Compendium of Onion and Garlic Diseases and Pests SECOND EDITION
Edited by Howard F. Schwartz Colorado State University Fort Collins
S. Krishna Mohan University of Idaho Parma
The American Phytopathological Society
Front and back cover photographs by H. F. Schwartz Reference in this publication to a trademark, proprietary product, or company name by personnel of the U.S. Department of Agriculture or anyone else is intended for explicit description only and does not imply approval or recommendation to the exclusion of others that may be suitable. Library of Congress Control Number: 2008922967 International Standard Book Number: 978-0-89054-357-3 ď›™ 1995, 2008 by The American Phytopathological Society First edition published 1995 Second edition published 2008 All rights reserved. No portion of this book may be reproduced in any form, including photocopy, microfilm, information storage and retrieval system, computer database, or software, or by any means, including electronic or mechanical, without written permission from the publisher. Copyright is not claimed in any portion of this work written by U.S. government employees as a part of their official duties. Printed in China on acid-free paper. The American Phytopathological Society 3340 Pilot Knob Road St. Paul, Minnesota 55121, U.S.A.
Preface Y. Anikster, Tel Aviv University, Ramat Aviv, Israel T. A. S. Aveling, University of Pretoria, Pretoria, South Africa M. E. Bartolo, Colorado State University, Rocky Ford D. J. Brotslaw, Sensient Dehydrated Flavors Co., Turlock, CA J. L. Capinera, University of Florida, Gainesville W. S. Cranshaw, Colorado State University, Fort Collins F. J. Crowe, Oregon State University, Madras R. M. Davis, University of California, Davis F. M. Dugan, USDA-ARS, Washington State University, Pullman L. J. du Toit, Washington State University, Mount Vernon R. Ehn, R3 Ag Consulting LLC, Clovis, CA K. L. Everts, University of Maryland, Salisbury L. E. Francois, U.S. Salinity Laboratory, Riverside, CA D. H. Gent, USDA-ARS, National Forage Seed Production Research Center, Corvallis, OR R. D. Gitaitis, University of Georgia, Tifton D. A. Glawe, Washington State University, Puyallup K. Gray, Oregon State University, Corvallis P. D. Hildebrand, Agriculture & Agri-Food Canada, Kentville, Canada A. W. Johnson, USDA-ARS, Tifton, GA D. A. Johnson, Washington State University, Pullman S. T. Koike, University of California, Salinas E. A. Kurtz, Lettuce Board, Salinas, CA M. L. Lacy, Michigan State University, East Lansing J. W. Lorbeer, Cornell University, Ithaca, NY M. R. McDonald, University of Guelph, Guelph, Ontario, Canada M. S. McMillan, Colorado State University, Fort Collins J. Ogrodnick, New York State Agricultural Experiment Station, Geneva, NY F. B. Peairs, Colorado State University, Fort Collins G. Q. Pelter, Washington State University, Ephrata J. D. Rogers, Washington State University, Pullman R. Rohner, Garlic & Onion Dehydration Advisory Board, Stockton, CA A. N. Sparks Jr., University of Georgia, Tifton W. L. Stump, University of Wyoming, Laramie D. R. Sumner, University of Georgia, Tifton J. C. Sutton, University of Guelph, Guelph, Ontario, Canada R. Tahvonen, Agricultural Research Centre of Finland, Piikkiรถ, Finland T. A. Turini, University of California, Davis P. Vincelli, University of Kentucky, Lexington D. D. Warncke, Michigan State University, East Lansing
The purpose of the Compendium of Onion and Garlic Diseases and Pests, Second Edition is to provide an updated, comprehensive, authoritative, and modern account of onion and garlic diseases and pests. It is international in scope and practical in emphasis. It is designed to assist in the diagnosis of onion and garlic diseases and pests in the field, laboratory, or diagnostic clinic and to provide recommendations for their management. The compendium should be useful to plant pathologists, entomologists, crop protection and production specialists, growers, diagnostic clinicians, students, regulatory agents, crop consultants, agribusiness representatives, educators, researchers, and others interested in the recognition or management of onion and garlic diseases and pests throughout the world. The compendium describes infectious diseases caused by fungi, bacteria, nematodes, viruses, and phytoplasmas, as well as noninfectious diseases caused by abiotic factors, such as moisture stress, temperature stress, pesticides, air pollution, and mineral deficiencies and toxicities. It deals with insects as pests and their involvement in the diseases discussed, for example, as vectors of viruses. Symptoms of the diseases and identifying characteristics of the causal agents are described. The compendium also contains many illustrations of onion and garlic disease symptoms and their causal agents, as well as onion and garlic pests. The description of each disease includes a general account of its importance and world distribution, symptoms, causal organism or agent, disease cycle and epidemiology, management, and selected references. The references document the descriptions and may be consulted for further information. The management recommendations provided are general in nature so that they may be adapted to a wide range of cropping conditions. Specific recommendations on chemicals or cultivars are not given because they readily become outdated, may not generally be available, or may not be applicable to certain regions. Disease and pest management practices should be economical and must be compatible with the environment and the production system. Thus, many options for onion and garlic disease and pest management are discussed. This compendium resulted from the efforts of many people as authors, photographers, reviewers, and sponsors to whom we express our deepest thanks. The editors gratefully acknowledge the support, time, and facilities provided by the home institutions of the various contributors to this effort. We also thank the following individuals who supplied figures, photographs, and editorial reviews for this compendium. Agriculture and Agri-Food Canada British Mycological Society G. N. Agrios, University of Florida, Gainesville
Howard F. Schwartz S. Krishna Mohan
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Contributors Whitney S. Cranshaw Colorado State University Fort Collins
David B. Langston University of Georgia Tifton
Frederick Crowe Oregon State University Central Oregon Agricultural Research Center Madras
James Lorbeer Cornell University Ithaca, NY Mary Ruth McDonald University of Guelph Guelph, ON Canada
R. Mike Davis University of California Davis Frank M. Dugan USDA-ARS Western Regional Plant Introduction Station Pullman, WA
S. Krishna Mohan University of Idaho Parma Scott J. Nissen Colorado State University Fort Collins
Lindsey J. du Toit Washington State University Mount Vernon
Philip A. Roberts University of California Riverside
Bryce W. Falk University of California Davis
Jack D. Rogers Washington State University Pullman
David H. Gent USDA-ARS Pacific West Area Corvallis, OR
Brenda K. Schroeder Washington State University Pullman
Michael J. Havey USDA-ARS University of Wisconsin Madison
Howard F. Schwartz Colorado State University Fort Collins
Joseph P. Hill Colorado State University Fort Collins
Kenneth W. Seebold University of Kentucky Lexington
Dennis A. Johnson Washington State University Pullman
Les J. Szabo USDA-ARS Cereal Disease Laboratory St. Paul, MN
Steven T. Koike University of California Salinas
Paul Vincelli University of Kentucky Lexington
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Contents Introduction 1 1 4 5
55 56 58 59 62 63 63 64 66 67 68 68 70 70 72 74 76 77 77 78 78 79 80 83 84 85 85
The Genus Allium Onion and Garlic Diseases Onion and Garlic Pathogens Onion and Garlic Disease and Pest Management
Part I Infectious/Biotic Diseases 8 Diseases of Subterranean Parts Caused by Fungi and Oomycetes 8 Pythium Seed Rot and Damping-Off 10 Rhizoctonia Seed Rot and Seedling Diseases 11 Fusarium Diseases 11 Fusarium Damping-Off 12 Fusarium Basal Rot 14 Fusarium Basal Rot of Garlic 15 Fusarium Bulb Rot of Onion and Garlic 17 Embellisia Skin Blotch and Bulb Canker of Garlic 18 Charcoal Rot 18 Pink Root 20 Sclerotinia Rot 21 Southern Blight 22 White Rot 26 Diseases of Aerial Parts Caused by Fungi and Oomycetes 26 Botrytis Diseases 26 Botrytis Leaf Blight 29 Scape Blight of Onion 30 Flower and Capsule Blight of Onion 30 Botrytis Rot of Garlic 32 Downy Mildew 35 Leaf Blotch 36 Cercospora Leaf Spot 36 Phyllosticta Leaf Blight 36 Powdery Mildew 38 Purple Blotch 41 Rust 44 Smut 45 Stemphylium Leaf Blight and Stalk Rot 47 Twister 47 Diseases of Bulbs Caused by Fungi 47 Neck Rot 49 Brown Stain of Onion 49 Other Botrytis Rots 50 Black Mold 52 Penicillium Decay of Garlic 52 Blue Mold 53 Diplodia Stain 53 Mushy Rot 54 Smudge
Diseases Caused by Bacteria and Yeast Xanthomonas Leaf Blight Leaf Streak and Bulb Rot Soft Rots Other Bacterial Soft Rots Slippery Skin Sour Skin Center Rot Bacterial Stalk and Leaf Necrosis Enterobacter Bulb Decay Other Bacterial Diseases Yeast Soft Rot Diseases Caused by Nematodes Stem and Bulb Nematode (Bloat) Lesion Nematode Root-Knot Nematode Stubby-Root Nematode Sting Nematode Needle Nematode Diseases Caused by Viruses and Phytoplasmas Onion Yellow Dwarf Garlic Mosaic Iris Yellow Spot Other Viral Diseases Aster Yellows (Phytoplasma) Parasitic Flowering Plants Dodder
Part II Pests 87 88 89 91 92 93 93 94
Onion Maggot Other Root Maggots Thrips Leafminers Cutworms and Armyworms Bulb Mites Aster Leafhopper Shallot Aphid
Part III Noninfectious/Abiotic Conditions 95 96 96 97 99 100 103 104 vii
Temperature Stress Air Pollution Hail and Lightning Injury Chemical Response Soil Acidity, Alkalinity (pH), and Salinity Mineral Deficiencies and Toxicities Genetic Abnormalities Greening
104 105 105 106
Pinking Sunscald Translucent and Leathery Scale Waxy Breakdown
107 Appendix 113 Glossary 123 Index
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Introduction The Genus Allium The genus Allium is in the monocot order Asparagales, family Alliaceae, and includes various economically important and cultivated species: the onion (A. cepa) and the closely related shallot (A. cepa var. ascalonicum) and potato onion (A. cepa var. aggregatum), bunching onion (A. fistulosum), chive (A. schoenoprasum), Chinese chive (A. tuberosum), garlic (A. sativum), leek (A. ampeloprasum var. porrum [syn. A. porrum]), and rakkyo (A. chinense). There are at least 18 other Allium spp. that are consumed as fresh vegetables, pickled, or used as flavoring. Several alliums, including A. giganteum, A. moly, and A. caeruleum, are also grown as ornamentals. A. vineale is a weed of pastures. The distinctive flavor or odor of members of the genus is produced when plant tissues are bruised or cut and the enzyme alliinase hydrolyzes S-alk(en)yl cysteine sulfoxide precursors to form volatile sulfur compounds. Onion, garlic, and their relatives, although primarily grown for food, are also used in traditional medicine, including the treatment of chicken pox, common cold, influenza, measles, and rheumatism. Antimicrobial characteristics of the alliums are likely the result of sulfur compounds. Research has demonstrated that extracts of onion and garlic decrease sugars, lipids, and platelet aggregation and enhance fibrinolysis in the blood, indicating that the alliums may help prevent arteriosclerosis and other cardiovascular diseases. According to artifacts recovered in Egyptian tombs, onion and garlic have been part of our food from as far back as 3200 b.c. and are cited as important food staples in the Bible and Koran. The Greeks and Romans wrote about onion and garlic about 400–300 b.c., and onion was popular in northern Europe at the start of the Middle Ages. Its medicinal properties were reviewed in the Indian medical treatise Charaka Samhita nearly 2,000 years ago. Garlic is an ancient crop of central Asian origin. It was grown and consumed in Egypt about 2780–2100 b.c. during the building of the pyramids. It was recorded in a medical treatise in India about 6 b.c. Today, the bulb onion, with a total world production during 2001–2005 of approximately 50 million metric tons on 3 million hectares in 175 countries, is the most valuable Allium species. On average, worldwide production of garlic is about 10% that of the bulb onion. Leek and bunching onion are the next most valuable species, with production concentrated in Europe and the Orient, respectively. The bunching onion is also important in some areas of the United States, such as California. The bulb onion exists only in cultivation and likely originated in central Asia. It is now cultivated worldwide (Fig. 1) and is commonly found in vegetable markets of most countries. Local phenotypes vary in shape (tall, round, or flat), color (white, yellow, pink, or red), firmness, pungency, dormancy, and solids content. Onions produced for dehydration have a much higher solids content than does the sweet, fresh-market type. Onion is a diploid (2n = 2x = 16), herbaceous biennial; i.e., it requires 2 years per generation. The bulb is a modified stem with fibrous roots and fleshy leaves. Onion forms about 15
leaves per growing season but rarely has more than 10 living leaves at any one time. The plant loses four to five leaves during the growing season to natural senescence and death. Premature leaf death is associated with disease or other damage. Bulb formation in onion is affected by temperature and photoperiod. Onion populations have been classified on the basis of the length of daylight required to initiate bulb formation; shortday populations need about 12 h of daylight and long-day types require up to 16 h. Onion is an insect-pollinated crop (Fig. 2). The seed is formed within a three-celled capsule, which usually contains two black seeds. A cluster of capsules forms in the spherical inflorescence (umbel) at the terminal end of the hollow stalk (scape), which elongates from the biennial bulb (Fig. 3). Although most of the world’s onions are grown from seeds, shallot is commonly grown in tropical areas where seed production is difficult. The viviparous onion, A. × proliferum (syn. A. cepa var. viviparum) reproduces by small bulbils that replace all or most of the flowers in the inflorescence. Garlic is propagated vegetatively by cloves and, in those cultivars that bolt, by inflorescence bulbils. Some modern cultivars may produce flowers mixed with the bulbils, but they rarely set true (or viable) seeds. Garlic resembles onion in growth, except that the leaves are thin and flat and the seed stalk (scape), when present, is solid instead of hollow. Cultivars that develop a seed stalk are often called “stick garlic”. Cloves are bound to the central axis of the plant and are covered with several layers of sheathing leaves. Most cloves, when peeled, are white and have white, tan, pink, reddish purple, or purple clove skins. The Japanese bunching onion is grown for its edible tops and leaf bases and has long been the main garden onion of China and Japan. Leek and kurrat (A. ampeloprasum var. kurrat) exist primarily as tetraploids (2n = 4x = 32) and closely resemble wild A. ampeloprasum. Many cultivars of leek have been selected for long, white, edible leaf bases with green tops and for winter hardiness and resistance to bolting. Kurrat is primarily grown in Egypt and other Near Eastern countries for its green leaves. Hexaploid (2n = 6x = 48) great-headed or ele phant garlic (A. ampeloprasum var. holmense) is propagated vegetatively by its large cloves or smaller ground bulblets. It produces flowers but sets few or no seeds. Chive is cultivated for its leaves. Chinese chive (A. tuberosum) and rakkyo (A. chinense) have been domesticated in the Orient since ancient times. Both are perennials, are spread by rhizomes, and are cultivated for their leaves and inflorescences. Cultivated forms of rakkyo are primarily tetraploid and are propagated vegetatively by bulb multiplication.
Onion and Garlic Diseases This compendium describes more than 60 onion and garlic diseases, 40 of which are caused by fungi and oomycetes, 14 by bacteria, 1 by a yeast, 6 by nematodes, 3 by viruses, and 1 by a phytoplasma. In addition, it describes the damage caused to onion and garlic plants by various environmental stresses, a 1
parasitic plant, and nine insect pests. Some diseases, such as purple blotch, downy mildew, and those caused by Botrytis spp., can lead to extensive crop losses and are important throughout the garlic and onion production areas of the world. Other diseases, such as white rot, are important in localized areas. Still other diseases, such as powdery mildew, are currently of minor importance. Annual production and storage losses in garlic and onion as a result of diseases can range from a trace to 50% or more, depending upon the location, environment, host cultivar, and causal agents involved. In view of the large number of potential diseases and pests, their wide distribution, and the capacity of several diseases and pests to cause extensive crop damage, it is apparent that losses in onion and garlic production would be much higher in the absence of ef-
fective disease and pest management practices. A concerted, worldwide approach to the study of onion and garlic diseases and pests and their management ensures the continued production of these important food crops for human consumption. Many of the pathogens and pests reviewed in this compendium also affect other Allium spp. throughout the world. A plant becomes diseased as the result of interactions among the plant, its environment, and one or more harmful agents, including insect pests, or factors in the environment. These harmful agents may be parasitic organisms, such as fungi and oomycetes, bacteria, nematodes, parasitic flowering plants, phyto足plasmas, viruses, and viroids (Fig. 4). Plant diseases are also caused by abiotic factors, such as toxic chemicals, nutrient deficiencies, drought, and heat stress. Biotic agents that cause
Fig. 1. Onion and garlic harvest operations. A, Cultivation; B, pesticide application; C, onion harvest; and D, garlic harvest. (Courtesy H. F. Schwartz and E. A. Kurtz)
Fig. 2. Onion umbel and pollinator. (Courtesy M. E. Bartolo)
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Fig. 3. Field of flowering onions grown for seed production. (Cour足 tesy H. F. Schwartz)
Fig. 4. Range of shapes and sizes of onion and garlic pathogens relative to the size of the plant leaf cell. (Reprinted, by permission from Elsevier, from Agrios, 2005)
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disease are called “pathogens”, and abiotic diseases are related to nonliving factors or conditions. The visible indications of distress shown by diseased plants are called “symptoms” and may include yellowing (chlorosis) of leaves, discolorations, dead spots or patches (necrosis), wilting, stunting, malformations, and numerous other abnormalities. The abnormal functioning of the plant generally leads to reductions in quantity and quality of yield. Parts of the pathogen seen on diseased plants are called “signs” of the disease. Symptoms and signs are very useful in determining the cause of a disease. Accurate disease and pest diagnoses are critical to developing and recommending effective disease and pest management procedures.
Onion and Garlic Pathogens Most onion and garlic diseases are caused by fungi. Fungi are microscopic organisms whose bodies are made of threadlike tiny tubes called “hyphae”, which, en masse, form a mycelium. Hyphae may have partitions, called “septa”, and they obtain their nutrients from the plant. The fungus reproduces by forming specialized structures called “spores”, which serve the fungus in many important ways. Some spores tolerate adverse conditions and enable the fungus to survive in the absence of onion or garlic plants. Some spores may be disseminated by wind, soil, water, or other agents and serve as inoculum to produce new hyphae that penetrate the onion or garlic plant through wounds or natural openings or that penetrate the intact
surface. Spores of a fungus may differ genetically from one another and thus enable new races of the fungus to develop. Fungal pathogens are identified mostly by the size, shape, and color of their spores. These and other structures produced by fungal pathogens of onion and garlic, such as sclerotia and sexual fruiting bodies, are described more fully for each pathogen. Fungal pathogens cause a wide range of symptoms on onion and garlic. Most frequently, they cause variously colored (e.g., brown, yellow, gray, purple, or black) spots or areas on leaves, seed stalks (scapes), bulbs, and roots. They enter onion and garlic plants or bulbs through natural openings or wounds and cause discolored spots, streaks, blighting of leaves, and rotting of bulbs (Fig. 5). Bacteria that cause onion and garlic diseases are microscopic, single-celled organisms that are rod shaped, motile, and generally gram-negative; they do not form spores. They survive well in infected plant material, such as leaves and bulbs. However, in natural environments, they survive only for short periods apart from living plants or plant residues. They are dispersed by the movement of water, soil, seeds, infected plant parts, aerosols, and insects and by man’s activities. They enter onion and garlic plants or bulbs through natural openings or wounds and cause water-soaked (then brown) spots, streaks, blighting of leaves, and rotting of bulbs (Fig. 6). Nematodes (eelworms) are microscopic, slender, wormlike organisms. They move by swimming in films of water between soil particles or on plant surfaces. Nematodes that attack onion and garlic develop from eggs through several (usually four) juvenile stages to the adult. To feed, they puncture the plant with
Fig. 5. Methods of penetration and invasion by fungi. (Reprinted, by permission from Elsevier, from Agrios, 2005)
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Fig. 6. Methods of penetration and invasion by bacteria. (Reprinted, by permission from Elsevier, from Agrios, 2005)
Fig. 7. Methods of penetration and invasion by nematodes. (Reprinted, by permission from Elsevier, from Agrios, 2005)
a hollow, needlelike mouthpiece (stylet) and absorb the plant cell contents (Fig. 7). They are disseminated in water, soil, and plant material. In onion and garlic, they cause rotting or swelling of the bulb and damage to roots. Viruses of onion and garlic are relatively large, complex, infectious molecules composed of a nucleic acid core, usually ribonucleic acid (RNA), and a protein coat. They can be seen with an electron microscope but not with a light microscope. Virus particles (virions) may be short or long rods or polyhedral in shape. They reproduce only in the living plant and generally inhabit the phloem. They may be transmitted among plants in sap (mechanical transmission), in seeds or bulbs, or by insects, such as aphids, thrips, and leafhoppers. Common symptoms of virus infections include leaf mosaics or streaks (light and dark green or yellow areas), malformations (twisting), necrotic spots, and yellowing and stunting of plants. Phytoplasmas range in size from 175 nm to 150 µm. They are of various shapes, including spherical, ovoid, and filamentous. They lack a cell wall, are bounded by a three-layered membrane, and contain cytoplasm, ribosomes, and strands of nuclear material. They occur in phloem sieve tubes and are transmitted by leafhoppers. Symptoms of phytoplasma infection often include yellowing, stunting, malformation, and reduced yield.
Onion and Garlic Disease and Pest Management Rationaldiseaseandpestmanagementrecommendationsare developed from a detailed knowledge of the causal agent or insect pest, the epidemiology of a plant disease, and the developmental stages of the host plant and pest (Figs. 8 and 9; Table 1). Thus, for most of the diseases caused by an infectious organism or agent, this compendium describes survival, transmission, infection, host range (scientific and common names of hosts of Allium pathogens are listed in the Appendix), response to environment, and variability of the pathogen; genetic resistance and other characteristics of the plant; and cultural
practices of the production system. From this knowledge, it is possible to develop procedures that reduce the harmful effects of the pathogen on the onion or garlic plant and that are consistent with economic production of the crop and protection of the environment. Insects, such as thrips and maggots, are an extremely common and diverse group of animals. Physically, adult insects are characterized by having three pairs of legs, three body segments (head, thorax, abdomen), and a winged adult stage. However, insects undergo changes in form (metamorphosis) as they develop and can have a wide range of forms and habits. Although some insects feed upon plants and may become plant pests, the great majority have innocuous or beneficial habits. However, others, like aphids, mites, and onion thrips, play an important role as vectors in the transmission of yield-reducing viruses, such as Onion yellow dwarf virus, Garlic latent virus, and Iris yellow spot virus. The most common management practices for onion and garlic diseases include the use of disease-resistant cultivars, pathogen-and pest-free seeds and bulbs, and other cultural practices (e.g., crop rotation and crop residue management) that suppress the pathogen and pest or restrict its ability to spread to or infect the plants. Another common avenue of disease and pest management is the treatment of soil, seeds, or crop with chemical pesticides and biopesticides. The most effective and sustainable management of onion and garlic diseases and pests is obtained when several disease and pest management methods are integrated with the onion and garlic production practices. Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, San Diego, CA. Augusti, K. T. 1990. Therapeutic and medicinal values of onions and garlics. Pages 93-108 in: Onions and Allied Crops. H. D. Rabinowitch and J. L. Brewster, eds. CRC Press, Boca Raton, FL. Brewster, J. L. 1994. Onions and Other Vegetable Alliums. CABI Publishing, Wallingford, Oxon, United Kingdom. Chase, M., Duvall, M., Hills, H., Conran, J., Cox, A., Eguiarte, L., Hatwell, K., Fay, M., Caddick, R., Cameron, K., and Hoot, S. 1995.
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Fig. 8. A, Onion seedling stages and bulb structure. B, Onion growth stages. C, Garlic bulb and clove arrangement. (Courtesy A and B, W. L. Stump, and C, H. F. Schwartz)
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Fig. 9. Developmental stages of the seeded onion cultivar Colorado 6. (Courtesy M. E. Bartolo)
Molecular systematics of Lilianae. Pages 109-137 in: Monocotyle dons: Systematics and Evolution. P. Rudall, P. Crib, D. Culter, and C. Humphries, eds. Royal Botanic Gardens, Kew, United Kingdom. Currah, L., and Proctor, F. J. 1990. Onions in tropical regions. Nat. Resour. Inst. Bull. 35. Dorofeyev, V. F., ed. (English ed.) 1992. Phyto- geographical basis for plant breeding. Pages 337-344 in: Origin and Geography of Cultivated Plants. N. I. Vavilov. (First published in Russian.) Cambridge University Press, New York. Fenwick, G., and Hanley, A. 1985. The Genus Allium. Crit. Rev. Food Sci. Nutr. 22:199-271. Jones, H. A., and Mann, L. K. 1963. Onions and Their Allies—Botany, Cultivation, and Utilization. Interscience Publishers, Inc., New York. McCollum, G. D. 1976. Onions and allies. Pages 186-190 in: Evolution of Crop Plants. N. Simmonds, ed. Longman, London. Nonnecke, I. L. 1989. Bulbs. Pages 294-319 in: Vegetable Production. Van Nostrand Reinhold, New York.
Rabinowitch, H. D., and Brewster, J. L., eds. 1990. Onions and Allied Crops, Vol. I: Botany, Physiology, and Genetics. CRC Press, Boca Raton, FL. Rabinowitch, H. D., and Brewster, J. L., eds. 1990. Onions and Allied Crops, Vol. II: Agronomy, Biotic Interactions, Pathology, and Crop Protection. CRC Press, Boca Raton, FL. Rabinowitch, H. D., and Currah, L. 2002. Allium Crop Science: Recent Advances. CABI Publishing, Wallingford, Oxon, United Kingdom. Schwartz, H. F., and Bartolo, M. E. 1995. Colorado onion production and integrated pest management. Colo. State Univ. Ext. Bull. 547A. Yamaguchi, M. 1983. Alliums: Onion, garlic, and others. Pages 184206 in: World Vegetables. AVI Publishing Co., Westport, CT.
(Prepared by H. F. Schwartz, S. K. Mohan, M. J. Havey, and F. J. Crowe)
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Part I. Infectious/Biotic Diseases Diseases of Subterranean Parts Caused by Fungi and Oomycetes Pythium Seed Rot and Damping- Off Seed rot and preemergence or postemergence damping-off of onion seedlings are commonly caused by Pythium spp., usually under conditions of poor soil drainage. These oomycetes can cause roots of established plants to decay. Pythium spp. are common in agricultural soils, and the diseases they cause can occur wherever onions are grown.
Symptoms
Seeds that are infected with Pythium spp. become waters oaked and mushy and quickly decompose. Roots of infected onion seedlings initially exhibit a grayish, water-soaked appearance. Infected seedlings that become symptomatic after emergence quickly collapse and die. When infected after the seedling stage, plants are seldom killed but can become severely stunted. Leaves of affected plants exhibit yellowing that progresses from leaf tip to base, with older leaves affected most severely. Wilting of leaves may occur in severely affected plants. Foliar symptoms are most striking in areas of fields with poor drainage (Fig. 10). Roots of affected plants initially appear water-soaked. As the disease progresses, the cortex of affected roots disintegrates but the epidermis and stele remain intact. Symptomatic roots thus characteristically appear collapsed with a white strand within. Infected older roots may become faintly yellow or brown, but marked color changes are not typical.
Fig. 10. Damage to onions caused by Pythium species in a field with poor drainage. (Courtesy P. Vincelli)
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Causal Organisms
P. irregulare has been commonly reported from throughout the world. Other species reported on diseased onion seedlings include P. coloratum, P. graminicola, P. mamillatum, P. paroecandrum, P. rostratum, P. spinosum, P. sylvaticum, P. torulosum, P. ultimum, and P. vexans. P. irregulare and P. coloratum can also cause root rot in older onion plants. These organisms are considered to be fungal-like and are now classified in the kingdom Stramenopila, which was formerly referred to as the kingdom Chromista. Stramenopiles are characterized by the presence of tripartite tubular hairs on flagella or cysts. Pythium spp. produce spherical, thick-walled oospores (Fig. 11) in infected tissues as a result of sexual reproduction. They also produce a variety of asexual reproductive structures. Some species readily produce spherical or distinctively shaped sporangia, which give rise to swimming zoospores. However, several species produce sporangia rarely or not at all, and in at least one species (P. coloratum), the filamentous sporangia are indistinguishable from vegetative hyphae until they produce zoospores. Some Pythium spp. produce “hyphal swellings” in a variety of shapes, ranging from spherical to lemon shaped to irregular. These hyphal swellings can function like chlamydospores, since under favorable conditions they can germinate to produce filamentous hyphae.
Fig. 11. Oospore within an oogonium of Pythium coloratum. (Cour tesy P. Vincelli)
Disease Cycle and Epidemiology Oospores typically serve as long-term survival structures for Pythium spp., although sporangia and hyphal swellings may also allow survival between seasons in some instances. Survival structures remain dormant until stimulated to germinate by an exogenous source of nutrients, such as seed or root exudates. Germination can either be direct (filamentous hyphae) or indirect (zoospores) depending on the species, fungal structures present, and perhaps environmental conditions. Zoospores swim limited distances through water films in soil and encyst along roots near sites where leakage of nutrients is high, such as root tips or subepidermal “short cells”. Encysted zoospores germinate and produce hyphae, which infect and colonize the roots and cause roots to decay. Zoospores released by sporangia in infected tissues can act as secondary inoculum. Oospores also are produced in infected tissues (Fig. 12). Pythium spp. that infect onion are ubiquitous in agricultural soils. The occurrence of Pythium-induced onion diseases in the field almost always is a result of environmental conditions that favor disease development rather than of the spread of pathogenic Pythium spp. into noninfested fields. In greenhouses, however, where efforts are made to follow sanitary production practices, secondary spread of Pythium spp. from an initial infestation may be important. Pythium-induced diseases of onion are most severe under conditions of high levels of soil moisture and soil temperatures below 18°C. In studies conducted to date, Pythium spp. that readily produce zoospores were most commonly isolated from onion roots during periods of high rainfall, while species producing propagules that germinate directly were more common during periods of moderate rainfall.
Spores can be dispersed with anything that moves soil, such as equipment and boots. Active zoospores can also be dispersed in water, such as irrigation water, runoff from rain, or splashing water.
Management
Agricultural practices that minimize periods of excessive soil moisture are recommended for managing Pythium diseases of onion. Practices such as breaking up compacted soil horizons, land leveling, installing tile drains, or planting on raised beds are typically used to reduce the likelihood of seedling diseases and to eliminate significant root rot problems. Seed and soil treatments with fungicides also are recommended practices. Treating onion seeds provides protection against serious stand loss from Pythium-induced seedling diseases for very little cost and poses insignificant environmental and food-safety hazards. Use of fungicides to manage Pythium root rot of established onion plants is neither recommended nor necessary. Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, San Diego, CA. Bruckart, W. L., and Lorbeer, J. W. 1982. Pythium species pathogenic to onion seedlings grown in organic soils in New York. Phyto pathology 72:469- 475. McKeen, C. D. 1950. Preliminary studies on a Pythium root rot of spanish onion seedlings. Sci. Agric. 30:125-131. Robertson, G. I. 1976. Pythium species in market gardens and their pathogenicity to fourteen vegetable crops. N.Z. J. Agric. Res. 19:97-102. Shishkoff, N. 1989. Zoospore encystment pattern and germination on onion roots, and the colonization of hypodermal cells by Pythium coloratum. Can. J. Bot. 67:258-262.
Fig. 12. Disease cycle of damping-off and seed decay caused by a Pythium sp. (Reprinted, by permission from Elsevier, from Agrios, 2005)
9
Sumner, D. R., Gitaitis, R. D., Gay, J. D., Smittle, D. A., Maw, B. W., Tollner, E. W., and Hung, Y. C. 1997. Control of soilborne pathogenic fungi in fields of sweet onion. Plant Dis. 81:885-891. Van der Plaats-Niterink, A. J. 1981. Monograph of the genus Pythium. Studies in Mycology, No. 21. Centraalbureau voor Schimmel cultures, Baarn, the Netherlands. Vincelli, P. C, and Lorbeer, J. W. 1990. Pythium irregulare and P. coloratum causing root rot of onion. Mycopathologia 111:67-72.
(Prepared by P. Vincelli)
Rhizoctonia Seed Rot and Seedling Diseases Rhizoctonia seed rot and seedling diseases occur in soils wherever onion is grown. Disease losses are usually minor, but occasionally, the pathogens can prevent good stand establishment. The fungi that cause the diseases are important seed, root, hypocotyl, and stem pathogens on many vegetable and agronomic crops.
Symptoms
Seeds may decay, and roots of infected seedlings and older plants become discolored (tan to brown) (Fig. 13). Roots and lower stems decay and disintegrate, and seedlings usually wilt and die.
Causal Organisms
The fungi causing the diseases are the anamorphs Rhizoctonia solani anastomosis group (AG)- 4 (teleomorph Thanatephorus cucumeris) and other Rhizoctonia spp. (teleomorph Ceratobasidium spp.). R. solani is multinucleate, whereas the other Rhizoctonia spp. are binucleate. Three different binucleate Rhizoctonia types are known to be pathogenic on onion: AG-E (syn. R. muneratii, CAG-3), AG-F (syn. CAG- 4), and AG-R (syn. CAG-5). Characteristics of the Rhizoctonia spp. include some shade of brown pigmentation of mycelium, approximately 30° branching near the distal septum in young vegetative hyphae, constrictions on both sides of the branch base, formation of septa near the point of origin of hyphal branches, and dolipore septa. Some isolates have monilioid cells, sclerotial hyphae greater than 5 µm in diameter, and a rapid growth rate. Characteristics that have never been reported include clamp connections, conidia, differentiation of sclerotia into rind and medulla, rhizomorphs, and pigments other than brown.
Disease Cycle and Epidemiology
R. solani AG- 4 and the other Rhizoctonia spp. survive in soil in colonized plant debris as sclerotia and on roots of weeds (Fig. 14). These fungi infect plants by forming dome-shaped infection cushions or lobate appressoria on subterranean tissues, producingoneormoreinfectionpegsthatpenetratethroughthe cuticle and epidermis directly or by entering through natural openings or wounds. After invasion, hyphae ramify throughout the tissues (Fig. 15). Pectolytic and cellulolytic enzymes are produced by the pathogen during infection and colonization. Very little is known about the epidemiology of Rhizoctonia diseases in onion. Infection by R. solani AG- 4 occurs at diurnal temperature ranges of 10–21°C and 25–30°C and by the other Rhizoctonia spp. at 23°C. The fungus can be disseminated on tillage equipment and in irrigation water but is not known to be seedborne.
Management
Turning soil 20–30 cm deep with a moldboard plow buries colonized plant debris and sclerotia. The viability of the 10
Fig. 13. Rhizoctonia solani development on an inoculated seedling on the right; a healthy plant is on the left. (Courtesy L. J. du Toit)
fungus declines gradually in soil below 15–20 cm deep, and plowing allows roots to develop in soil with low inoculum levels of the pathogens. Seeds, seedbeds, and transplants may be treated with fungicides. Soil can be treated with fumigants or steam. Soil fumigants, such as methyl bromide, chloropicrin, and metam sodium, have been shown to reduce levels of R. solani AG- 4 when applied prior to planting onion. Soil solarization for at least 1 month during periods of intense solar radiation has been successful in the warm, dry climate of Israel. This method should be useful in many subtropical and tropical areas but probably will not be feasible in temperate regions with short periods of intense sunlight. Crop rotation is of limited value since most crops, except grasses and cereals, are susceptible to the pathogens. No research has been done on the resistance of onion to R. solani AG- 4 or the other Rhizoctonia spp. Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, San Diego, CA. Burpee, L. L., Sanders, P. L., Cole, H., Jr., and Sherwood, R. T. 1980. Pathogenicity of Ceratobasidium cornigerum and related fungi representing five anastomosis groups. Phytopathology 70:843- 8 46. Dodman, R. L., Barker, K. R., and Walker, J. C. 1968. A detailed study of the different modes of penetration by Rhizoctonia solani. Phytopathology 58:1271-1276. Jaworski, C. A., McCarter, S. M., Johnson, A. W., and Williamson, R. E. 1978. Response of onions grown for transplants to soil fumigation. J. Am. Soc. Hortic. Sci. 103:385-388. Katan, J., Rotem, I., Finkel, Y., and Daniel, J. 1980. Solar heating of the soil for the control of pink root and other soilborne diseases of onions. Phytoparasitica 8:39-50. Sneh, B., Burpee, L., and Ogoshi, A. 1991. Identification of Rhizoctonia Species. American Phytopathological Society, St. Paul, MN. Suhag, L. S., and Rana, R. S. 1984. Studies on the chemical control of seedling mortality of kharif onions in nursery. Indian J. Plant Pathol. 2:13-15. Sumner, D. R., Doupnik, B., Jr., and Boosalis, M. G. 1981. Effects of reduced tillage and multiple cropping on plant diseases. Annu. Rev. Phytopathol. 19:167-187. Sumner, D. R., Gitaitis, R. D., Gay, J. D., Smittle, D. A., Maw, B. W., Tollner, E. W., and Hung, Y. C. 1997. Control of soilborne pathogenic fungi in fields of sweet onion. Plant Dis. 81:885-891.
(Prepared by D. R. Sumner; Revised by D. B. Langston and K. W. Seebold)