Compendium of Bean Diseases, Second Edition

Compendium of

Bean Diseases SECOND EDITION

Compendium of Bean Diseases SECOND EDITION

Edited by Howard F. Schwartz Colorado State University Fort Collins

James R. Steadman University of Nebraska Lincoln

Robert Hall University of Guelph Guelph, Ontario

Robert L. Forster (retired) University of Idaho R & E Center Kimberly

The American Phytopathology Society

Cover photographs by Howard 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: 2005930061 International Standard Book Number: 0-89054-327-5 Š 1991, 2005 by The American Phytopathological Society First edition published 1991 Second edition published 2005 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 the United States of America on acid-free paper. The American Phytopathological Society 3340 Pilot Knob Road St. Paul, Minnesota 55121, U.S.A.

Preface G. S. Abawi, Cornell University, Geneva, NY L. Bos, Research Institute for Plant Protection, Wageningen, Netherlands M. H. Dickson, Cornell University, Geneva, NY E. Drijfhout, Institute for Horticulural Plant Breeding, Wag­ eningen, Netherlands R. L. Forster, University of Idaho, Kimberly, ID G. D. Franc, University of Wyoming, Laramie, WY G. Godoy-Lutz, University of Nebraska, Lincoln, NE D. J. Hagedorn, University of Wisconsin, Madison, WI R. Hall, University of Guelph, Guelph, Ontario R. O. Hampton, USDA-ARS, Corvallis, OR L. E. Hanson, USDA-ARS, Fort Collins, CO R. M. Harveson, University of Nebraska, Scotts Bluff, NE W. R. Jarvis, Agriculture Canada, Harrow, Ontario C. W. Kuhn, University of Georgia, Athens, GA A. J. Liebenberg, ARC-Grain Crops Institute, Potchefstroom, Republic of South Africa M. M. Liebenberg, ARC-Grain Crops Institute, Potchef­ stroom, Republic of South Africa H. H. Lyon, Cornell University, Ithaca, NY W. F. Mai, Cornell University, Ithaca, NY M. S. McMillan, Colorado State University, Fort Collins, CO S. K. Mohan, University of Idaho, Parma, ID F. J. Morales, Centro Internacional de Agricultura Tropical, Cali, Colombia M. Pastor-Corrales, USDA-ARS, Beltsville, MD W. F. Pfender, USDA-ARS, Corvallis, OR R. Provvidenti, Cornell University, Geneva, NY A. W. Saettler, USDA-ARS, East Lansing, MI H. F. Schwartz, Colorado State University, Fort Collins, CO H. A. Scott, University of Arkansas, Fayetteville, AR M. J. Silbernagel, USDA-ARS, Prosser, WA J. R. Stavely, USDA-ARS, Beltsville, MD J. R. Steadman, University of Nebraska, Lincoln, NE D. R. Sumner, University of Georgia, Tifton, GA J. C. Tu, Agriculture Canada, Harrow, Ontario D. M. Webster, Seminis Inc., Twin Falls, ID

The purpose of this Compendium of Bean Diseases, Second Edition is to provide an updated, comprehensive, authoritative, and modern account of bean diseases. It is international in scope and practical in emphasis. It is designed to assist in the diagnosis of bean diseases, whether in the field, laboratory, or diagnostic clinic, and to provide recommendations for man­ agement of bean diseases. The compendium should be useful to plant pathologists, crop production specialists, growers, di­ agnostic clinicians, students, regulatory agents, crop consult­ ants, agribusiness representatives, educators, researchers, and others interested in the recognition or management of bean diseases throughout the world. The compendium describes infectious diseases caused by fungi, bacteria,nematodes,viruses, and phytoplasmas and non­ infectious diseases caused by abiotic factors, such as moisture stress, temperature stress, pesticides, air pollution, and mineral deficiencies and toxicities. It does not deal with insects except to the extent that they are involved in the disease discussed, for example, as vectors of viruses. The compendium contains many illustrations of bean dis­ eases and their causal agents. In addition, symptoms of the diseases and identifying characteristics of the causal agents are described. The management recommendations are general in nature so that they may be adapted to a wide range of cropping condi­ tions. Specific recommendations on chemicals or cultivars are not given because they are soon outdated, may not be gener­ ally available, or may not be applicable to certain regions. Dis­ease management practices should be economical and must be compatible with the environment and the production system. Thus, many options for bean disease management are ­discussed. The description of each disease includes a general account of its importance and world distribution, symptoms, causal organism or agent, disease cycle and epidemiology, manage­ ment, and selected references. The references document the descriptions and may be consulted for further information. This compendium resulted from the efforts of many people as authors, photographers, reviewers, and sponsors to whom we express our deepest thanks. Theeditorsgratefully acknowledge the support, time, and facilities provided by our home institu­ tions to this effort on behalf of the international community. We also wish to thank the following individuals who sup­ plied figures and photographs for this compendium.

Howard F. Schwartz James R. Steadman Robert Hall Robert L. Forster

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Contributors George Abawi Cornell University Geneva

George Mahuku Centro Internacional de Agricultura Tropical Cali, Colombia

Greg Boland University of Guelph Guelph, Ontario

Robert McMillan Univ. of Florida, IFAS Homestead

Mark Brick Colorado State University Fort Collins

Krishna Mohan University of Idaho Parma

Robert Forster (retired) University of Idaho R & E Center Kimberly

Francisco Morales Centro Internacional de Agricultura Tropical Cali, Colombia

Gary Franc University of Wyoming Laramie

Marcial Pastor Corrales USDA-ARS Beltsville

Graciela Godoy-Lutz University of Nebraska Lincoln

Howard F. Schwartz Colorado State University Fort Collins

Robert Hall University of Guelph Guelph, Ontario

James R. Steadman University of Nebraska Lincoln

Linda Hanson USDA-ARS Sugarbeet Lab Fort Collins

Jui-Chang Tu Harrow Research Station, Agr. Canada Harrow, Ontario

Robert Harveson University of Nebraska Scottsbluff

David Webster Seminis Inc. Twin Falls

Carol Ishimaru University of Minnesota St. Paul

Gary Yuen University of Nebraska Lincoln

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Contents Introduction

1 5 5 6 6 8

52 52 52 55 56 57 57 57 58 58 59 59 60 62 63 64 66 67 68 68 69 70 71 72 73 73 74 75 76 77 79 80 81 82 83 84 84 85 86 86

The Bean Plant Bean Diseases Bean Pathogens Bean Disease Management Bean Diagnostic Guidelines Bean Crop Health and Integrated Pest Management

Part I Infectious Diseases 10 10 12 13 15 16 17 19 20 21 22 22 24 25 27 28 29 30 31 31 32 32 33 34 35 36 36 38 39 40 41 43 44 46 46 46 47 49 50

Fungal Diseases of Subterranean Parts Aphanomyces Root and Hypocotyl Rot Black Root Rot Fusarium Root Rot Fusarium Wilt (Yellows) Phymatotrichum Root Rot Pythium Diseases Rhizoctonia Root Rot Southern Blight Stem Rot Fungal Diseases of Aerial Parts Alternaria Leaf and Pod Spot Angular Leaf Spot Anthracnose Ascochyta Leaf Spot Ashy Stem Blight Cercospora Leaf Spot and Blotch Chaetoseptoria Leaf Spot Diaporthe Pod Blight Downy Mildew Entyloma Leaf Smut Floury Leaf Spot Gray Leaf Spot Gray Mold Phyllosticta Leaf Spot Pink Pod Rot Powdery Mildew Rust Scab Soybean Rust Web Blight White Leaf Spot White Mold Yeast Spot Diseases Caused by Bacteria Bacterial Brown Spot Common Bacterial Blight Halo Blight Bacterial Wilt

Wildfire Diseases Caused by Nematodes Root-Knot Nematodes Lesion Nematodes Reniform Nematode Soybean Cyst Nematode Sting Nematode Other Nematodes Diseases Caused by Viruses Alfalfa Mosaic Angular Mosaic Bean Calico Mosaic Bean Common Mosaic Bean Common Mosaic—Black Root Bean Dwarf Mosaic Bean Golden Mosaic Bean Golden Yellow Mosaic Bean Mild Mosaic Bean Necrosis Mosaic Bean Pod Mottle Bean Rugose Mosaic Bean Severe Mosaic Bean Southern Mosaic Bean Summer Death Bean Yellow Dwarf Bean Yellow Mosaic Bean Yellow Stipple Clover Yellow Vein Cucumber Mosaic Curly Top Peanut Mottle Peanut Stunt Red Node Soybean Mosaic Stipple Streak Diseases Caused by Phytoplasmas Long Stem Machismo Phyllody Witches’-Broom

Part II Noninfectious Diseases 87 87 87 88 89 89 90 vii

Environmental and Genetic Disorders Air Pollution Baldheads Genetic Abnormalities Green Spot Hail Injury Lightning Injury

90 90 92 92 92 93 93

Moisture Stress Pesticide Injury pH Sunscald Temperature Stress Wind and Sand Damage Mineral Deficiences and Toxicities

96   96   97   98

Seed Quality Mechanical Damage Seed Coat Rupture Hypocotyl Collor Rot

99   Glossary 105   Index

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Compendium of Bean Diseases second EDITION

Introduction The Bean Plant Common bean (Phaseolus ­vulgaris L.) was domesticated by Native Americans during pre-­Colombian times. Archeological data suggest that bean was independently domesticated in different regions of the Americas, including the Andean region of South America, Argentina, and Mexico. The oldest domesticated beans found at archeological sites in each of these regions were estimated to have been cultivated between 7,000 and 9,600 years ago. Wild or putatively wild relatives of P. vulgaris grow currently from northern Mexico to Argentina, often in the same regions as cultivated forms. Domestication has altered the morphology and phenology of the plant, especially growth habit, seed size, seed retention, and maturity. Selection toward smaller,denserplants resulted in shorter internodes, suppressed climbing ability, fewer and thicker stems, and larger leaves. This selection strategy culminated in the compact growth habit of free-­standing, determinate, and upright indeterminate bean cultivars that were more suitable for mechanized crop production. The most striking difference between wild ancestors and cultivated beans are changes in pod and seed size. During domestication, large seeds were selected for dry seed production in preference to the small seeds (preferred for garden bean production) and less dehiscent pods with lower pod fiber content. The large seed size of early domesticates indicates that gain from selection for large seed size was rapid rather than gradual. Seed colors, markings, and shapes vary widely in the species, and local landraces reflect regional preferences in seed type. For example, Venezuela and Guatemala favor black beans; Colombia and Honduras, red; Peru and Mexico, cream, tan, or black; and Brazil, black or tan striped. Landraces of climbing beans also occur as mixtures of seed types, especially in Africa where large-­seeded, colored Andean beans are preferred. Common bean is the third most important food legume crop worldwide; only soybean (Glycine max (L.) Merr.) and peanut (Arachis hypogaea L.) have more production. Cultivated beans are divided into two groups based on their edible parts. Dry edible beans are consumed as the mature dry seeds after rehydration, and snap beans (e.g., green, string, French, or Haricot beans) are consumed for their fleshy immature pods. Dry beans are further divided into distinct market classes based on seed characteristics, and snap bean classes are based on pod characteristics and plant type. Market classes of dry beans grown in North America include pinto, great northern, pink, small red, black, navy, small white, light red kidney, dark red kidney, yellow eye, Anasazi, and cranberry. Other bean species produced include lima bean, mung bean, and azuki bean. Snap bean classifications include green, wax, and Romano (e.g., Italian, flat pod). Both the dry seeds and fresh green pods of common bean are consumed throughout the world for their nutritional ­content. Taxonomically, common bean belongs to the family Fabaceae (Leguminosae), which is further subdivided into subfamily, tribe, subtribe, and genus. The genus Phaseolus is a member

of the subfamily Papilonoideae, tribe Phaseoleae, and subtribe Phaseolinae. The subtribe Phaseolinae includes many other important pulse crops, such as cowpea (Vigna unguiculata (L.) Walp. subsp. unguicalata (L.) Walp.), mung bean (V. radiata (L.) R. Wilczek var. radiata (L.) R. Wilczek), azuki bean (V. angularis (Willd.) Ohwi & H. Ohashi var. angularis (Willd.) Ohwi & H. Ohashi), moth bean (V. aconitifolia (Jacq.) Maréchal), and winged bean (Psophocarpus tetragonolobus (L.) DC.). Within the genus Phaseolus, the exact number of species is still unknown. A 1999 review of the genus by ­Debouck suggests that it contains 51 species. Species of the genus Phaseolushavebeengroupedintosections,basedonplantmorphology, hybridology, palynology, and molecular genetics, that reflect different lines of evolution and speciation. Debouck classified four sections, including Chiapasana, Phaseolus, Minkelersia, and Xanthotricha. The Phaseolus section included four of the cultivated Phaseolus species, namely, P. vulgaris (common bean), P. coccineus L. (runner bean), P. lunatus L. var. lunatus L. (lima bean), and P. acutifolius A. Gray var. acutifolius A. Gray (tepary bean). Each cultivated species was domesticated from wild ancestors that still grow in the neotropics. Worldwide, P. vulgaris is the most widely grown of the four species. It is cultivated extensively in North, South, and Central America, Africa, Asia, and throughout Europe. According to the Food and Agricultural Organization (FAO), Brazil and Mexico are the largest Phaseolus-­producing nations in the world, with an annual production of 138,700 and 75,000 metric tons (t), respectively, in 2001. The FAO statistics suggest that Asia, in particular India (213,000 t) and China (84,400 t), produces large quantities of dry beans; however, these are largely Vigna beans. Worldwide production of dry beans is approximately 11.6 million t harvested from 14.3 million ha. Data on the world production of snap beans are confounded by FAO statistics that combine pod production of common bean with Vigna species, which are consumed largely in India and China. Morphologically, P. vulgaris is distinct from other legumes. The primary leaves are unifoliolate and subsequent leaves are trifoliolate. Flowers are borne on a pedicel in the axes of nodes of both primary and secondary branches. Flowers are perfect and have typical legume morphology, consisting of five petals, 10 stamens, a style, a stigma, and a superior ovary. The five petals of the corolla are differentiated into two fused petals that form a keel, two wing petals, and a standard. The keel is coiled into two to three spiral turns and contains one free and nine fused stamens with one pistil. The ovary typically contains five to eight ovules. Triangular-­shaped stipules are present at the base of the corolla. Bean pods are linear and have two valves. Pods may be parchmented with strong dehiscence, leathery with less dehiscence, or fleshy and stringless with little dehiscence. Plants with parchmented pods are used for dry bean production and are harvested when mature. Plants with fleshy pods are used for snap bean production and are harvested when the pods and seeds are still immature. Plants with leathery pods can be used for both dry and fresh bean production. 1

The seed consists of the embryo, two cotyledons, and a seed coat (testa). These parts constitute 9, 90, and 1% of the dry weight, respectively (Fig. 1). The embryo is essentially a miniature plant with three basic components, including the primary root or radicle, a plumule or shoot, and cotyledons. The cotyledons are simple leaves that serve as a food source for the developing plant during seed germination. The seed coat or testa is a thin structure, made up of several layers, that serves to protect the seed from mechanical damage and a potentially harmful environment during seed storage. The two scars visible on the incurved edge of the seed surface are the hilum and micropyle. The hilum is a scar that forms at the point of seed detachment from the pod after dehiscence. The micropyle is the remnant of the opening in the ovule where the pollen tube entered during fertilization. Both structures can serve as a site of water entry during the imbibition phase of seed germination. Seed germination is the resumption of embryonic growth following a period of dormancy. Seed germination is initiated by the imbibition of water, followed by enzyme activation and

Fig. 1. Bean seed morphology. (Reprinted, with permission from Schwartz, Brick, Harveson, and Franc, 2004)

synthesis, cell expansion, and subsequent rupture of the seed coat. The optimum temperature for germination is between 18 and 25째C. The minimum temperature for uniform germination is 12째C. Germination of common bean is considered epigeal, because the cotyledons are pushed above the soil surface. Following imbibition, the hypocotyl arch pushes the cotyledons through the soil and straightens, and the two primary (unifoliolate) leaves unfold (Fig. 2). After seedling emergence, the first trifoliolate leaf expands and the terminal meristem initiates formation of new leaves. Injury to the terminal bud during seedling development causes axillary buds to initiate growth and assume the function of the terminal bud. If the injury destroys both the terminal meristem and axillary buds at the unifoliolate leaf, the plant dies because no buds exist below that point. This type of injury is often associated with seed damage in the handling process or during seedling emergence because of mechanical injury or hail damage. The bean plant undergoes four distinct developmental stages during its life cycle. The stages include I) emergence and early vegetative growth, II) branching and rapid vegetative growth, III) flower and pod formation, and IV) pod fill and maturation (Fig. 3; Table 1). The first two developmental stages occur during vegetative growth and the final two occur during reproductive growth. The time period required to complete each stage varies among cultivars and is influenced by environmental factors. Stage I includes seed germination, emergence, and early vegetative growth. This stage is initiated at planting and terminates after the third trifoliolate leaf opens. Stage II includes the period between emergence of the third trifoliolate leaf and opening of the first flower. This period is characterized by branching and rapid vegetative growth. A new trifoliolate leaf develops on the main stem approximately every 3 days under favorable growing conditions. Stage III is the period between the first flower and mid pod set. At the end of stage III, floral initiation has normally ceased and 50% of the pods are fully elongated. Stage IV starts when the first formed pods begin to fill and continues until harvest maturation. Near the end of stage IV, small pods that have not started to fill cease to develop,

Fig. 2. Seed germination and seedling development. (Reprinted, with permission from Schwartz, Brick, Harveson, and Franc, 2004)

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while existing pods and leaves begin to senesce. Upon completion of stage IV, the plant is mature and ready for harvest. Considerable variation exists in the growth characteristics of common bean plants. This variation is used to separate germ plasm into four classifications based on determinacy of growth and plant architecture. The classifications include type I (determinate, bush), type II (indeterminate, upright), type III (indeterminate, semivine), and type IV (indeterminate, climbing vine) (Table 2). Classes are also subdivided into an “a” or “b”

subclassification based on the presence of a guide. Type I plants have a determinate growth habit, distinguished by a thick main stem, reproductive terminal buds, few internodes, short floral duration period (12–21 days), and more-­uniform pod maturity than that of the other types. Because type I plants usually have uniform pod maturity, most snap bean cultivars developed for mechanical harvest have type I growth habit. Type Ia plants have a strong main stem and upright branches, whereas type Ib plants have weak branches and main stem and possess some

Fig. 3. The four major growth and developmental stages in the vegetative and reproductive development of determinate and indeterminate bean plants. For determinate (type I/bush) beans, stems and branches terminate in an inflorescence. For indeterminate (type II and type III/vine) beans, stems and branch terminals remain vegetative. (Courtesy H. F. Schwartz and M. S. McMillan)

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ability to climb. Type II and type III bean plants have an indeterminate growth habit distinguished by vegetative terminal buds on the main stem and lateral branches. This allows the plant to continue vegetative growth during flowering and pod fill. Type II and type III plants produce more nodes and usually have a longer floral duration than do type I plants. Type II plants are distinguished from type III plants by their erect main stem and branches, whereas type III plants have a weak main stem that grows semiprostrate or is twining to produce a dense canopy. Type IIa and type IIIa plants lack a strong terminal guide or leader and thus lack climbing ability, while type IIb and type IIIb plants have a terminal guide of varying length and possess some climbing ability. Type IV plants have very weak and excessively long stems and branches. They possess

strong climbing ability and a structural support is necessary for maximum production. Type IVa plants have the pod load distributed all along the length of the plant, whereas type IVb plants have pods borne mostly on the upper part of the plant. Because the environment influences the number, length, and erectness of branches and the strength of the main stem, some cultivars vary in architecture across environments, whereas some cultivars are stable in their classification. Therefore, the characterization of growth habit for some genotypes may only be useful in a given environment. Current breeding programs use broad-­based parental germ plasm to improve disease resistance and agronomic characteristics. The categorization of P. vulgaris germ plasm into six races within two primary centers of domestication has contributed immensely to our knowledge about genetic diversity in Phaseolus germ plasm. The primary centers of domestication are Andean and Middle American. The Andean center of diversity from South America is further subdivided into three races that include Nueva Granada (northern Andes), Peruvian (Peruvian highlands), and Chilean (northern Chile and Argentina). Race Nueva Granada is represented by large-­seeded light and dark red kidney bean, cranberry, yellow or Azufrado, and Calima beans, as well as other mottled types known as sugar and speckled beans, which are grown widely in Africa and the Caribbean. Germ plasm of races Peruvian and Chilean are not widely grown commercially in the Northern Hemisphere but include Nuña (popping beans) and coroscos. Beans from the Middle American center of diversity were domesticated in Mexico and Central America and include the races Durango (central highlands of Mexico), Jalisco (coastal Mexico near the state of Jalisco), and Mesoamerica (lowland tropical Central America). Market classes that typify race Durango include pinto, great northern, small red, pink, and bayo. Race Jalisco is composed primarily of photoperiod-­sensitive material, such as Flor de Mayo and Flor de Junio. Race Mesoamerica is represented by small-­seed classes, such as navy, small white, carioca, and black beans. Based on phaseolin type, snap beans are considered to be derived from the Andean center of domestication. However, some snap bean cultivars possess genetic material from both centers of domestication based on molecular markers. This categorization of centers of domestication and races has provided us with a better understanding of combining traits among races, coevolution of genes between the host and pathogen, and genetic incompatibility factors between genes from different centers of origin that can result in lethality of F1 hybrids, give rise to crippling of trifoliolate leaves, or both. In summary, common beans possess an immense spectrum of genetic diversity for morphological, architectural, nutritional, and economically important traits that have been exploited for human benefit throughout the world. Our understanding of interactionsbetweenhostgenesandpathogenscontinuestobean important component of bean research. New information about host–pathogeninteractionswillcontinuetoenhanceproduction and production efficiency in the future. We must continue our quest for a better understanding of both the host and pathogens to ensure that we can build upon our past accomplishments. Selected References Brick, M. A., and Johnson, J. J. 2004. Classification, development and varietal performance. Pages 7-­13 in: Dry Bean Production and Pest Management, 2nd ed. H. F. Schwartz, M. A. Brick, R. M. Harveson, and G. D. Franc, eds. Reg. Bull. 562A. Colorado State University, Fort Collins, CO. Debouck, D. 1991. Systematics and morphology. Pages 55-­118 in: Common Beans: Research for Crop Improvement. A. van Schoonhoven and O. Voysest, eds. CAB International, Wallingford, U.K., and CIAT, Cali, Colombia. Debouck, D. 1999. Diversity in Phaseolus species in relation to the common bean. Pages 25-­52 in: Common Bean Improvement in the

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Twenty-­First Century. S. P. Singh, ed. Kluwer Academic Publishers, Dordrecht, the Netherlands. Debouck, D., and Smartt, A. J. 1995. Beans, Phaseolus spp. ­(Leguminosae-­Papilionoideae). Pages 287-­294 in: Evolution of Crop Plants, 2nd ed. J. Smartt and N. W. Simmonds, eds. ­Longman, London, U.K. Gepts, P. 1998. Origin and evolution of common bean: Past events and recent trends. HortScience 33:1124-­1130. Gepts, P., and Debouck, D. 1991. Origin, domestication, and evolution of the common bean (Phaseolus vulgaris L.). Pages 7-­53 in: Common Beans: Research for Crop Improvement. A. van Schoonhoven and O. Voysest, eds. CAB International, Wallingford, U.K., and CIAT, Cali, Colombia. Kaplan, L. 1967. Archeological Phaseolus from Tehuacán. Pages 201­211 in: The Prehistory of the Tehuacán Valley, Vol. 1: Environment and Subsistence. D. E. Beyers, ed. University of Texas, Austin. Kaplan, L. 1980. Variation in the cultivated beans. Pages 145-­148 in: Guitarrero Cave: Early Man in the Andes. T. F. Lynch, ed. Academic Press, New York. Kaplan, L., and McNesh, R. S. 1960. Prehistoric bean remains from caves in the Ocampo region of Tamaulipas, Mexico. Bot. Mus. Leafl. Harv. Univ. 19:33-­56. Koinange, E. M. K., Singh, S. P., and Gepts, P. 1996. Genetic control of the domestication syndrome in common-­bean. Crop Sci. 36:1037-­1045. Myers, J. R., and, Baggett, J. R. 1999. Improvement of snap beans. Pages 289-­330 in: Common Bean Improvement in the Twenty-­First Century. S. P. Singh, ed. Kluwer Academic Publishers, Dordrecht, the Netherlands. Schwartz, H. F., Brick, M. A., Harveson, R. M., and Franc, G. D., eds. 2004. Dry Bean Production and Pest Management, 2nd ed. Reg. Bull. 562A. Colorado State University, Fort Collins, CO. Singh, S. P. 1982. A key for identification of different growth habits of Phaseolus vulgaris L. Annu. Rep. Bean Improv. Coop. 25:92-­94. Singh, S. P. 1999. Production and utilization. Pages 1-­24 in: Common Bean Improvement in the Twenty-­First Century. S. P. Singh, ed. Kluwer Academic Publishers, Dordrecht, the Netherlands. Singh, S. P., and Gutiérrez, J. A. 1984. Geographical distribution of the DL1 and DL2 genes causing hybrid dwarfism in Phaseolus vulgaris L., their association with seed size, and their significance to breeding. Euphytica 33:337-­345. Singh, S. P., and Molina, A. 1996. Inheritance of crippled trifoliolate leaves occurring in intensive crosses of common bean and its relationship with hybrid dwarfism. Euphytica 26:665-­679. Singh, S. P., Gepts, P., and Debouck, D. G. 1991. Races of common bean (Phaseolus vulgaris L.). Econ. Bot. 45:379-­396. Singh, S. P., Gutiérrez, J. A., Molina, A., Urrea, C., and Gepts, P. 1991. Genetic diversity in cultivated common bean: II. Marker-­based analysis of morphological and agronomic traits. Crop Sci. 31:23-­29. Skroch, P. W., and Nienhuis, J. 1995. Qualitative and quantitative characterization of RAPD variation among snap bean (Phaseolus vulgaris) genotypes. Theor. Appl. Genet. 91:1078-­1085. Voysest, O., Valencia, M. C., and Amezquita, M. C. 1994. Genetic diversity among Latin American Andean and Mesoamerican common bean cultivars. Crop Sci. 34:1100-­1110. White, J. F., and Laing, D. R. 1989. Photoperiod response of flowering in diverse genotypes of common bean (P. vulgaris). Field Crops Res. 22:113-­128.

diseases, such as bean golden mosaic and southern blight, are important in localized geographic areas. Still other diseases, such as wildfire, are of minor importance. Annual production losses in world bean production as a result of diseases average about 10%. In view of the large number of potential diseases, their wide distribution, and the capacity of several diseases to cause extensive crop damage, it is apparent that losses in bean production would be much higher in the absence of disease management practices. A concerted, worldwide approach to the study of bean diseases and their management ensures the continued production of this important food legume for direct human consumption. A plant is diseased when it is not functioning normally. Disease is the result of an interaction among the plant, its environment, and one or more harmful factors in the environment. These harmful agents may be infectious organisms (such as fungi, bacteria, nematodes, and phytoplasmas) or infectious agents (such as viruses, viroids, and related entities) that can reproduce only in the living plant. Plant diseases are also caused by abiotic agents, such as toxic chemicals, nutrient deficiencies, drought, and heat. Biotic and abiotic agents that cause disease are called pathogens. 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 irregularities. The abnormal functioning of the plant generally leads to reductions in quantity and quality of harvested pods or seeds. Parts of the pathogen seen on or in diseased plants are called signs of the disease; examples include fungal mycelium, masses of white to colored spores, and brown to black sclerotia. Symptoms and signs are very useful in determining the cause of a disease. Accurate disease diagnosis is critical to developing and recommending effective disease management procedures.

(Prepared by T. E. Michaels; Revised by M. A. Brick)

(Prepared by R. Hall; Revised by H. F. Schwartz and R. Hall)

Bean Diseases

Bean Pathogens

This compendium describes 73 bean diseases, 32 of which are caused by fungi, 5 by bacteria, 6 by nematodes, 26 by viruses, and 4 by phytoplasmas, plus numerous other noninfectious (abiotic) diseases and disorders. In addition, it describes the damage caused to bean plants by a wide range of environmental stresses. Some diseases, such as anthracnose, bean common mosaic, common bacterial blight, and white mold, can cause extensive or complete crop failure and are important throughout the bean production areas of the world. Other

Most bean diseases are caused by fungi. Fungi that cause diseases in beans are microscopic organisms whose body cells resemble threads (called hyphae), which, en masse, form a mycelium. Hyphae may have cross-­walls, called septa, and feed on the nutrients in the plant. Most fungi reproduce by forming specialized cells, called spores, that serve the fungus in many important ways. Some tolerate adverse conditions and permit the fungus to survive in the absence of the bean plant. Spores are an important means of dispersal and are often moved to the

Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, San Diego, CA. Allen, D. J., and Lenné, J. M. 1998. The Pathology of Food and Pasture Legumes. CAB International, Wallingford, U.K. Schwartz, H. F., and Pastor-­Corrales, M. A., eds. 1989. Bean Production Problems in the Tropics, 2nd ed. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Schwartz, H. F., Brick, M. A., Harveson, R. M., and Franc, G. D., eds. 2004. Dry Bean Production and Pest Management, 2nd ed. Reg. Bull. 562A. Colorado State University, Fort Collins, CO. Wortmann, C. S., Kirkby, R. A., Eledu, C. A., and Allen, D. J. 1998. Bean diseases. Pages 63-­86 in: Atlas of Common Bean (Phaseolus vulgaris L.) Production in Africa. CIAT Pub. No. 297. Pan-­Africa Bean Research Alliance Report, Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Zaumeyer, W. J., and Thomas, H. R. 1957. A Monographic Study of Bean Diseases and Methods for Their Control. U.S. Dep. Agric. Tech. Bull. 868.

5

bean plant by wind, soil, water, or other agents. Once at a site suitableforinfectionunderfavorableenvironmentalconditions, they germinate to produce germ tubes and, subsequently, new hyphae that penetrate the bean plant through wounds, natural openings, or the intact surface. Spores may also differ genetically from one another and thus enable new forms of the fungus to develop. Fungal pathogens of beans are identified mostly by the size, shape, and color of their spores. These and other structures, such as sclerotia and sexual fruiting bodies produced by fungal pathogens of beans, are described more fully under each pathogen. Fungal pathogens cause a wide range of symptoms on beans. Most frequently they cause variously colored (brown, yellow, red, or black) spots or blotches on leaves, stems, pods, seeds, or roots. Bacteria that cause bean diseases are microscopic and appear cream colored or yellow en masse. They are rod shaped, motile, and generally gram negative; they do not form spores. They survive well in infected plant material, such as seeds and debris. However, in natural environments, they generally survive only for short periods apart from living plants or plant residues. They are dispersed by water, soil, infected plant parts, aerosols, and insects. They enter bean plants through natural openings or wounds and cause water-­soaked spots and blotches that soon die and turn reddish brown on leaves, pods, or seeds. Nematodes (eelworms) are microscopic, slender, wormlike animals. They move by swimming in films of water between soil particlesoronplantsurfaces.Nematodesdevelopfromeggs,and the subsequent juvenile stages feed on the root system by puncturing the plant with a hollow, needlelike mouthpiece ­(stylet) and absorbing the plant cell contents. They are disseminated in water, soil, and plant material. In beans, they cause rotting or swelling (galls) of roots and may produce stunted plants. Viral pathogens of beans are large, complex molecules composed of a nucleic acid core (either ribonucleic acid [RNA] or deoxyribonucleic acid [DNA]) and a protein coat. They can be seen with an electron microscope but are too small to be seen with a light microscope. Virus particles (virions) may be short or long rods or polyhedral in shape. They reproduce only in the living plant cells. They may be transmitted among plants in sap (mechanical transmission), in seeds, or by insects, such as aphids, whiteflies, and beetles. Common symptoms of viral infections include leaf mosaics (light and dark green or yellow areas), chlorosis, malformations (twisting or puckering), and plant stunting. Phytoplasma organisms are prokaryotes and range in size from 175 nm to 150 µm. They are various shapes, including spherical, ovoid, and filamentous. They lack a cell wall; are bounded by a three-­layered membrane; and contain cytoplasm, ribosomes, RNA, and DNA. They occur in phloem sieve tubes and are transmitted by leafhoppers. Symptoms of infection include yellowing, stunting, reddening, witches’-­broom, and dieback. Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, San Diego, CA. Allen, D. J., and Lenné, J. M. 1998. The Pathology of Food and Pasture Legumes. CAB International, Wallingford, U.K. Schwartz, H. F., and Pastor-­Corrales, M. A., eds. 1989. Bean Production Problems in the Tropics, 2nd ed. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Schwartz, H. F., Brick, M. A., Harveson, R. M., and Franc, G. D., eds. 2004. Dry Bean Production and Pest Management, 2nd ed. Reg. Bull. 562A. Colorado State University, Fort Collins, CO. Zaumeyer, W. J., and Thomas, H. R. 1957. A Monographic Study of Bean Diseases and Methods for Their Control. U.S. Dep. Agric. Tech. Bull. 868.

(Prepared by R. Hall; Revised by H. F. Schwartz and R. Hall) 6

Bean Disease Management Rational disease management recommendations are developed from detailed knowledge of the biology of the plant pathogen and the epidemiology of the disease. Thus, for each disease caused by an infectious organism or agent, this compendium describes survival, transmission, infection, host range, 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 developeffectivescoutingcalendarsandmanagementstrategies thatreducetheharmfuleffectsofthepathogenonthebeanplant andthatareconsistentwitheconomicproductionofthecropand protectionoftheenvironment.Themostcommonmanagement approachesforbeandiseasesincludetheuseofdisease-­resistant cultivars, pathogen-­free seeds, and cultural practices (e.g., crop rotation, crop residue management, and tillage practices) that suppress the pathogen or restrict its ability to spread or infect the plant. Another common avenue of disease management is the treatment of the soil, seeds, or crops with timely applications of chemical pesticides and biopesticides. The most effective and sustainable management of bean disease is obtained whenseveraldiseasemanagementmethodsareintegratedwith each other and with bean production ­practices. Selected References Agrios, G. N. 2005. Plant Pathology, 5th ed. Academic Press, San Diego, CA. Allen, D. J., and Lenné, J. M. 1998. The Pathology of Food and Pasture Legumes. CAB International, Wallingford, U.K. Schwartz, H. F., and Pastor-­Corrales, M. A., eds. 1989. Bean Production Problems in the Tropics, 2nd ed. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Schwartz, H. F., Brick, M. A., Harveson, R. M., and Franc, G. D., eds. 2004. Dry Bean Production and Pest Management, 2nd ed. Reg. Bull. 562A. Colorado State University, Fort Collins, CO. Zaumeyer, W. J., and Thomas, H. R. 1957. A Monographic Study of Bean Diseases and Methods for Their Control. U.S. Dep. Agric. Tech. Bull. 868.

(Prepared by R. Hall; Revised by H. F. Schwartz and R. Hall)

Bean Diagnostic Guidelines Effective diagnostic procedure follows a logical sequence of steps, and considerable experience is necessary to achieve a high degree of competence in this process. This section provides guidelines regarding the sequential nature of disease diagnosis that may be helpful to less-­experienced individuals. It is important to remember that multiple pathogens are commonly associated in a diseased plant and that disease symptoms vary greatly on different bean cultivars and under different environmental conditions. Classical disease symptoms and the abbreviated identification key provided here might, therefore, be a misleading oversimplification of the problem at hand. Disease in beans, as in other plants, can be considered an interaction among susceptible bean genera and species (i.e., host or susceptible), the causal agent (pathogen), and an environment favorable for pathogen attack on the host. These contributing factors provide helpful sources of information needed for disease diagnosis.

Observe the Symptoms

The appearance of disease symptoms on affected beans is an important source of diagnostic information. However, one should view symptoms in the entire field, as well on individual bean plants.

Field symptoms are the visible disease patterns within the field. Stand symptoms are quite varied and are extremely important in disease diagnosis. For example, affected plants may be uniformly scattered across the area or they may be confined to low-­lying wet areas or drier ridge tops. Disease may appear in the field as small circular spots, irregular concentrated patches, or large rings or circles, or it may have an unpatterned appearance or be uniform throughout the field. Occasionally, injury appears in the affected fields as bands, streaks, or other patternsthatsuggestmechanicaldamagefromfarmequipment or misapplication of fertilizers or pesticides. The soil under the plant and the roots should be closely inspected for insect pests or evidence of excessively applied fertilizers or other granular ­chemicals. Individual plant symptoms are generally more apparent than are overall crop symptoms and include leaf spots, stem or petiole lesions, leaf blighting, wilting, yellowing, mottling, stunting, necrosis, and root rots. It is essential to observe carefully what parts of individual plants are affected. Leaf spots can be very diagnostic, since leaf spots are often distinctive in shape, color, and size for an individual disease. Leaf blighting, wherein the tissue dies quickly, is a symptom that is distinct from leaf spots. Leaf-­blighting fungi typically produce a brownish necrosis or rot of leaf tissue, which lacks a definite form that is characteristic of leaf spots. Blighted areas in leaves can be any size or shape and may involve sectors between leaf veins of the entire leaf. Symptoms of viral infection differ according to the cultivar of bean and virus species. Bean cultivars that are susceptible to viruses may respond by turning yellow or forming necrotic local lesions, mild systemic mottling, or severe mosaic and stunting, or they may remain symptomless. Symptoms on pods may appear as dark green, irregularly shaped, blotched areas on green-­podded types and as greenish yellow areas on yellow-­podded types. Pod deformation with poor seed set and reduced seed size or plants that are completely barren of flowers and pods may also occur.

Observe the Environmental Conditions

The cultural and climatological environment prior to and during the onset of disease problems is an additional source of diagnostic information. Temperature, light intensity and duration, and moisture conditions provide critical diagnostic information. The nature of the affected site is also important. Air, water drainage, soil type, sun exposure, terrain slope, age of the stand, and proximity of windbreaks or structures may all be significant factors in bean disease development. Prior chemical applications (including pesticides, fertilizers, and industrial waste from a leak or spill [i.e., lubricating oil]) to the site may also provide important clues in disease diagnosis. Dense bean stands may trigger or amplify certain disease problems by altering the microenvironment.

Identify Visible or Microscopic Signs of the Pathogen The appearance of the causal agent, when it can be observed, is a critical and important aid to disease diagnosis. This is true whether the observation of the pathogen is macroscopic, microscopic, or both. Certain structures of some bean pathogens may be visible without magnification. For diseases such as powdery mildew and rust, black, white, or orange spores of the causal fungus often are visible on affected bean foliage. Observation of lower leaves may reveal other signs, such as infection mats, acervuli, or sclerotia. When the causal fungus is visible, its appearance is often the most important clue in disease ­identification. The use of a 10–20× hand lens may assist in identifying the cause of observed abnormalities. Mechanical and insect feeding injury may be differentiated from leaf damage caused by infectious agents under the lens. Fungal fruiting bodies, such as

acervuli, sporodochia, pycnidia, or perithecia, may be visible with low magnification. If microscopic examination of affected plant parts does not reveal the presence of fungal structures, tissues showing symptoms may be incubated for 24–48 h in a moist chamber (e.g., plastic bag with wet paper towel at 25°C). The moist environment may induce sporulation or hyphal proliferation. It must be remembered, however, that any fungus present on infected tissue, including saprophytes and epiphytes, may grow in such an environment. When spores or other structures are produced on infected tissue, this material can be mounted in tap water on a glass slide for microscopic examination. Small, dark structures that are sometimes present in leaf or stem lesions may be the necks of flask-­shaped pycnidia produced by fungi in the subdivision Deuteromycotina (order Sphaeropsidales) or the perithecia of fungi in the subdivision Ascomycotina. These structures can be removed from the leaf or stem tissue with a needle, mounted intact in a drop of water on a glass slide, and gently crushed by applying pressure to a glass coverslip placed on the drop of water. Mature spores will ooze out of the pycnidia or perithecia and may be identifiable. If small, spore-­bearing fruiting bodies or cushions (acervuli or pycnidia) are present in leaf lesions, it may be necessary to cut thin cross sections of these structures to observe the morphology of the fruiting body. This technique is particularly useful for fungi that produce spores in acervuli (Colletotrichum spp.) or pycnidia (Ascochyta or Phoma spp.). There are three blights of beans caused by bacteria: common blight, caused by Xanthomonas axonopodis pv. phaseoli (Smith) Vauterin et al.; halo blight, caused by Pseudomonas syringae pv. phaseolicola (Burkholder) Young et al.; and bacterial brown spot, caused by Pseudomonas syringae pv. syringae van Hall. The symptoms appear first on the lower side of the leaves as small, water-­soaked spots and many have yellow halos. The spots enlarge, coalesce, and may form large areas that later become necrotic. When small slices of the infected leaves or pods are placed on a slide in a drop of water and observed with a dissecting scope, a cloud of bacterial ooze may be evident emerging from the cut edge. If pathogenic fungi and bacteria are not apparent on or within affected tissue, symptoms may have resulted from viral infection or abiotic causes, such as excessive fertilizers, salts, herbicides, heat, moisture, cold, atmospheric pollution, soil pH, mechanical injuries, or other noninfectious agents. The foregoing techniques are particularly useful in attempts to diagnose foliar diseases of beans. Because soils abound with saprophytic fungi, it may be more difficult to determine the cause of injury or disease occurring in roots and belowground stems. Diagnostic techniques may initially include washing the roots and preparing thin sections of symptomatic tissue to view with a microscope. Other techniques include attempts to isolate causal pathogens on various culture media, treating root or stem tissues with chemicals to render them transparent, applying stains to selectively color fungal structures, and growing susceptible plants over infected tissue to trap a pathogen. These techniques require specialized equipment and considerable skill on the part of the diagnostician.

Collection and Submission of Samples

Samples for disease diagnosis should be taken when the problem is active or increasing. Areas should be selected for sampling where the damage or symptoms are representative of the entire affected area, and samples should be obtained before the application of pesticides. Samples should be collected at the edge of an infected area, and they should include both healthy and infected plants exhibiting various stages of infection. Samples taken weeks after the onset of symptoms or when plants are senescing are generally of little value to the diagnostician. As soon as possible after collection, samples should be wrapped in dry paper toweling (wet paper toweling frequently 7

leads to sample decay prior to arrival at the clinic); placed in a container, such as a self-­sealing plastic bag, to prevent desiccation; and delivered promptly to the clinic. In cases in which the whole plant is collected, it is helpful to wrap the root system in a smaller plastic bag to prevent contamination of foliage with soil particles during handling and shipment. Since the clinician who receives the sample will not have an opportunity to observe the problem in the field, it is essential that the following information accompany the sample: 1) the bean cultivar affected and extent of damage; 2) the cultural and climatological environment of the affected area; 3) a complete, accurate description of the symptoms and date of first appearance on individual plants (Polaroid or digital photographs of symptoms included with samples are very useful to diagnosticians); and 4) the chemicals (e.g., herbicides) used on or near the crop during that season or the previous season. For the most accurate diagnosis, samples should reach the diagnostician in approximately the condition they were in when collected. Rapid delivery of samples to the clinic is essential. If personal delivery of the sample is not possible, the quickest carrier available should be used. Priority mail or overnight delivery services are valuable for this purpose. Samples should never be sent at the end of the week, since this may result in the sample sitting undelivered over the weekend. (Prepared by R. T. McMillan)

Bean Crop Health and Integrated Pest Management The major components of pest management that provide the foundation for integrated pest management (IPM) consist of exclusion, eradication, protection, resistance, and biological ­management. Exclusion prevents the entrance and establishment of a plant pathogen in an uninfested region by prohibition, interception, and elimination. This is primarily accomplished by implementation of quarantine, embargo, inspection, and certification of plant materials, such as bean seeds, that are transported between production regions. Eradication emphasizes the removal, elimination, or destruction of a pest from an area in which it is already established. This is primarily accomplished for beans by detection and removal of diseased plants or infested plant debris; elimination of weed hosts and alternate crops; sanitation; crop rotation; and destruction of pests by disinfestation or disinfection by heat (burning), tillage, or pesticides. Protection is the placement of a protective barrier between the susceptible host and the pest. Application of protectant or systemic chemicals, such as fungicides, bactericides, insecticides, nematicides, and herbicides, is the best example of this principle, but manipulation of environmental factors, usually by cultural practices such as planting time, row orientation, and row spacing/plant density, are also beneficial. Resistance to a pathogen is genetically inherited and is usually expressed as a result of an interaction between a pest and the host at the cellular level that limits, but does not eliminate, pest development; that elicits plant defense mechanisms; or both. Resistance also helps plants escape disease (via modifications in canopy architecture, flowering, and maturity). Tolerance, whereby plants are susceptible to disease but yield and quality are not diminished, is often mistakenly referred to as resistance. Resistance strategies used with beans include nutrition to increase plant vigor but not to overstimulate vegetative growth; selection of plants that are less affected by a pest, and multiplication of seeds of the selected plants; and hybridization and selection of desirable progeny from crosses between 8

susceptible and less-­susceptible or resistant parents. The developing field of genetic engineering offers much promise for improved resistance, particularly in those species in which limited progress has been made to date. Biological management is the use of natural enemies and competitors to manage insect pests, pathogens, and weeds. This may be accomplished through conservation of existing biological control agents via appropriate choice of selective pesticides to be applied, augmentation of biological control agent population densities through release of additional individuals, or inundation through the release of sufficient biological control agents to reduce the pest population densities to a subeconomic damage level. An additional approach, often termed classical biological management, is to collect natural enemies of an exotic pest within its native range and release them into areas where the pest has been introduced.

Bean Crop Health

This section contains excerpts from the review chapter on IPM published in the authoritative book edited by S. P. Singh entitled Common Bean Improvement in the Twenty-­First Century. The goal of IPM is to achieve relief from pests in a manner that ensures safety, profitability, and durability while shifting the perceived focus on pesticide-­intensive strategies to a systems approach that emphasizes biological knowledge of pests and their interactions with crops. The shift to a systems approach with primary and secondary tactics requires that we move toward management of all pests rather than target only key pests, such as a single insect, pathogen, or weed species. Primary tactics rely upon knowledge of the managed ecosystem and its natural processes that suppress pest populations; and secondary tactics rely upon intervention with pesticides or physical or biological supplementation. A simplistic categorization of bean IPM strategies during the last 25 years in temperate-­cropping systems would show that the bean industry has emphasized pest management via pesticides as a primary tool, followed closely by plant resistance and, finally, by cultural practices. On the other hand, tropical-­cropping systems have emphasized traditional cultural practices, followed by plant resistance, with pesticide management often assuming a distant third. It is also important to note the important common role that host resistance plays across bean production systems. Host resistance is reviewed in great detail in other references and is obviously an important fundamental of, but is not an exclusive substitute for, any IPM strategy that is devised and implemented for the dynamic complex of pests faced by bean crops in various cropping systems throughout the world. Reliance on a single management strategy, e.g., host resistance, runs counter to the very core of the IPM philosophy. More in-­depth sources of information on specific biotic stress managementapproachesareavailablefromnumerousresearch papers and reviews, including those by Allen et al., Beebe and Pastor-­Corrales, Hall, Hall and Nasser, Schwartz and ­Pastor­Corrales, Schwartz and Peairs, van Schoonhoven and Voysest, and Wortmann et al.

Bean IPM Tactics

Hall and Nasser published a thorough review of 33 specific diseasemanagementelementsthatareutilizedorrecommended individually and collectively to manage 50 bean diseases worldwide. A review of the elements utilized to manage diseases reveals that only a small number of those elements actually constitute the bulk of the current IPM strategies employed. The major emphasis for most diseases has been on 1) crop rotation of more than 2 years between bean crops; 2) timely application of specific pesticides that are effective against the target pest; 3) tillage practices that promote host plant development, reduce carryover of the pathogen, or both; 4) weed management to reduce the level of host plant stress from competition, microclimatic influences, and sources of pests (refugia); 5) multiple

cropping with nonhosts and crop barriers to reduce pathogen spread; and 6) plant resistance to one or more plant pathogens. Cultural practices, which include crop rotation, are recommended as a management strategy for 80% of the bean diseases; whereas use of resistant cultivars is recommended as a management practice for 44% of the more-­common bean diseases (e.g., rust, common bacterial blight, and bean common mosaic). The effectiveness of individual IPM elements is quite varied and unique for specific types of diseases and underscores the complexity surrounding the design and implementation of disease management strategies. Resistance to many plant pathogens may not be complete enough to protect the plant from significant loss in yield and quality, so other elements, which include cultural practices, are essential to supplement the partial gain realized by resistance. In addition, resistance may be less effective because of genotype × environmental interactions, and few cultivars are likely to possess long-­lasting resistances to all elements (i.e., races) of a pathogen or pest complex, thereby requiring a more complete protection strategy for overall plant health. The following list of cultural practices has been applied in various combinations to bean IPM strategies in temperate-­and ­tropical-­cropping systems alike. Continued emphasis upon adoption of the primary elements will provide the most immediate impact upon priority pathogens and diseases, and adoption of the secondary elements can further enhance the effectiveness of IPM strategies in specific cropping systems in temperate and tropical regions.

Primary IPM Elements • • • • • • • • • • •

crop rotation eliminating volunteer beans and infested debris clean fallow and burning pathogen-­free seeds cultivar selection for adaptation and disease ­resistance soil temperatures of 18°C or higher at planting seeding dates seeding depth suppressing weeds and insect pests tillage (preplant and postemergence) timely harvest

Secondary IPM Elements • •

acceptable pH adequate level of organic matter

• • • • • • • •

adequate and balanced soil fertility soil moisture levels near field capacity judiciously using surface or overhead irrigation appropriate growth habit, plant population, and plant spacing row orientation separating bean fields and using biological barriers roguing limiting movement of equipment and personnel within and between fields Selected References

Allen, D. J., Buruchara, R. A., and Smithson, J. B. 1998. Diseases of common bean. Pages 179-­265 in: The Pathology of Food and Pasture Legumes. D. J. Allen and J. M. Lenné, eds. CAB International, Wallingford, U.K. Beebe, S. E., and Pastor-­Corrales, M. A. 1991. Breeding for disease resistance. Pages 561-­617 in: Common Beans—­Research for Crop Improvement. A. van Schoonhoven and O. Voysest, eds. CAB International, Wallingford, U.K., and CIAT, Cali, Colombia. Hall, R. 1995. Challenges and prospects of integrated pest management. Pages 1-­19 in: Novel Approaches to Integrated Pest Management. R. Reuveni, ed. Lewis Publishers, Boca Raton, FL. Hall, R., and Nasser, L. C. B. 1996. Practice and precept in cultural management of bean diseases. Can. J. Plant Pathol. 18:176-­195. Maloy, O. C. 1993. Plant Disease Control—­Principles and Practice. J. Wiley & Sons, Inc., New York. Schwartz, H. F., and Pastor-­Corrales, M. A. 1989. Bean Production Problems in the Tropics. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Schwartz, H. F., and Peairs, F. B. 1999. Integrated pest management. Pages 371-­388 in: Common Bean Improvement in the Twenty-­First Century. S. P. Singh, ed. Kluwer Academic Publishers, Boston, MA. Schwartz, H. F., Brick, M. A., Harveson, R. M., and Franc, G. D., eds. 2004. Dry Bean Production and Pest Management, 2nd ed. Reg. Bull. 562A. Colorado State University, Fort Collins, CO. van Schoonhoven, A., and Voysest, O. 1991. Common Beans: Research for Crop Improvement. CAB International, Wallingford, U.K., and CIAT, Cali, Colombia. Wortmann, C. S., Kirkby, R. A., Eledu, C. A., and Allen, D. J. 1998. Atlas of Common Bean (Phaseolus vulgaris L.) Production in Africa. CIAT Pub. No. 297. Pan-­Africa Bean Research Alliance Report, Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia.

(Prepared by H. F. Schwartz, J. R. Steadman, and R. Hall)

9

Part I. Infectious Diseases Fungal Diseases of Subterranean Parts Aphanomyces Root and Hypocotyl Rot Aphanomyces euteiches Drechs. was known to infect beans under greenhouse conditions as early as the 1960s, but it wasn’t until 1979 that A. euteiches was isolated from beans in the field. That year, a strain designated A. euteiches f. sp. phaseoli W. F. Pfender & D. J. Hagedorn, capable of causing severe root and hypocotyl rot in beans in the field, was discovered in central Wisconsin. A. eutiches f. sp. phaseoli has also been reported in New York, and Aphanomyces spp. have also been reported to cause root rot in Australia. Since Aphanomyces spp. generally are associated with other pathogenic fungi, they may be obscured on culture media and go undetected.

Plants may be severely stunted. Typically, the pathogen grows up the hypocotyl to produce a lesion above the soil line (Figs. 4 and 5). This lesion is slightly water-­soaked and gray-­green in appearance at its leading edge, but it becomes brown as the necrosis develops. Seedlings may be killed as the lesions extend to the growing point of the plant, especially in mixed infections with Pythium spp. (Figs. 6 and 7).

Symptoms

The pathogen can infect plants from soon after emergence to late in the season. It does not cause seed rot or preemergence damping-­off. Lesions on roots are initially yellow-­brown and fairly firm. They rapidly coalesce to involve most of the roots, which become softer as the cortex is destroyed. The infected roots soon darken from the activity of secondary invaders.

Fig. 5. Snap beans from a field infested with Pythium ultimum and Aphanomyces euteiches f. sp. phaseoli, showing moderate (left) and mild (right) root rot. (Courtesy D. J. Hagedorn, from the files of W. F. Pfender)

Fig. 4. Snap beans grown in soil containing Aphanomyces euteiches f. sp. phaseoli (center and right). Check is on the left. (Cour­ tesy D. J. Hagedorn, from the files of W. F. Pfender)

10

Fig. 6. Snap beans grown at 28°C in soil that were (left to right) uninfested, infested with Pythium ultimum alone, infested with Aphanomyces euteiches f. sp. phaseoli alone, and infested with both pathogens. (Courtesy D. J. Hagedorn, from the files of W. F. Pfender)

Causal Organism

A. euteiches has aseptate mycelium and can produce two kinds of spores. Thick-­walled oospores are formed by sexual fusion of the oogonia and antheridia (Fig. 8). When they germinate, oospores form hyphae or sporangia. The sporangia produce asexual swimming spores (zoospores). Primary spores are extruded from the sporangia in single file and encyst at the mouth of the sporangium. Within hours, zoospores emerge from these cysts, swim for a brief time, encyst again, and then germinate to produce hyphae that infect host tissue. A. euteiches f. sp. phaseoli can be differentiated from other strains of A. euteiches by slow growth at 30°C and a larger aplerotic zone. The fungus is readily isolated from newly infected plants before the infected tissue is severely rotted. Isolation from the advancing margin of the hypocotyl lesion is often successful. The pathogen grows quickly from segments of surface-­sterilized tissue placed on water agar or on a semiselective culture medium. Aphanomyces spp. can be recognized by their sparse, arachnoid growth habit on cornmeal agar and by the characteristic appearance of the hyphae under microscopic observation. The identity of a suspected isolate of the genus Aphanomyces can be confirmed by inducing it to form its characteristic sporangia and zoospore cysts. This can be accomplished by floating small agar plugs, cut from the margin of a colony grown on cornmeal agar, in a dilute solution of salts or in dilute, sterilized lake water.

sandy soils, the population of Aphanomyces spp. can increase rapidly (during one to two seasons) to very damaging levels. Severe losses have occurred in the second year of production on land that had been previously uncultivated. The host range and persistenceofthispathogeninweedshavenotbeen­determined. Soil moisture and temperature are important determinants of disease severity. Since Aphanomyces spp. are water molds, they are most active at high soil moisture levels and cause the most severe disease during wet seasons and in fields irrigated frequently. Infection can occur at all temperatures favorable to bean growth, but disease is more severe at 20–28°C (Fig. 6) than at 16°C (Fig. 7). Pythium ultimum Trow is frequently associated with Aphanomyces spp. in infected plants. In controlled studies with inoculum levels similar to those in field soil, A. euteiches f. sp. phaseoli was more damaging than was P. ultimum at 20–28°C but less damaging than was P. ultimum at 16°C. Mixed infections by the two pathogens increase disease severity synergistically and cause increased mortality of infected plants, especially at higher temperatures.

Disease Cycle and Epidemiology

Oospores can persist in a dormant state in the soil for years. Sporangia and zoospores are produced in infected roots and presumably are active in secondary cycles of the disease, although this has not been demonstrated in nature. They are produced in infected cortical tissue within 2 weeks after infection and are released to the soil as roots decay. Oospores may be dispersed long distances in infested soil. The host range of A. euteiches f. sp. phaseoli includes alfalfa, as well as snap beans and dry beans. The fungus does not cause severe disease on pea, soybean, or common hosts of several other Aphanomyces spp. Some A. euteiches isolates can produce disease on beans but cause much less damage than does A. euteiches f. sp. phaseoli (Fig. 9). To date, A. euteiches f. sp. phaseoli has been reported only from irrigated, sandy soils. Whether it is limited to this environment is not known, but an unidentified Aphanomyces species was important in a root rot complex in a clay loam soil in Australia. When beans are grown without rotation on irrigated,

Fig. 7. Snap beans grown at 16°C in soil that were (left to right) uninfested, infested with Pythium ultimum alone, infested with Aphanomyces euteiches f. sp. phaseoli alone, and infested with both pathogens. (Courtesy D. J. Hagedorn, from the files of W. F. Pfender)

Fig. 8. Oogonia, antheridia, and oospores of Aphanomyces euteiches f. sp. phaseoli. (Courtesy W. F. Pfender)

Fig. 9. Snap beans infected with Apha­ nomyces euteiches f. sp. pisi W. F. Pfender & D. J. Hagedorn (left) and A. euteiches f. sp. phaseoli (right). Check is in the center. (Courtesy D. J. Hagedorn, from the files of W. F. Pfender)

11

Management

The most effective management for this disease is avoidance of infested fields. Soil from prospective bean fields should be tested in the laboratory for its root rot potential. Regular rotation of crops may be helpful in delaying buildup of Aphanomyces populations. Chemical management is not currently ­available. Managementthroughgeneticresistanceisbeinginvestigated, and resistance has been found in some breeding lines. However, genetic linkages between resistance and agronomically un­ desirable traits must be overcome. The incorporation of crucifer green manures has shown some potential for reducing the incidence of Aphanomyces root rot in several crops, including beans. Selected References Carley, H. E. 1970. Detection of Aphanomyces euteiches races using a differential bean series. Plant Dis. Rep. 54:943-­945. Delwiche, P. A., Grau, C. R., Holub, E. B., and Perry, J. B. 1987. Characterization of Aphanomyces euteiches isolates recovered from alfalfa in Wisconsin. Plant Dis. 71:155-­161. Holub, E. B., Grau, C. R., and Parke, J. L. 1991. Evaluation of the forma specialis concept in Aphanomyces euteiches. Mycol. Res. 95:147-­157. Malvick, D. K., Grau, C. R., and Percich, J. A. 1998. Characterization of Aphanomyces euteiches strains based on pathogenicity tests and random amplified polymorphic DNA analyses. Mycol. Res. 102:465-­475. O’Brien, R. G., O’Hare, P. J., and Glass, R. J. 1991. Cultural practices in the control of bean root rot. Aust. J. Exp. Agric. 31:551-­555. Pfender, W. F., and Hagedorn, D. J. 1982. Aphanomyces euteiches f. sp. phaseoli, a causal agent of bean root and hypocotyl rot. Phytopathology 72:306-­310. Pfender, W. F., and Hagedorn, D. J. 1982. Comparative virulence of Aphanomyces euteiches f. sp. phaseoli and Pythium ultimum on Phaseolus vulgaris at naturally occurring inoculum levels. Phytopathology 72:1200-­1204. Scott, W. W. 1961. A monograph of the genus Aphanomyces. Va. Agric. Exp. Stn. Tech. Bull. 151. Stamps, D. J. 1978. Aphanomyces euteiches. Descriptions of Pathogenic Fungi and Bacteria, No. 600. Commonwealth Mycological Institute and Association of Applied Biologists, Kew, Surrey, England.

produced. The pathogen can be easily isolated from soil and infected tissues on fresh carrot disks or on culture media selective for the fungus. Asexual reproduction of T. basicola occurs by the formation of endoconidia (phialospores) and chlamydo­ spores (aleuriospores). Endoconidia are hyaline, small, and cylindrical. They are produced within the conidiophores (phialides) and are extruded singly or in chains. Chlamydo­ spores (Fig. 11) are thick walled, dark brown, and multicellular and are produced laterally or terminally in the hyphae. Cells of the chlamydo­spores eventually separate and germinate as individual infection units. Chlamydo­spores survive for long periods in soil, whereas endoconidia are short-­lived. The pathogen is disseminated within and between bean fields by movement of infested soil, infected host tissues, colonized debris, drainage water, or irrigation water, as well as by other means.

Disease Cycle and Epidemiology

Chlamydo­spores of T. basicola in soil germinate to produce multiple germ tubes and (eventually) several hyphae, which grow toward and onto the hypocotyl and root surfaces. These hyphae penetrate bean tissues through wounds, lesions incited by other bean pathogens, or the intact surface (without forming appressoria). Phosphatidase enzymes may play a major role in the initial penetration of epidermal cells and in later phases of pathogenesis. After penetration, the pathogen produces constrictedandnonconstrictedhyphaethatgrowwithinandbetween plant cells, respectively. Chlamydo­spores are produced by nonconstrictedhyphaethroughouttheinfectedtissues.Undermoist conditions,reproductivehyphaeemergethroughtheepidermal layer and eventually produce masses of chlamydo­spores and endoconidia. As infected host tissues decay, chlamydo­spores are

(Prepared by W. F. Pfender; Revised by L. E. Hanson)

Black Root Rot Black root rot is caused by Thielaviopsis basicola (Berk. & Broome) Ferraris (syn. Chalara elegans Nag Raj & Kendrick). The pathogen is widely distributed, can infect more than 130 plant species in 15 families, and causes severe black root rot diseases in ornamentals and crops, such as bean, carrot, cotton, pea, peanut, tomato, and tobacco. Black root rot can be a problem on beans in limited areas of the United States, Italy, and Germany, but it does not appear to be of significance in Latin America.

Fig. 10. Black root rot, caused by Thielaviopsis basicola (plants on the right). Healthy plant is on the left. (Courtesy D. J. Hagedorn, from the files of G. S. Abawi)

Symptoms

Initial symptoms of black root rot in beans appear as elongated, narrow lesions on the hypocotyl and root tissues. These lesions are initially reddish purple and then become dark charcoal to black. As the disease progresses, the lesions often coalesce and form large black areas (Fig. 10). The lesions may remain superficial and cause limited damage or become deep and cause stunting, premature defoliation, and eventually plant death.

Causal Organism

T. basicola grows and sporulates readily on artificial agar media but exhibits considerable variation in colony appearance, zonation, growth rate, and shape and number of spores 12

Fig. 11. Chlamydospores of Thielaviopsis basicola. (Courtesy G. S. Abawi)

released into the soil and, under favorable conditions, germinate to infect host tissue or colonize available organic debris. T. basicola grows and sporulates most abundantly in the labo­ ratory at relatively high temperatures (25–28°C) but damages beans most severely at lower temperatures (15–20°C). Black root rot is favored by wet, cool, neutral to alkaline soils and nitrogen fertilizers.

Management

Soil treatments with fungicides, such as thiabendazole and captan,orfumigants,suchasmethylisothiocyanateanddazomet, are effective against T. basicola on beans. However, the use of such chemicals is very limited because they are expensive and difficult to apply. Breeding lines have been produced with high levels of resistance to T. basicola and have been used in many breeding programs as sources of resistance to the black root rot pathogen. Three partially recessive genes appear to be responsible for this resistance through the production of two phytoalexins. Lowering the soil pH to less than 5.2 can significantly reduce the incidence of black root rot but may cause reduced plant growth.

seedlings. The cortex of the hypocotyl and older portions of the root become progressively more streaked and generally necrotic. Necrosis is largely confined to the cortex. If the root system grows unrestricted, plant productivity appears un­affected (Fig. 13). Diseasedplantsoftenrespondbyproducingnumerousadventitious roots (Fig. 12) from the hypocotyl in longitudinal rows near the soil surface, particularly when soil is mounded around the base of the plant during cultivation. When the disease is severe, plants are stunted and typically depend on a clump of adventitious roots for survival. Primary leaves of such plants prematurely turn yellow and drop off, especially if plants are stressed by moisture extremes and soil compaction. Diseased plants vary in size and vigor within a field, creating an irregular crop canopy.

Causal Organism

The causal organism is Fusarium solani (Mart.) Sacc. f. sp. phaseoli (Burkholder) W. C. Snyder & H. N. Hans. The fungus produces septate, hyaline mycelium. Its macroconidia have mostly three septa (5.1 × 44.5 µm) and four septa (5.3 × 50.9

Selected References Abawi, G. S. 1989. Root rots. Pages 105-­157 in: Bean Production Problems in the Tropics, 2nd ed. H. F. Schwartz and M. A. ­Pastor­Corrales, eds. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Chittaranjan, S., and Punja, Z. K. 1994. Factors influencing survival of phialospores of Chalara elegans in organic soil. Plant Dis. 78:411-­415. Christou, T. 1962. Penetration and host-­parasite relationships of Thielaviopsis basicola in the bean plant. Phytopathology 52:194-­198. Hassan, A. A., Wilkinson, R. E., and Wallace, D. H. 1971. Relationship between genes controlling resistance to Fusarium and Thielaviopsis root rots in bean. J. Am. Soc. Hortic. Sci. 96:631-­632. Papavizas, G. C., Lewis, J. A., and Adams, P. B. 1970. Survival of root­infecting fungi in soil. XIV: Effect of amendments and fungicides on bean root rot caused by Thielaviopsis basicola. Plant Dis. Rep. 54:114-­118. Pierre, R. E. 1971. Phytoalexin induction in beans resistant or susceptible to Fusarium and Thielaviopsis. Phytopathology 61:322-­327. Punja, Z. K., and Sun, L. J. 1999. Morphological and molecular characterization of Chalara elegans (Thielaviopsis basicola), cause of black root rot on diverse plant species. Can. J. Bot. 77:1801-­1812. Yarwood, C. E., and Levkina, L. M. 1976. Crops favoring Thielaviopsis. Plant Dis. Rep. 60:347-­349.

Fig. 12. Fusarium root rot, caused by Fusarium solani f. sp. phaseoli. Note proliferation of adventitious roots on the plant on the right following severe rotting of the lower roots. (Courtesy R. Hall)

(Prepared by G. S. Abawi; Revised by L. E. Hanson)

Fusarium Root Rot Fusarium root rot (Fusarium foot rot, dry root rot) of beans occurs in most bean-­growing areas throughout the world. The disease usually causes little damage in unstressed plants. However, under conditions of reduced root growth caused by drought, soil compaction, soil saturation after rill irrigation, or oxygen stress, Fusarium root rot can almost destroy a bean crop. Even the highest levels of resistance to the disease are overcome by the pathogen when fields are flooded or roots are deprived of oxygen for short time periods (e.g., 24 h). The disease is often found associated with Rhizoctonia root rot and Pythium root rot (and possibly others) in a complex (Fig. 12).

Symptoms

The first symptoms that appear are narrow, longitudinal, red to brown streaks on hypocotyls and taproots of 7-­to 10-­day-­old

Fig. 13. Improved root growth by subsoiling at a depth of 20 cm between rows (right) compared with lack of subsoiling (left). (Courtesy H. F. Schwartz)

13

µm), rarely five septa, of uniform diameter along their length, are curved, and are rounded or slightly pointed at the apex (Fig. 14). Microconidia are rare. Conidia are borne in sporodochia. Chlamydo­spores are globose (11.6 µm), terminal or intercalary in conidia or hyphae, and single or in short chains (Fig. 15). Cultures are relatively slow-­growing compared with other formae speciales of F. solani and contain various shades of blue or green depending on the isolate and the culture medium (Fig. 16). No perfect state has been described for this forma ­specialis.

inconsequential until a third crop of beans is grown in that new field, when, for example, in sandy loam soils of the northwestern United States, the fungus becomes uniformly distributed in the plowed layer of soil. Observations suggest that F. solani f. sp. phaseoli can sustain itself as a saprophyte but reaches pathogenic potential only by multiplying on bean crops. Excellent methods have been developed to monitor this pathogen in soil. The disease is more severe in cool, moist soil, but suppression of yield is greater under drought conditions.

Disease Cycle and Epidemiology

Numerous efforts to reduce localized foot rot symptoms on the hypocotyl and taproot have failed. Rarely, if ever, have seed treatments or other localized chemical treatments increased bean yields. Bean yields in Fusarium-­infested fields were not increased even by complete protection of hypocotyls and taproots if the remainder of the root system extended into infested soil. Promising treatments with various biological organisms have recently been reported for reducing disease severity and improving nutrient uptake and plant growth. These organisms include the root-­nodulating symbiont Rhizobium leguminosarum (Frank) Frank bv. phaseoli (of D. C. Jordan in Bergey’s Manual), and the vesicular-­arbuscular mycorrhizal Glomus mosseae (Nicolson & Gerdemann) Gerdemann & Trappe. Soil fumigation with chemicals, such as chloropicrin or methyl bromide, also can manage the disease but is rarely cost effective. Because soil conditions greatly affect Fusarium root rot, cultural practices can be employed to counteract the disease. Good soil fertility is important in maximizing bean yields, whether or not root rot is a problem. However, the form or quantity of nitrogen or other fertilizer elements has not been found to either stimulate or reduce the disease incidence in the field. Mounding soil around the plants can increase adventitious root formation and reduce the damaging effects of the disease on plant productivity. Wide spacing of plants within the row decreases spread between root systems, but plant populations that provide complete ground cover often give the highest seed yields. Beans grown in warm soil (20°C and higher) with near-­optimal soil water potential usually suffer little from Fusarium root rot. Several green manure crops, when plowed into the soil, reduced disease severity from Fusarium root rot in subsequent kidney bean crops. The strongest antifungal activity was observed with red clover and alfalfa as precrops. Minimizing soil compaction is probably the most effective means of root rot management. This can be achieved by loosening sublayers or wheel tracks with chisels before or at planting time, by not cultivating wet soil, and by reducing the pressure exerted by wheels on the soil surface. The addition of large amounts of organic matter to the soil by rotation of beans with crops such as small grains and alfalfa tends to counteract root

The pathogen resides in soil mainly as thick-­walled chlamydo­ spores. These resting spores germinate readily when stimulated by nutrients (e.g., sugars and amino acids) exuded by germinating seeds and root tips. Resulting hyphae penetrate the bean plant directly and through stomata and wounds. Hyphae pene­ trate the intercellular spaces of the cortex but stop at the endodermis. Under conditions of high soil moisture levels, conidia may be produced on sporodochia emerging from stomata near the soil surface. As infected tissues degenerate, conidia and hyphae convert to chlamydo­spores to complete the life cycle. Chlamydo­spores of F. solani f. sp. phaseoli can germinate and reproduce in soil near seeds and roots of many nonsusceptible plants and other organic matter. Thus, the fungus may survive in infested fields indefinitely, for example, in soil planted continuously to nonhost crops for more than 30 years. F. solani f. sp. phaseoli is believed to disperse in soil, in dust, or on seeds. Infested soil and organic matter are also spread locally by wind and water. When beans are grown for the first time in fields adjacent to infested fields, however, the disease is

Fig. 14. Macroconidia of Fusarium solani f. sp. phaseoli. (Cour­ tesy R. Hall)

Fig. 15. Chlamydospores of Fusarium solani f. sp. phaseoli. (Cour­tesy R. Hall)

14

Management

Fig. 16. Cultures of Fusarium solani f. sp. phaseoli (left and center) and F. solani (right) on potato dextrose agar. (Courtesy R. Hall)

rot by reducing compaction and increasing the water-­holding capacity of the soil. Decaying alfalfa roots provide channels for deep penetration of the soil by bean roots. Sometimes, however, nondecomposed organic matter from almost any previous crop may be toxic to bean roots and increase root rot. Bean genotypes differ in degree of sensitivity to Fusarium root rot. None are known to be highly resistant. Bush-­type beans with less-­vigorous root systems generally suffer more root rot than do indeterminate types with larger, more-­vigorous root systems. Cultivars with resistance or tolerance to the disease or to predisposing factors have recently become available. Rapid improvement of resistance may now be enhanced with the discovery of resistance in the bean genome associated with certain host defense responses, including loci controlling ­pathogenesis­related proteins. Utilization of resistant or tolerant beans together with practicable management of soil nutrition, moisture, and compaction manage Fusarium root rot effectively. Selected References Buonassi, A. J., Copeman, R. J., Pepin, H. S., and Eaton, G. W. 1986. Effect of Rhizobium spp. on Fusarium solani f. sp. phaseoli. Can. J. Plant Pathol. 8:140-­146. Burke, D. W., and Miller, D. E. 1983. Control of Fusarium root rot with resistant beans and cultural management. Plant Dis. 67:1312-­1317. Dar, G. H., Zargar, M. Y., and Beigh, G. M. 1997. Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mossea and Rhizobium leguminosarum. Microb. Ecol. 34:74-­80. Kraft, J. M., Burke, D. W., and Haglund, W. A. 1981. Fusarium diseases of beans, peas, and lentils. Pages 142-­156 in: Fusarium Diseases, Biology, and Taxonomy. P. E. Nelson, T. A. Tousson, and R. J. Cook, eds. Pennsylvania State University Press, University Park. Okumura, M., Higashida, S., Yamagami, M., and Shimono, K. 1994. Effects of different preceding crops on Fusarium root rot of kidney bean. Jpn. J. Soil Sci. Plant Nutr. 65:274-­281. Roman-­Aviles, B., Snapp, S. S., and Kelly, J. D. 2004. Assessing root traits associated with root rot resistance in common bean. Field Crops Res. 86:147-­156. Schneider, K. A., Grafton, K. F., and Kelly, J. D. 2001. QTL analysis of resistance to Fusarium root rot in bean. Crop Sci. 41:535-­542. Sippell, D. W., and Hall, R. 1982. Effects of pathogen species, inoculum concentration, temperature, and soil moisture on bean root rot and plant growth. Can. J. Plant Pathol. 4:1-­7. Snapp, S., Kirk, W., Roman-­Aviles, B., and Kelly, J. 2003. Root traits play a role in integrated management of Fusarium root rot in snap bean. HortScience 38:187-­191.

Causal Organism

Fusarium yellows is caused by the fungus Fusarium oxy­ sporum Schlechtend.:Fr. f. sp. phaseoli J. B. Kendrick & W. C. Snyder. At least seven pathogenic races are known. Maximum mycelial growth occurs on culture medium at 28°C. The fungus typically has hyaline, nonseptate chlamydo­spores (2–4 × 6–15 µm) and macroconidia that are elongate, have two or three septa (3–6 × 25–35 µm), and are slightly curved.

Disease Cycle and Epidemiology

The pathogen inhabits soil in the form of chlamydo­spores and may also infest seeds. Although symptoms occur only on Phaseolus spp., the pathogen can colonize the roots of other plants, particularly legumes, and produce chlamydo­spores without causing symptoms or disease. Infection of Phaseolus beans occurs through roots and hypocotyls, most commonly through wounds. Thereafter, the fungus grows throughout and plugs the vascular tissue, causing the plant to become chlorotic and drop its leaves or wilt. The optimum temperature for disease development is 20°C. Extremes of soil moisture levels do not appear to be needed

Fig. 17. Fusarium yellows, caused by Fusarium oxysporum f. sp. phaseoli. (Courtesy H. F. Schwartz)

(Prepared by D. W. Burke and R. Hall; Revised by R. M. Harveson and G. Yuen)

Fusarium Wilt (Yellows) Fusarium wilt or yellows was originally discovered in dry beans in California in 1928. It has since been found elsewhere in the United States, South and Central America, Spain, and Africa. The disease is becoming more important in the midwestern United States and is considered to be important in Brazil. A similar disease of scarlet runner bean has been reported in England and the Netherlands.

Symptoms

Initial symptoms are slight yellowing and premature senescence of the lower leaves. The chlorotic symptoms progress up the plant until all leaves are bright yellow (Fig. 17), followed by wilting and discoloration (tan to brown) of foliage. If plants are infected when young, they remain stunted. The vascular tissues usually become reddish brown, often extending beyond the second node (Fig. 18).

Fig. 18. Reddish brown discoloration of vascular tissue of a plant affected by Fusarium yellows, caused by Fusarium oxysporum f. sp. phaseoli. (Courtesy H. F. Schwartz)

15

for the disease to occur but can influence disease severity. Soil compaction and poor drainage also appear to aggravate disease ­severity.

Management

Little information is available on management of the disease. Tolerant or resistant cultivars are recommended where available. Race-­specific resistance conferred by single to multiple genes from different races of beans has been incorporated with conventional breeding and molecular techniques into various bean cultivars. This resistance is effective against many of the seven or more pathogenic races that occur worldwide. Crop rotation may help in reducing soil inoculum levels if reservoir hosts are avoided. Chemical seed treatment and reduction of soil compaction also may be useful. Selected References Abawi, G. S. 1989. Root rots. Pages 105-­157 in: Bean Production Problems in the Tropics, 2nd ed. H. F. Schwartz and M. A. ­Pastor­Corrales, eds. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. Alves-­Santos, F. M., Benito, E. P., Eslava, A. P., and Diaz-­Minguez, J. M. 1999. Genetic diversity of Fusarium oxysporum strains from common bean fields in Spain. Appl. Environ. Microbiol. 65:3335-­3340. Cramer, R. A., Byrne, P. F., Brick, M. A., Panella, L., Wickliffe, E., and Schwartz, H. F. 2003. Characterization of Fusarium oxysporum isolates from common bean and sugar beet using pathogenicity assays and random-­amplified polymorphic DNA markers. J. Phytopathol. 151:352-­360. Dhingra, O. D., and Coelho Netto, R. A. 2001. Reservoir and non­reservoir hosts of bean-­wilt pathogen, Fusarium oxysporum f. sp. phaseoli. J. Phytopathol. 149:463-­467. Fall, A. L., Byrne, P. F., Jung, G., Coyne, D. P., Brick, M. A., and Schwartz, H. F. 2001. Detection and mapping of a major locus for Fusarium wilt resistance in common bean. Crop Sci. 41:1494-­1498. Ribeiro, R. de L. D., and Hagedorn, D. J. 1979. Screening for resistance to and pathogenic specialization of Fusarium oxysporum f. sp. phaseoli, the causal agent of bean yellows. Phytopathology 69:272-­276. Salgado, M. O., Schwartz, H. F., and Brick, M. A. 1995. Inheritance of resistance to a Colorado race of Fusarium oxysporum f. sp. phaseoli in common beans. Plant Dis. 79:279-­281.

(Prepared by D. J. Hagedorn; Revised by H. F. Schwartz and G. Yuen)

Phymatotrichum Root Rot Phymatotrichum root rot, also commonly known as Texas root rot, cotton root rot, and Ozonium root rot, is found primarily in alkaline, calcareous soils of the southwestern United States and northern Mexico. The fungus has been reported in India, Russia, and the United States (Hawaii), but disease losses have not been reported in those areas. The pathogen infects more than 2,000 species of dicotyledonous plants, and all beans are very susceptible.

Symptoms

The first symptom of the disease is slight yellowing or bronzing of the leaves, followed by sudden wilting when plants begin to flower. Cortical tissue is usually killed, sloughs easily, and is covered by a visible network of hyphal strands. Plants usually die within a few days after wilting, often in a circular pattern, as the fungus grows radially from dying plants. After rains, spore mats of the fungus may occur on the soil surface around the stems of dead plants. 16

Causal Organism

Phymatotrichum omnivorum Duggar (syn. Phymatotrichopsis omnivora (Duggar) Hennebert), also referred to as Ozonium omnivorum Shear in older literature, produces rhizomorphlike strands in soil that are composed of a large central hypha entwined by many smaller hyphae. Hyphae have characteristic branches at right angles to the strands, often referred to as cruciform branching. Sclerotia are formed in coarse portions of strands away from a food base. A conidial state (similar to Botrytis spp.) is formed on spore mats after frequent rains and cloudy days. Conidia are globose, single-­celled, and 4.5–5.0 µm in diameter; they usually do not germinate in culture. The teleomorph has been reported as Hydnum omnivorum Shear and as Sistotrema brinkmannii (Bres.) J. Eriksson. In another case, a basidial stage produced in vitro was named Trechispora brinkmannii (Bres.) D. P. Rogers & H. Jackson.

Disease Cycle and Epidemiology

As plants die, sclerotia form on rhizomorphlike strands in the roots. The sclerotia persist deep (45–75 cm) in the soil or in the living roots of susceptible hosts. Strands of the fungus grow outward from sclerotia until they contact a descending root. They entwine the root and grow toward the soil surface. When the strands grow around the upper root system, they proliferate and form a cottony growth of hyphae around the plant. The fungus invades the roots through wounds or directly through the cortex. It can invade the inner root tissues, blocking the flow of water and photosynthates through the vascular system. Environmental fluctuations cause disease severity to vary from year to year. The disease is rarely found in acidic soils (pH <6.0) or in soils with less than 1% calcium carbonate. The pathogen may be introduced on the roots of various plants, including transplanted trees and ornamentals. The fungus is favored by warm (25–35°C), moist soils and thrives in heavier soils with irrigation. It persists where the temperature does not fall below –23°C, where the mean annual temperature exceeds 15°C, and where a frost-­free period of 200 days annually occurs. It is thought that high CO2 levels and the formation of bicarbonate in poorly drained soils promote pathogen growth and suppress competitive microorganisms. If the fungus is introduced into sandy, acidic soils, it grows and kills plants, but it does not produce sclerotia and persist.

Management

It is very difficult to manage Phymatotrichum root rot because the fungus behaves erratically and disease severity varies from year to year. No resistance to the pathogen is known in beans. Monocotyledons are less susceptible to the pathogen than are dicotyledons, and a 4-­year rotation with corn, sorghum, or grasses is recommended. Weeds should be managed. Clean fallow for 1 year delays infection and reduces disease severity. Deep-­chisel or deep-­plow tillage and organic soil amendments, such as green manure crops, animal manure, or composts, may reduce the disease severity. Planting rows of monocotyledons or digging barriers adjacent to infested areas keeps the fungus from growing into surrounding soil. Soil fumigation or deep injection of ammonia to kill the fungus may be justified in a high-­value crop. Selected References Baniecki, J. F., and Bloss, H. E. 1969. The basidial stage of Phymatotrichum omnivorum. Mycologia 61:1054-­1059. Lyda, S. A. 1978. Ecology of Phymatotrichum omnivorum. Annu. Rev. Phytopathol. 16:193-­209. Streets, R. B., and Bloss, H. E. 1973. Phymatotrichum Root Rot. Monogr. 8. American Phytopathological Society, St. Paul, MN.

(Prepared by D. R. Sumner; Revised by R. M. Harveson)