:172–213; 10:211–212 pathogens in postharvest storage, 3:412–461 rust, bean, 37:1–99 truffle cultivation, 16:71–107 Fungicide, & apple fruit set, 1:416 G Galanthus, 25:22–25 Gboma eggplant, history & iconography, 34:25 Garlic, 33:123–172 CA storage, 1:375 Genetics & breeding: almond, 34:197–238 aroids (edible), 8:72–75; 12:169 aroids (ornamental), 10:18–25 bean, bacterial resistance, 3:28–58 bitter gourd, 37:120–131 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 daylily, 35:207–214 dogrose, 25:225–244 embryogenesis, 1:23 fig, 12:432–433; 34:165–170 fire blight resistance, 1:435–436 flower bulb crops, 36:16–36 flower longevity, 1:208–209
375 flowering, 15:287–290, 303–305, 306–309, 314–315; 27:1–39, 41–77 ginseng, 9:197–198 gladiolus, 36:20–23 grafting use, 28:109–115 horseradish, 35:247–255 in vitro techniques, 9:318–324; 18:119–123 iris (bulbous), 36:23–25 kiwifruit, 33:1–121 lettuce, 2:185–187 lily, 36:25–29 lingonberry, 27:108–111 loquat, 23:252–257 macadamia, 35:1–125 melon, 36:165–198 muscadine grapes, 14:357–405 mushroom, 6:100–111 narcissus, 36:29–30 navel orange, 8:150–156 nitrogen nutrition, 2:410–411 pineapple, 21:138–164 plant regeneration, 3:278–283 pollution insensitivity, 8:18–19 pomegranate, 35:172–175 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 tulip, 36:30–33 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 Genetic variation: alternate bearing, 4:146–150 banana, 36:117–164 dogrose, 36:225–244 flower bulb crops. 36:16–36 kiwifruit, 33:1–121 melon, 36:165–198 photoperiodic response, 4:82 pollution injury, 8:16–19 temperature-photoperiod interaction, 17:73–123 wild apple, 29:63–303
376 Geophyte, see Bulb, tuber Geranium, fertilization, 5:355–357 Germination, seed, 2:117–141, 173–174; 24:229–275 Germplasm: acquisition, apple, 29:1–61 characterization, apple, 29:45–56 cryopreservation, 6:357–372 in vitro, 5:261–264; 9:324–325 macadamia, 35:1–125 pineapple, 21:133–175 pomegranate, 35:134–141 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 mango fruit drop, 31:113–155 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 history, 35:437–493 incompatibility, 15:183–232 phase change, 7:136–137, 141–142 rose, 9:56–57 Grape: CA storage, 1:308 carbohydrates, 37:143–211 chlorosis, 9:165–166 flower anatomy & morphology, 13:315–337 functional phytochemicals, 27:291–298 harvesting, 16:327–348 irrigation, 27:189–225 muscadine breeding, 14:357–405 nitrogen metabolism, 14:407–452
CUMULATIVE SUBJECT INDEX physiological disorder, 35:355–395 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, 29:342–343 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 floriculture, 7:399–481 flower induction, 4:190–195 flower storage, 10:46–51 flowering, 15:290–296 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 mango fruit drop, 31:113–155 mechanical stress, 17:16–21 meristem & shoot-tip culture, 5:221–227 1-methylcyclopropene, 35:355–395 navel oranges, 8:146–147
CUMULATIVE SUBJECT INDEX 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, wild of Kazakhstan, 29:365–366. See also Filbert Health phytochemicals: fruit, 27:269–315 horseradish, 35:243–244 pomegranate, 35:175–177 vegetables, 28:125–185 Heat treatment (postharvest), 22:91–121 Heliconia, 14:1–55 Henbane, history & iconography, 34:10–14 Herbaceous plants, subzero stress, 6:373–417 Hippeastrum, 25:29–34 Histochemistry: flower induction, 4:177–179 fruit abscission, 1:172–203 Histology, flower induction, 4:179–184. See also Anatomy & morphology History & iconography: alkekenge, 34:36–40 aubergine, see Eggplant belladonna, 34:14–19 capsicum pepper, 34:62–74 datura, 34:44–51 eggplant, 34:25–35. gboma eggplant, 34:25 grafting, 35:437–493 henbane, 34:10–14 husk tomato, 34:40–44 Lycium spp., 34:23
377 mandrake, 34:4–10 potato, 34:85–89 scarlet eggplant, 34:25 Scopolia spp., 34:20–23 Solanaceae, 34:1–111 Solanum dulcamara, 34:25 Solanum nigrum, 34:23–24 tobacco, 34:51–62 tomato, 34:75–85 Withania spp., 34:19–20 Honey bee, 9:237–272 Honeysuckle, wild of Kazakhstan, 29:350 Horseradish: botany, horticulture, breeding, 35:221–265 CA storage, 1:368 Husk tomato, history & iconography, 34:40–44 Hydrolases, 5:169–219 Hydroponic culture, 5:1–44; 7:483–558 Hymenocallis, 25:59 Hypovirulence, in Endothia parasitica, 8:299–310 I Ice, formation & spread in tissues, 13:215–255 Ice-nucleating bacteria, 7:210–212; 13:230–235 Iconography, see History 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; 34:417–445 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, 4:106–127 flowering bulbs, 18:87–169; 34:417–445 geophytes, 34:417–445 pear propagation, 10:325–326 phase change, 7:144–145
378 In vitro (Continued) 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 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 particle film control, 31:1–45 tree short life, 2:52 tulip, 5:63, 92 waxes, 23:1–68 Integrated pest management, greenhouse crops, 13:1–66 Invasive plants, 32:379–437 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; 32:111–165 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 scheduling, 32:111–165 Ismene, 25:59 J Jojoba, 17:233–266 Jujube, 32:229–298 Juvenility, 4:111–112
CUMULATIVE SUBJECT INDEX 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 genetic resources and breeding, 33:1–121 nutrition and 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 Leucadendron, 32:167–228 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, CA & MA, 22:150. See also Sapindaceous fruits 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 Lycium spp., history & iconography, 34:23 Lycoris, 25:39–43 M Macadamia, genetic resources & development, 35:1–125 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, temperature-photoperiod induction, 17:103–106 Mandarin, rootstock, 1:250–252 Mandrake, history & iconography, 34:4–10 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 fruit drop, 31:113–155 in vitro culture, 7:171–173 Mangosteen, CA & MA, 22:157 Master Gardener program, 33:393–420
379 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 Taxus, 32:299–327 Melon: diversity, 36:176–198 grafting, 28:96–98 Meristem culture, 5:221–277 Metabolism: flower, 1:219–223 nitrogen in citrus, 8:181–215 seed, 2:117–141 1-Methylcyclopropene, 35:263–313 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 Modified humidity packaging, 37:281–329 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 Momordica charantia, see Bitter gourd Monocot, in vitro, 5:253–257 Monstera, see Aroids, ornamental Morphology: navel orange, 8:132–133 orchid, 5:283–286 pecan flowering, 8:217–243 red bayberry, 30:92–96
380 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 Musa, see Banana 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: biochemistry & biology, 36:257–287 container growing, 9:93 Ericaceae, 10:211–212 fungi, 3:172–213 grape root, 5:145–146 Myrica, see Red bayberry 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 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
CUMULATIVE SUBJECT INDEX 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 breeding, 34:197–238 almond postharvest technology & utilization, 20:267–311 almond, wild of Kazakhstan, 29:262–265 chestnut blight, 8:291–336 chestnut, botany & horticulture, 31:293–349 fertilization, 1:106 hazelnut, wild of Kazakhstan, 29:365–366 honey bee pollination, 9:250–251 in vitro culture, 9:273–349 macadamia, 35:1–125 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: citrus diagnotics, 34:277–364 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 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 alkalois, 25:171–196 Nutrition (plant): air pollution, 8:22–23, 26
CUMULATIVE SUBJECT INDEX blueberry, 10:183–227 calcifuge, 10:183–227 citrus diagnostics, 34:277–364 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 physiology, 31:147–231 pollination, 34:265–266 processing technology, 25:235–260 salinity tolerance, 21:177–214 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
381 light, 2:208–267 root growth, 2:469–470 water, 7:301–344 Orchid: fertilization, 5:357–358 physiology, 5:279–315 pollination regulation of flower development, 19:28–38 Organic horticulture, sustainability, 36:257–287; 37:331–362 Organogenesis, 3:214–314. See also In vitro; Tissue culture Ornamental plants. See also individual plant Amaryllidaceae, 25:1–70 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 foliage acclimatization, 6:119–154 foliage industry, 31:47–112 geophytes, in vitro, 34:417–445 heliconia, 14:1–55 honeysuckle, wild of Kazakhstan, 29:350 Leucadendron, 32:167–228 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 Salix, 34:447–489 viburnam, wild of Kazakhstan, 29:361–362 Osier, see Salix 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
382 Parasitic weeds, 33:267–349 Parsley: CA storage, 1:375 drilling of seed, 3:13–14 Parsnip, fluid drilling of seed, 3:13–14 Parthenocarpy, tomato, 6:65–84 Particle films, 31:1–45 Passion fruit: in vitro culture, 7:180–181 CA & MA, 22:160–161 Pathogen elimination, in vitro, 5:257–261 Pawpaw, 31:351–384 Peach: bloom delay, 15:105–106 CA storage, 1:309–310 orchard systems, 32:63–109 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
CUMULATIVE SUBJECT INDEX Pepper (Piper), 33:173–266 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 parasitic weeds, 33:267–349 particle films, 31:1–45 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 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
CUMULATIVE SUBJECT INDEX ginseng, 9:223–226 light, 2:237–238 Physiology. See also Postharvest physiology Abuscular mycorrhizae, 36:257–290 Allium development, 32:329–378 apple crop load, 31:233–292 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 floral scents, 24:31–53 flower development, 19:1–58 flowering, 4:106–127 flower bulb crops, 36:36–49 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 grapevine carbohydrates, 37:143–211 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 mango fruit drop, 31:113–155 mechanical stress, 17:1–42 1-methylcyclopropene, 35:253–313 mycorrhizae, 36:257–289 nitrogen metabolism in grapevine, 14:407–452 nutritional quality & CA storage, 8:118–120 olive, 31:157–231 olive salinity tolerance, 21:177–214
383 orchid, 5:279–315 particle films, 31:1–45 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, 28:325–349 subzero stress, 6:373–417 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 water relations cut flowers, 18:1–85 watercore, 6:189–251 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 Pine bark, potting media, 9:103–131 Pineapple: CA & MA, 22:161–162 CA storage, 1:314 genetic resources, 21:138–141 in vitro culture, 7:181–182
384 Piper, see Black pepper Pistachio: alternate bearing, 4:137–139 culture, 3:376–393 in vitro culture, 9:315 pollination, 34:264 wild of Kazakhstan, 29:366–368 Plant: architecture, 32:1–63 classification, 28:1–60 protection, short life, 2:79–84 systematics, 28:1–60 Plantain: CA & MA, 22:141–146 in vitro culture, 7:178–180 Plastic cover, sod production, 27:317–351 Plug transplant technology, 35:397–436 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 artificial, 34:239–276 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: chilling injury, 15:80 in horticulture, 14:333–356
CUMULATIVE SUBJECT INDEX mango fruit drop, 31:125–127 Polygalacturonase, 13:67–103 Pomegranate, 35:127–191 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 bitter melon, 35:343–344 CA for tropical fruit, 22:123–183 CA for storage & quality, 8:101–127 carrot storage, 30:284–288 cassava storage, 30:288–295 chlorophyll fluorescence, 23:69–107 coated fruits & vegetables, 26:161–238 cucumber, 35:325–330 cucurbits, 35: 315–354 cut flower, 1:204–236; 3:59–143; 10:35–62 fig, 34:146–164 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 luffa, 35:344–345 MA for tropical fruit, 22:123–183 melon, 35:330–337 modified humidity packaging, 37:281–329 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; 27:227–267 pear maturity indices, 13:407–432 pear scald, 27:227–257 petal senescence, 11:15–43
CUMULATIVE SUBJECT INDEX potato low temperature sweetening, 30:317–355 potato storage, 30:259–271 protea leaf blackening, 17:173–201 pumpkin & squash, 35:337–341 quality evaluation, 20:1–119 scald, 27:227–267 seed, 2:117–141 sweet potato storage, 30:276–284 taro storage, 30:295–297 texture in fresh fruit, 20:121–244 tomato fruit ripening, 13:67–103 tomato posthavest losses, 33:351–391 vegetables, 1:337–394 watercore, 6:189–251; 11:385–387 watermelon, 35:319–325 wax gourd, 35:342 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 history & iconography, 34:85–89 low temperature sweetening, 17:203–231; 30:317–353 phytochemicals, 28:160–161 postharvest physiology & storage, 30:259–271 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 foliage plants, 31:47–112 ginseng, 9:206–209 macadamia, 35:92–95 orchid, 5:291–297 pear, 10:324–326 rose, 9:54–58 tropical fruit, palms 7:157–200
385 woody legumes in vitro, 14:265–332 Protea: floricultural crop, 26:1–48 leaf blackening, 17:173–201 Proteaceous flower crop: Banksia, 22:1–25 Leucospermum, 22:27–90 Leukcadendron, 32:167–228 Protea, 17:173–201; 26:1–48 Protected crops, carbon dioxide, 7:345–398 Protoplast culture, woody species, 10:173–201 Pruning: alternate bearing, 4:161 apple, 9:351–375 apple training, 1:414 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 physiology, 8:339–380 plant architecture, 32:1–63 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, CA & MA, 22:163. See also Sapindaceous fruits
386 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 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 horseradish, 35:221–265 low-temperature sweetening, 17:203–231; 30:317 -355 minor crops, 12:184–188 potato low temperature sweetening, 30:317–355 potato tuberization, 14:89–188
CUMULATIVE SUBJECT INDEX 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 citrus, 1:237–269 clonal history, 35:475–478 cold hardiness, 11:57–58 fire blight, 1:432–435 light interception, 2:249–250 macadamia, 35:92–95 navel orange, 8:156–161 root systems, 2:471–474 stress, 4:253–254 tree short life, 2:70–75 Rosa, see Dogrose; Rose Rosaceae, in vitro, 5:239–248 Rose: dogrose, 36:199–255 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 Salix, botany & horticulture, 34:447–489 Sambucus, see Elderberry Sapindaceous fruits, 16:143–196 Sapodilla, CA & MA, 22:164 Scadoxus, 25:25–28 Scald, apple & pear, 27:227–265 Scarlet eggplant, history & iconography, 34:25 Scopolia spp., history & iconography, 34:20–23. Scoring & fruit set, 1:416–417 Sea buckthorn, wild of Kazakhstan, 29:361 Secondary metabolites, woody legumes, 14:314–322
CUMULATIVE SUBJECT INDEX 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 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: history and iconography, 34:1–111. in vitro, 5:229–232
387 steroidal alkaloids, 25:171–196 Solanum dulcamara, history & iconography, 34:25 Solanum nigrum, history & iconography, 34:23–24 Somatic embryogenesis. See Asexual embryogenesis Sorghum, sweet, 21:73–104 Spathiphyllum, see Aroids, ornamental Squash, history, 25:71–170 Stem, apple morphology, 12:272–283 Sternbergia, 25:59 Steroidal alkaloids, solanaceous, 25:171–196 Storage. See also Controlled-atmosphere (CA) storage; Postharvest physiology 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; 30:317–353 potato low temperature sweetening, 30:317–353 potato postharvest physiology, 30:259–271 root & tuber crops, 30:253–316 rose plants, 9:58–59 seed, 2:117–141 sweet potato 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
388 Stress (Continued) flooding, 13:257–313 irrigation scheduling, 32:11–165 mechanical, 17:1–42 olive, 31:205–217 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 & nuts, 2:154 nutrition, 5:323–324 Sustainable horticulture, 36:289–333; 37:331–362 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, postharvest physiology & storage, 30:276–284. See also Aroids, edible Taxonomy, 28:1–60 Taxus, 32:299–327 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
CUMULATIVE SUBJECT INDEX 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 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. See also In vitro culture bulb organ formation, 34:417–444 cassava, 26:85–159 dwarfing, 3:347–348 geophyte organ formation, 34:417–444 nutrient analysis, 7:52–56; 9:90 Tobacco, history & iconography, 34:51–62 Tomato: CA storage, 1:380–386 chilling injury, 20:199–200 classification, 28:21–23 fertilization, 1:121–123 fluid drilling of seed, 3:19–20 fruit cracking, 30:163–184 fruit ripening, 13:67–103 galacturonase, 13:67–103 grafting, 28:98–103 greenhouse quality, 26:239 history & iconography, 34:75–85 parthenocarpy, 6:65–84 phytochemicals, 28:160 postharvest losses, 33:351–391 Toxicity symptoms in fruit & nut crops, 2:145–154 Transport, cut flowers, 3:100–104 Tree decline, 2:1–116 Triazoles, 10:63–105; 24:55–138 chilling injury, 15:79–80
CUMULATIVE SUBJECT INDEX 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 Turf grass, 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 development, 32:329–378 Allium phytochemicals, 28:156–159 aroids, 8:43–99; 12:166–170 asparagus postharvest, 12:69–155 bean rust, 37:1–99 bitter gourd, 37:101–141 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 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 cucurbit postharvest, 35:315–354 ecologically based, 24:139–228
389 eggplant grafting, 28:103–104 eggplant phytochemicals, 28:162–163 fertilization, 1:117–124 fluid drilling of seeds, 3:1–58 fresh cut, 30:185–255 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 horseradish, 35:221–265 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, 36:165–198 melon grafting, 28:96–98 minor root & tubers, 12:184–188 mushroom cultivation, 19:59–97 mushroom spawn, 6:85–118 nondestructive postharvest quality evaluation, 20:1–119 nutrition, 22:185–223 okra, 21:41–72 packaging, modified humidity, 37:281–329 pepper phytochemicals, 28:161–162 phytochemicals, 28:125–185 plug industry & technology, 35:387–436 potato low temperature sweetening, 30:317–353 potato phytochemicals, 28:160–161 potato postharvest physiology & storage, 30:271–276 potato tuberization, 14:89–188 pumpkin history, 25:71–170 root & tuber postharvest & storage, 30:295–297 seed conditioning, 13:131–181 seed priming, 16:109–141 squash history, 25:71–170 steroidal alkaloids, Solanaceae, 25:171–196 sweet potato, 12:170–176
390 Vegetable crops.(Continued) sweet potato physiology, 23:277–338 tomato fruit ripening, 13:67–103 tomato (greenhouse) fruit cracking, 30:163–184 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 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, greenhouse crops, 1:117–124 grape & grapevine, 27:189–225 kiwifruit, 12:332–339 light in orchards, 2:248–249
CUMULATIVE SUBJECT INDEX packaging, modified humidity, 37:281–329 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: invasive, 32:379–437 lettuce research, 2:198 parasitic, 267–349 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 rose, 29:353–360 sea buckthorn, 29:361 strawberry, 29:347 vacciniums, 29:347–349 viburnam, 29:361–362 walnut, 29:369–370 Willow, see Salix
CUMULATIVE SUBJECT INDEX Withania spp., history & iconography, 34:19–20 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
391 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 Zizipus, see Jujube
Cumulative Contributor Index (Volumes 1–37) Abbott, J.A., 20:1 Adams III, W.W., 18:215 Afek, U., 30:253 Aharoni, N., 37:281 Albrigo, L.G., 34:277 Aldwinckle, H.S., 1:423; 15:xiii; 29:1 Alonso, J.M., 34:197 Aly, R., 33:267 Amarante, C., 28:161 Anderson, I.C., 21:73 Anderson, J.L., 15:97 Anderson, P.C., 13:257 Andrews, P.K., 15:183 Ascough, G.D., 34:417 Ashworth, E.N., 13:215; 23:1 Asokan, M.P., 8:43 Atkinson, D., 2:424 Aung, L.H., 5:45 Babadoost, M., 35:221 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., 2:41; 36:xiii Bartz, J.A., 30:185; 33:351 Bar-Ya’akov, I., 35:127 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 Behera, S., 37:101 Behera, T.K., 37:101 Ben-Jaacov, J., 32:167 Bennett, A.B., 13:67
Horticultural Reviews, Volume 37 Copyright 2010 Wiley-Blackwell.
Benschop, M., 5:45; 36:1 Ben-Ya’acov, A., 17:381 Ben-Yehoshua, S., 37:281 Benzioni, A., 17:233 Bevington, K.B., 24:277 Bewley, J.D., 18:171 Bharathi, L.K., 37:101 Bieleski, R.L., 35:xiii Binder, B.M., 35:263 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 Bounous, G., 31:293 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 Burger, Y., 36:165 Burke, M.J., 11:xiii Buwalda, J.G., 12:307 Byers, R.E., 6:253; 28:351 Byers, P.L., 37:213 Caldas, L.S., 2:568 Campbell, L.E., 2:524 Cantliffe, D.J., 16:109; 17:43; 24:229; 28:325; 35:397
Edited by Jules Janick
393
394 Carter, G., 20:121 Carter, J., 35:193 Carter, J.V., 3:144 Cathey, H.M., 2:524 Chambers, R.J., 13:1 Chandler, C.K., 28:325 Charlebois, D., 37:213 Charles, J., 34:447 Charron, C.S., 17:43 Chen, J., 31:47 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 Cohen, S., 37:281 Cohen, R., 36:165 Collier, G.F., 4:49 Collins, G., 25:235 Collins, W.L., 7:483 Colmagro, S., 25:235 Compton, M.E., 14:239 Connor, D.J., 31:157 Conover, C.A., 5:317; 6:119 Coombs, B., 32:xi Coppens d’Eeckenbrugge, G., 21:133 Corelli-Grappadelli, L., 32:63 Costa, G., 28:351 Costes, E., 32:1 Coyne, D.P., 3:28 Crane, J.C., 3:376 Criley, R.A., 14:1; 22:27; 24:x Crowley, W., 15:1 Cuevas, J., 34:239 Cutting, J.G., 10:229 Daie, J., 7:69 Dale, A., 11:185; 16:255 Darnell, R.L., 13:339; 28:325 Daunay, M.-C., 34:1 Davenport, T.L., 8:257; 12:349; 31:113 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; 36:1
CUMULATIVE CONTRIBUTOR INDEX Deikman, J., 16:1 DellaPenna, D., 13:67 DeLong, J.M., 32:299 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 D€ uzyaman, E., 21:41 Dyer, W.E., 15:371 Dzhangaliev, A.D., 29:63, 305 Early, J.D., 13:339 Eastman, K., 28:125 Eizenberg, H., 33:267 Ejeta, G., 33:267 Elfving, D.C., 4:1; 11:229 El-Goorani, M.A., 3:412 Erwin, J.E., 34:417 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 Fenner, M., 13:183 Fenwick, G.R., 19:99 Fereres, E., 31:157 Ferguson, A.R., 6:1; 33:1 Ferguson, I.B., 11:289; 30:83; 31:233 Ferguson, J.J., 24:277 Ferguson, L., 12:409 Ferree, D.C., 6:155; 31:xi Ferreira, J.F.S., 19:319 Fery, R.L., 2:311; 12:157 Field, S.K., 37:143 Finn, C.E., 37:213 Fischer, R.L., 13:67 Flaishman, M.A., 34:113 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
CUMULATIVE CONTRIBUTOR INDEX Franks, R. G., 27:41 Fujiwara, K., 17:125 Gadkar, V., 36:257 Gazit, S., 28:393 Geisler, D., 6:155 Geneve, R.L., 14:265 George, K.J., 33:173 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; 31:1 Goffinet, M.C., 20:ix Goldschmidt, E.E., 4:128; 30:1; 35:437 Goldy, R.G., 14:357 Goren, R., 15:145; 30:1 Gosselin, A., 26:239 Goszczynska, D.M., 10:35 Grace, S.C., 18:215 Gradziel, T.M., 30:xiii; 34:197 Graves, C.J., 5:1 Gray, D., 3:1 Grierson, W., 4:247 Griesbach, R.J., 35:193 Griffen, G.J., 8:291 Grodzinski, B., 7:345 Gucci, R., 21:177 Guest, D.I., 17:299 Guiltinan, M.J., 16:1 Gulia, S.K., 35:193 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 Hardie, W.J., 37:143 Hardner, C.M., 35:1 Harker, F.R., 20:121 Hatib, K., 35:127 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; 31:47 Hergert, G.B., 16:255 Hershenhorn, J., 33:267 Hess, F.D., 15:371
395 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 Holland, D., 35:127 Holt, J.S., 15:371 Holzapfel, B.P., 37:143 Huang, Hongwen, 33:1 Huber, D.J., 5:169 Huberman, M., 30:1 Hunter, E.L., 21:73 Hurst, S., 34:447 Hutchinson, J.F., 9:273 Hutton, R.J., 24:277 Indira, P., 23:277 Ingle, M. 27:227 Isenberg, F.M.R., 1:337 Iwakiri, B.T., 3:376 Jackson, J.E., 2:208 Jahn, M., 37:v Janick, J., 1:ix; 8:xi; 17:xiii; 19:319; 21:xi; 23:233; 34:1; 35:437 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 Joel, D.M., 33:267 Joiner, J.N., 5:317 Jones, H.G., 7:301 Jones, J.B., Jr., 7:1 Jones, R.B., 17:173 Joseph John, K., 37:101 Kagan-Zur, V., 16:71 Kalt, W. 27:269; 28:125 Kamenetsky, R., 32:329; 33:123; 36:1 Kang, S.-M., 4:204 Kapulnik, Y., 36:257 Karp, A., 34:447 Kato, T., 8:181 Katzir, N., 36:165 Kawa, L., 14:57 Kawada, K., 4:247 Kays, S.J., 30:253 Kelly, J.F., 10:ix; 22:xi
396 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 Kodad, O., 34:197 Kofranek, A.M., 8:xi Koltai, H., 36:257 Korcak, R.F., 9:133; 10:183 Kozai, T., 17:125 Krezdorn, A.H., 1:vii Kushad, M.M., 28:125 Kuzovkina, Y.A., 34:447 Labrecque, M. 34:447 Laimer, M., 28:187 Lakso, A.N., 7:301; 11:111 Lamb, R.C., 15:xiii Lang, G.A., 13:339 Larsen, R.P., 9:xi Larson, R.A., 7:399 Laterrot, H., 34:1 Lauri, P.E. 32:1 Layne, D.R., 31:351 Leal, F., 21:133 Ledbetter, C.A., 11:159 Lee, J.-M., 28:61 Le Nard, M., 36:1 Levy, Y., 30:37 Lewinsohn, E., 36:165 Li, P.H., 6:373 Liebenberg, M.M., 37:1 Lill, R.E., 11:413 Lin, S., 23:233 Liu, M., 32:229 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 Lowe, A.J. 35:1 Lu, R., 20:1
CUMULATIVE CONTRIBUTOR INDEX Luby, J.J., 29:1 Lurie, S., 22:91-121 Lyrene, P., 21:xi Maguire, K.M., 25:197 Mahovic, M.J., 33:351 Malik, A.U., 31:113 Manivel, L., 22:267 Maraffa, S.B., 2:268 Marangoni, A.G., 17:203; 30:317 Marini, R.P., 9:351; 32:63 Marinoni, D.T., 31:293 Marlow, G.C., 6:189 Maronek, D.M., 3:172 Martin, G.G., 13:339 Masiunas, J., 28:125 Mattoo, A.K., 37:331 Mayak, S., 1:204; 3:59 Maynard, D.N., 1:79; 35:315 McConchie, R., 17:173 McConnell, D.B., 31:47 McIvor, I., 34:447 McNicol, R.J., 16:255 Merkle, S.A., 14:265 Merwin, I.A., 34:365 Meyer, M.H., 33:393 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 Mudge, K., 35:437 Mulwa, R.M.S., 35:221 Murashige, T., 1:1 Mureinik, I., 34:xi Murr, D.P., 23:69 Murray, S.H., 20:121 Myers, P.N., 17:1
CUMULATIVE CONTRIBUTOR INDEX Nadeau, J.A., 19:1 Nair, R.R., 33:173 Naor, A., 32:111 Nascimento, W.M., 24:229 Nayar, N.W., 36:117 Neal, J., 35:1 Neilsen, G.H., 9:377 Nelson, P.V., 26:xi Nerd, A., 18:291, 321 Niemiera, A.X., 9:75; 32:379 Nobel, P.S., 18:291 Norman, D.J., 31:47 Norton, M.A., 35:221 Nybom, H., 36:199 Nyujto`, 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 Okubo, H., 36:1 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 Padilla-Zakour, O.I., 34:365 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; 36:165 Parthasarathy, V.A., 33:173 Peace, C., 35:1 Pegg, K.G., 17:299 Pellett, H.M., 3:144 Perkins-Veazil, P., 17:267 Phillips, G., 32:379 Pichersky, E., 24:31 Pickering, A.H., 35:355 Piechulla, B., 24:31 Pisanu, P., 35:1 Ploetz, R.C., 13:257 Pokorny, F.A., 9:103 Pomper, K.W., 31:351 Poole, R.T., 5:317; 6:119 Poovaiah, B.W., 10:107 Portas, C.A.M., 19:99
397 Porter, M.A., 7:345 Possingham, J.V., 16:235 Prange, R.K., 23:69; 32:299; 35:263 Pratt, C., 10:273; 12:265 Predieri, S., 28:237 Preece, J.E., 14:265 Pretorius, Z.A., 37:1 Priestley, C.A., 10:403 Proctor, J.T.A., 9:187 Puonti-Kaerlas, J., 26:85 Puterka, G.J., 31:1 Qu, D., 30:115 Quamme, H., 18:xiii Rabinowitch, H.D., 32:329 Raese, J.T., 11:357 Ramming, D.W., 11:159 Ransom, J.K., 33:267 Rapparini, F., 28:237 Ravi, V., 23:277; 30:355 Raviv, M., 36:289 Reddy, A.S.N., 10:107 Redgwell, R.J., 20:121 Regnard, J.L., 32:1 Reid, M., 12:xiii; 17:123 Reuveni, M., 16:33 Rich, P.J., 33:267 Richards, D., 5:127 Rieger, M., 11:45 Rodov, V., 34:113; 37:281 Romero, M.A., 34:447 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 Rubiales, D., 33:267 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; 30:185 San Antonio, J.P., 6:85 Sankhla, N., 10:63; 24:5 Sargent, S.A., 35:315
398 Sasikumar, B., 33:173 Sauerborn, J., 33:267 Saure, M.C., 7:239 Schaffer, A.A., 36:165 Schaffer, B., 13:257 Schenk, M.K., 22:185 Schneider, G.W., 3:315 Schneider, K.R., 30:185; 33:351 Schotsmans, W.C., 35:263 Schuster, M.L., 3:28 Scofield, A., 35:437 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 Shehata, A., 35:221 Shipp, J.L., 21:1 Shirra, M., 20:267 Shorey, H.H., 12:409 Silber, A., 32:167 Simon, J.E., 19:319 Simon, P.W., 37:101 Singh, B.P., 35:193 Singh, N.B., 34:447 Singh, S.H., 34:277 Singh, Z., 27:189; 31:113 Skirvin, R., 35:221 Sklensky, D.E., 15:335 Smart, L.B., 34:447 Smith, A.H., Jr., 28:351 Smith, G.S., 12:307 Smith, J.P., 37:143 Smith, M.A.L., 28:125 Smock, R.M., 1:301 Socias i Company, R., 34:197 Sommer, N.F., 3:412 Sondahl, M.R., 2:268 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
CUMULATIVE CONTRIBUTOR INDEX Srivastava, A.K., 34:277 Stang, E.J., 16:255 Staub, J.E., 37:101 Steffens, G.L., 10:63 Stern, R.A., 28:393 Stevens, M.A., 4:vii Stoffella, P.J., 33:xi Stover, E., 34:113 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 Suranyi, D., 19:263; 22:225; 23:179 Swanson, B., 12:xiii Swietlik, D., 6:287; 23:109 Syvertsen, J.P., 7:301, 30:37 Tadmor, Y., 36:165 Talcott, S.T., 30:185 Tattini, M., 21:177 Teasdale, J.R., 37:331 Teodorescu, T.L., 34:447 Tetenyi, P., 19:373 Theron, K.I., 25:1 Thomas, A.L., 37:213 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 Trybush, S., 34:447 Tunya, G.O., 13:105 Turekhanova, P.M., 29:305 Uchanski, M., 35:221 Upchurch, B.L., 20:1 Valenzuela, H.R., 24:139 Valois, S., 34:365 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 van Staden, J., 34:417 Veilleux, R.E., 14:239
CUMULATIVE CONTRIBUTOR INDEX Vizzotto, G., 28:351 Volk, T.A., 34:447 Vorsa, N., 21:215 Wallace, A., 15:413 Wallace, D.H., 17:73 Wallace, G.A., 15:413 Walters, S.A., 35:221 Wang, C.Y., 15:63 Wang, L., 30:115 Wang, S.Y., 14:333 Wann, S.R., 10:153 Warrington, I.J., 35:355 Watkins, C.B., 11:289 Watson, G.W., 15:1 Webster, B.D., 1:172; 13:xi Weichmann, J., 8:101 Weih, M., 34:447 Werlemark, G., 36:199 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
399 Williams, M.W., 1:270 Wismer, W.V., 17:203 Wittwer, S.H., 6:xi Woodson, W.R., 11:15 Wooley, D.J., 35:355 Wright, R.D., 9:75 W€ unsche, J.N., 31:23 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