Compendium of Wheat Diseases and Pests, Third Edition by Scientific Societies

Compendium of Wheat Diseases and Pests THIRD EDITION

Edited by William W. Bockus Kansas State University, Manhattan

Robert L. Bowden U.S. Department of Agriculture Manhattan, Kansas

Robert M. Hunger Oklahoma State University, Stillwater

Wendell L. Morrill Montana State University, Bozeman

Timothy D. Murray Washington State University, Pullman

Richard W. Smiley Oregon State University, Pendleton

The American Phytopathological Society

Front cover photograph by Jeff Vanuga, USDA Natural Resources Conservation Service Back cover photograph by William W. Bockus

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: 2010900316 International Standard Book Number: 978-0-89054-385-6 ďŁŠ 1977, 1987, 2010 by The American Phytopathological Society First edition published 1977 Second edition published 1987 Third edition published 2010 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 The first edition of the Compendium of Wheat Diseases was published in 1977, and the second edition in 1987. Dr. Maury Wiese, of Michigan State University and the University of Idaho, is to be commended for initiating and coordinating the preparation of those two editions. There are over 28,000 cop ies in circulation, and they have been an excellent resource for researchers, students, diagnosticians, producers, and virtually anyone else in the wheat industry. Because of the large amount of new information about wheat diseases that had been discovered since 1987, it became evident that a third edition was needed. The impetus for the third edition came from meetings of the North Central Edu cation/Extension Research Activities committee number 187 (NCERA-187: Management of Small Grain Diseases). As a result of discussions at the June 2005 meeting in Ithaca, New York, I was recruited to oversee the production of the third edi tion, with the understanding that the sister organization in the western United States, Western Education/Extension Activities committee number 97 (WERA-97: Diseases of Cereals), would be contacted and a representative from that region recruited for the editorial team. Some initial work had already been carried out by Dr. Rob ert Bowden (USDA-ARS), Dr. Robert Hunger (Oklahoma State University), Dr. Gregory Shaner (Purdue University), and Dr. Richard Smiley (Oregon State University). Dr. Shaner donated his list of potential chapters and authors for the third edition. The other three agreed to become associate editors to oversee the development of the sections on diseases caused by bacte ria, viruses, and nematodes, respectively. Dr. Timothy Murray (Washington State University) was recruited to oversee the update of the section on fungal diseases and to represent the western United States in addition to Dr. Smiley. The third edition is different from the earlier editions in that experts on each disease, insect, or disorder were recruited to

prepare the chapter on that specific problem. Additionally, the treatment of insects has been greatly expanded, and 16 chap ters on insect and mite pests of wheat have been added. There fore, an entomologist was needed on the editorial team, and Dr. Wendell Morrill (Montana State University) was recruited to serve as associate editor for the section on insects. To reflect this important addition, the title was changed to Compendium of Wheat Diseases and Pests. Over 70 authors were recruited to update existing chapters or to prepare new chapters. Compared with the second edition, the third edition has over 30 new chapters, the number of illus trations has been increased from 189 to 269, and the number of color illustrations has been increased from 74 to 246. Most of the illustrations are new. Another new feature of the third edition is that the color illustrations have been placed near the corresponding text rather than gathered in a separate section of color plates. It is hoped that this third edition will be as useful as the first two to those interested in wheat diseases and insects. While the important diseases and insects have been included, it is recog nized that even this comprehensive treatise is not an exhaustive treatment of all of the known pathogens and insects that have been documented on wheat. Similarly, the references that are cited after each chapter are designed to introduce the reader to the literature and are not exhaustive lists of all relevant publi cations. However, it is the view of the editorial team that the use of recognized experts as chapter authors has produced an upto-date treatment of each disease and insect that should prove to be a valuable resource to the wheat community.

iii

Bill Bockus Kansas State University

Authors Michael J. Adams Rothamsted Research Harpenden, Herts., United Kingdom

Xianming Chen U.S. Department of Agriculture Washington State University Pullman, Washington

Leopold A. Fucikovsky Instituto de Fitosanidad Colegio de Postgraduados Montecillo, Mexico

Vijay Kumar Choppakatla Oklahoma State University Stillwater, Oklahoma

Denis A. Gaudet Lethbridge Research Centre Agriculture and Agri-Food Canada Lethbridge, Alberta, Canada

Michael L. Avery U.S. Department of Agriculture National Wildlife Research Center Gainesville, Florida

Erica Cline U.S. Department of Agriculture Systematic Botany and Mycology Labo ratory Beltsville, Maryland

Rose C. Gergerich University of Arkansas Fayetteville, Arkansas

Martin J. Barbetti University of Western Australia Nedlands, Western Australia, Australia

R. James Cook Washington State University Pullman, Washington

Gary C. Bergstrom Cornell University Ithaca, New York

William T. Crow University of Florida Gainesville, Florida

William W. Bockus Kansas State University Manhattan, Kansas

Ruth Dill-Macky University of Minnesota St Paul, Minnesota

El-Desouky Ammar Ohio State University Ohio Agricultural Research and Devel opment Center Wooster, Ohio

Nilsa A. Bosque-Pérez University of Idaho Moscow, Idaho Robert L. Bowden U.S. Department of Agriculture Plant Science and Entomology Research Unit Manhattan, Kansas Lee A. Calvert Centro Internacional de Agricultura Tropical Medley, Florida

Mauro Di Vito Istituto per la Protezione delle Piante Bari, Italy Joseph P. Doskocil Oklahoma State University Stillwater, Oklahoma Etienne M. Duveiller CIMMYT Mexico City, Mexico

Bikram S. Gill Kansas State University Manhattan, Kansas Roy E. Gingery U.S. Department of Agriculture Ohio State University Ohio Agricultural Research and Devel opment Center Wooster, Ohio Stewart M. Gray U.S. Department of Agriculture Cornell University Ithaca, New York Steve Haber Agriculture and Agri-Food Canada Cereal Research Centre Winnipeg, Manitoba, Canada Gary L. Hein University of Nebraska Panhandle Research and Extension Center Scotts Bluff, Nebraska

Michael C. Edwards U.S. Department of Agriculture Northern Crop Science Research Labo ratory Fargo, North Dakota

Ron Hines University of Illinois Dixon Springs Agricultural Center Simpson, Illinois

Lori M. Carris Washington State University Pullman, Washington

Myriam R. Fernandez Agriculture and Agri-Food Canada Semiarid Prairie Agricultural Research Centre Swift Current, Saskatchewan, Canada

Charla R. Hollingsworth University of Minnesota Northwest Research and Outreach Center Crookston, Minnesota

Brett Carver Oklahoma State University Stillwater, Oklahoma

Bruce Fitt Rothamsted Research Harpenden, Herts., United Kingdom

Don M. Huber Purdue University West Lafayette, Indiana

John L. Capinera University of Florida Gainesville, Florida

Robert M. Hunger Oklahoma State University Stillwater, Oklahoma Barry J. Jacobsen Montana State University Bozeman, Montana Alexander V. Karasev University of Idaho Moscow, Idaho James A. Kolmer U.S. Department of Agriculture University of Minnesota Cereal Disease Laboratory St Paul, Minnesota Joseph M. Krupinsky U.S. Department of Agriculture Northern Great Plains Research Labora tory Mandan, North Dakota Dale Leikam Kansas State University Manhattan, Kansas Roland F. Line Pullman, Washington Marcia P. McMullen North Dakota State University Fargo, North Dakota

Timothy C. Paulitz U.S. Department of Agriculture Root Disease and Biological Control Research Unit Washington State University Pullman, Washington Analía Perelló Universidad Nacional de La Plata La Plata, Buenos Aires, Argentina Dallas E. Peterson Kansas State University Manhattan, Kansas Margaret G. Redinbaugh U.S. Department of Agriculture Ohio State University Ohio Agricultural Research and Devel opment Center Wooster, Ohio Jack H. Riesselman Montana State University Bozeman, Montana Ian T. Riley South Australian Research and Development Institute Plant Research Centre University of Adelaide Urrbrae, South Australia, Australia

Phillip E. Sloderbeck Kansas State University Garden City, Kansas Richard W. Smiley Oregon State University Columbia Basin Agricultural Research Center Pendleton, Oregon Mark Sorrells Cornell University Ithaca, New York Jeffrey M. Stein South Dakota State University Brookings, South Dakota Drake C. Stenger U.S. Department of Agriculture University of Nebraska Lincoln, Nebraska Erik L. Stromberg Virginia Polytechnic Institute and State University Blacksburg, Virginia Fiona Tanzer University of Cape Town Rondebosch, South Africa

Zoran Ristic U.S. Department of Agriculture Plant Science and Entomology Research Unit Kansas State University Manhattan, Kansas

Sharyn Taylor South Australian Research and Development Institute Plant Research Centre Adelaide, South Australia, Australia

Roger Rivoal Institut National de la Recherche Agro nomique École National Supérieure Agronomique de Rennes Centre de Recherches de Rennes Le Rheu, France

Timothy C. Todd Kansas State University Manhattan, Kansas

Alan P. Roelfs Grantsburg, Wisconsin

Robert Vasey Leicester, England

Christopher C. Mundt Oregon State University Corvallis, Oregon

Tom A. Royer Oklahoma State University Stillwater, Oklahoma

David K. Weaver Montana State University Bozeman, Montana

Gordon M. Murray Charles Sturt University New South Wales Department of Pri mary Industries Wagga Wagga Agricultural Institute Wagga Wagga, New South Wales, Aus tralia

Edward P. Rybicki University of Cape Town Rondebosch, South Africa

Robert J. Whitworth Kansas State University Manhattan Kansas

Dallas L. Seifers Kansas State University Agricultural Research Center Hays, Kansas

Maurice V. Wiese University of Idaho Moscow, Idaho

Timothy D. Murray Washington State University Pullman, Washington

Gregory Shaner Purdue University West Lafayette, Indiana

Charles P. Woloshuk Purdue University West Lafayette, Indiana

Julie Nicol CIMMYT International Ankara, Turkey

James P. Shroyer Kansas State University Manhattan, Kansas

Hailin Zhang Oklahoma State University Stillwater, Oklahoma

Eugene A. Milus University of Arkansas Fayetteville, Arkansas Wendell L. Morrill Montana State University Bozeman, Montana Craig F. Morris U.S. Department of Agriculture Washington State University Pullman, Washington

Alfredo Urashima Universidade Federal de São Carlos Araras, São Paulo, Brazil

Contents 54 Stem Rust 55 Stripe Rust 56 Septoria tritici Blotch 58 Sharp Eyespot 60 Smuts 60 Common Bunt (Stinking Smut) 62 Dwarf Bunt 64 Flag Smut 65 Karnal Bunt 66 Loose Smut 69 Snow Molds 70 Pink Snow Mold 71 Sclerotinia Snow Mold (Snow Scald) 72 Snow Rot 73 Speckled Snow Mold (Typhula Blight) 74 Southern Blight (Sclerotium Base Rot, Sclerotium Wilt) 75 Stagonospora nodorum Blotch and Stagonospora avenae Blotch 77 Stem Scald (False Eyespot) 78 Storage Molds 79 Take-All 82 Tan Spot (Yellow Leaf Spot) 84 Tar Spot 84 Zoosporic Root Colonizers

Introduction 1 1 2 3

Importance of Wheat Wheat Production Losses The Wheat Plant Genetic Resources of Wheat

Diseases Caused by Bacteria 6 7 8 8 9 11 11 12 12 13

Aster Yellows Bacterial Leaf Blight Bacterial Mosaic Bacterial Sheath Rot Bacterial Streak and Black Chaff Basal Glume Rot Gumming Pink Seed Spike Blight Stem Melanosis

Diseases Caused by Fungi and Fungus-Like Organisms 16 17 18 19 19 20 22 23 23 26 28 29 30 32 34 37 39 40 42 42 43 45 47 48 50 53

Alternaria Leaf Blight Anthracnose Ascochyta Leaf Spot Aureobasidium Decay Black Head Molds (Sooty Head Molds) Black Point (Smudge) Blast Brown Root Rot Cephalosporium Stripe Common Root and Foot Rot and Associated Leaf and Seedling Diseases Dilophospora Twist and Leaf Spot Downy Mildew (Crazy Top) Ergot Eyespot (Strawbreaker Foot Rot) Fusarium Head Blight (Scab) Fusarium Root, Crown, and Foot Rots and Associated Seedling Diseases Halo Spot Mycotoxins Phoma Spot Platyspora Leaf Spot Powdery Mildew Pythium Root Rot Rhizoctonia Root Rot Ring Spot Rusts Leaf Rust

Diseases Caused by Nematodes 88 Cyst Nematodes 90 Root-Gall Nematode 91 Root-Knot Nematodes 92 Root-Lesion Nematodes 94 Seed-Gall Nematode 95 Stem Nematode 95 Stubby-Root Nematodes 96 Stunt Nematodes 97 Other Nematodes Associated with Wheat

Diseases Caused by Viruses and Viruslike Agents 99 Agropyron Mosaic 99 Barley Stripe Mosaic and Barley Yellow Stripe 100 Barley Yellow Dwarf 102 Barley Yellow Striate Mosaic 103 Brome Mosaic 103 Chloris Striate Mosaic (Australian Wheat Striate Mosaic) 104 Cocksfoot Mottle 104 European Wheat Striate Mosaic 105 Flame Chlorosis vii

106 High Plains Disease 107 Maize Streak 109 Northern Cereal Mosaic 109 Tenuivirus Diseases: Iranian Wheat Stripe and Rice Hoja Blanca 110 Wheat American Striate Mosaic 111 Wheat Dwarf 112 Wheat Soilborne Mosaic 113 Wheat Spindle Streak Mosaic and Wheat Yellow Mosaic 115 Wheat Spot Mosaic 115 Wheat Streak Mosaic 117 Wheat Yellow Leaf 118 Winter Wheat (Russian) Mosaic 118 Yellow Head Disease 119 Other Viruses Infecting Wheat

136 Wheat Strawworm (Hymenoptera: Eurytomidae) 136 White Grubs (Coleoptera: Scarabaeidae) 137 Wireworms (Coleoptera: Elateridae) and False Wireworms (Coleoptera: Tenebrionidae)

Other Pests and Disorders 138 Air Pollution Injuries 139 Albinism 140 Birds 140 Chemical Injuries 143 Chloride- and Zinc-Deficient Leaf Spots 144 Cold Stress 147 Crinkle Joint (The Bends) 147 Hail Damage 148 Heat Stress 148 Mammals 149 Melanism (Pseudoâ&#x20AC;&#x201C;Black Chaff) 150 Nutrient Imbalances 153 Physiological Leaf Spots 154 Preharvest Sprouting 154 Soil Compaction 154 Soil pH 155 Water Stresses (Flooding and Drought) 156 Wind Damage (Lodging) 156 Witchweeds (Striga Species) 158 Yellow Berry

Damage Caused by Insects and Mites 120 Armyworms and Cutworms (Lepidoptera: Noctuidae) 122 Cereal Aphids (Homoptera: Aphididae) 124 Cereal Leaf Beetle (Coleoptera: Chrysomelidae) 125 Grasshoppers (Orthoptera: Acrididae) 126 Hessian Fly (Diptera: Cecidomyiidae) 128 Mites Other Than Wheat Curl Mite 130 Stored-Grain Insects 131 Thrips (Thysanoptera: Thripidae) 132 Wheat Curl Mite (Acari: Eriophyidae) 133 Wheat Jointworm (Hymenoptera: Eurytomidae) 133 Wheat Stem Maggot (Diptera: Chloropidae) 134 Wheat Stem Sawfly (Hymenoptera: Cephidae)

159 Glossary 167 Index

viii

Rusts Rusts have been of great importance historically. These dis eases are mentioned in the earliest records of wheat cultivation. Wheat rusts changed the course of early civilizations by de stroying their major food source. The potential for wheat rusts to develop into widespread epidemics is well documented. In past decades in North America, it has been conservatively esti mated that rusts have decreased wheat yields by over 1 million metric tons annually. Similar statistics could be quoted for most wheat-growing regions of the world. By a wide margin, most of the scientific literature on wheat diseases concerns rusts. Three different rust diseases occur in wheat—stem rust, leaf rust, and stripe rust. They are named for the dry, dusty, yel low red or black spots and stripes (sori or pustules) that erupt through the plant epidermis. The size and surrounding color ation of urediniospore pustules (uredinia) determine the specific infection type, which can vary with different wheat cultivars, temperature, and races of the rust pathogen (Figs. 76–78). Rust epidemics that occur before or during flowering are the most damaging. Stripe rust infection of the wheat head is espe cially damaging, even if no infection occurs elsewhere on the plant. Rusts reduce seed yield, lower the forage value of the crop and diminish its winterhardiness, and predispose plants to other diseases. Rust infection modifies the host epidermis, re sulting in increased transpiration and respiration and decreased

photosynthesis, while also removing water and nutrients needed for plant growth and reproduction. Overall, rusts reduce plant vigor, seed filling, and root growth. Rusted wheat plants are less palatable to livestock.

Fig. 76. Stem rust infection types, in infection of wheat culms by Puccinia graminis f. sp. tritici: R = resistant; MR = moderately resistant; MS = moderately susceptible; S = susceptible. (Reprinted from Rust Scoring Guide, by permission of the Research Institute for Plant Protection, Wageningen, the Netherlands, and CIMMYT, Mexico City)

Fig. 77. Leaf rust infection types, in infection of wheat leaves by Puccinia triticina: R = resistant; MR = moderately resistant; MS = moderately susceptible; S = susceptible. (Reprinted from Rust Scoring Guide, by permission of the Research Institute for Plant Protection, Wageningen, the Netherlands, and CIMMYT, Mexico City)

Symptoms Rust symptoms and signs are most obvious in spring and summer but may occur at any time, beginning shortly after seedlings emerge. All aerial parts of the wheat plant are sus ceptible to infection, and more than one rust can occur on a single plant or leaf. Some infections are visible only as chlo rotic flecks or brown, necrotic spots, whereas others may result in sporulating pustules of various sizes.

Causal Organisms The three rust diseases of wheat are caused by highly spe cialized fungi: stem rust fungus Puccinia graminis Pers.:Pers. f. sp. tritici Erikss. & E. Henn. leaf rust fungi P. triticina Erikss., with populations specialized for sur vival on Triticum aestivum (bread wheat) and others specialized for T. turgidum (durum wheat)

P. tritici-duri Viennot-Bourgin (a member of the P. re condita complex), specialized for survival on durum wheat stripe rust fungus P. striiformis Westend. f. sp. tritici Erikss. Each species comprises numerous physiological races, dis tinguished by their patterns of pathogenicity on differential hosts. The interaction of specific pathogen avirulence genes and specific host resistance genes determines the infection type (Figs. 76–78) and distinguishes races of rust fungi. Many races that were prevalent in the past are insignificant today, because specific resistance genes have been incorporated into modern wheat cultivars by breeding. However, because of the capacity for genetic change through mutation and sexual reproduction of these pathogens, new races of rust fungi continually surface to threaten wheat production.

Disease Cycles Wheat rust fungi are considered obligate parasites, although a few strains have been grown vegetatively on agar media. A few unique strains can sporulate and complete their life cycle apart from host plants. Wheat rusts have complex life cycles that can involve alter nate hosts and up to five spore stages (Fig. 79). Urediniospores are produced in great number. They are dispersed by wind to other wheat plants, where they generate new infections and

additional urediniospores in intervals of as little as 7 days. P. tritici-duri produces fewer urediniospores, but this inoculum can be supplemented by aeciospores from newly formed aecia. Urediniospores are one-celled, spiny-walled, and dikaryotic (Figs. 80 and 81). They are nutrient-independent and germinate in contact with a film of water. Germ tubes penetrate the plant by means of an appressorial peg or penetrate stomata directly (in the case of the stripe rust pathogen). The pathogen then forms substomatal vesicles and intercellular hyphae with glo bose or lobed haustoria, which establish physiological contact with host cell membranes, to complete the infection cycle. Urediniospore production on host plants may be followed by teliospore development within uredinia or within separate telial sori. Teliospores are brown black, binucleate, and two-celled and have thick, smooth walls (Fig. 80). In P. graminis and P. triticina, teliospores remain within the sorus and persist over the winter. They germinate in spring, by a process of nuclear fusion, reductive division (meiosis), and production of a promy celium (basidium) with four haploid sporidia (basidiospores). Basidiospores cannot re-infect wheat but are carried by the wind to alternate hosts (Fig. 79). Basidiospores of P. striiformis are presumed functionless, because there is no known alternate host. In most wheat-producing areas worldwide, the alternate host plays little direct role in epidemics. The exception is P. tritici-duri, which may cycle to its alternate host throughout the growing season. Infection of alternate hosts produces yellow orange sori (pyc nia, a type of spermagonium) on the upper surface of leaves. Within the pycnia, uninucleate, hyaline spores (pycniospores, a type of spermatium) and receptive hyphae fuse in compatible pairs when brought into contact by rain or insects. Their fusion restores the dikaryon, which proliferates and erupts through the opposite leaf surface as an aecial cup. Dikaryotic, dry, yellow spores (aeciospores) are liberated from aecia and are carried by wind to wheat plants. Aeciospores germinate and penetrate plants by entering through stomata, and infection results in the production of urediniospores.

Epidemiology

Fig. 78. Stripe rust infection types, in infection of wheat leaves by Puccinia striiformis f. sp. tritici: R = resistant; MR = moderately resistant; MS = moderately susceptible; S = susceptible. (Reprinted from Rust Scoring Guide, by permission of the Research Institute for Plant Protection, Wageningen, the Netherlands, and CIMMYT, Mexico City)

Rust epidemics develop when compatible wheat plants and rust fungi are both present over a large area. With free moisture and temperatures between 15 and 25°C, infection is completed in 6–8 h, and urediniospores are produced in 7–10 days. Ure diniospores are numerous and are readily disseminated over vast distances by wind, so that a small fungal population can rapidly increase within a few weeks (one uredium can produce up to 10,000 urediniospores). This combination of large num bers of viable spores and efficient dissemination by wind makes the rust fungi remarkably successful parasites. Uredinia have limited survival ability, compared to telia, but can survive year-round on hosts in milder climates. Ure diniospores of the stripe rust fungus maintain their infectiv ity at lower temperatures than those of the leaf rust and stem rust fungi. Urediniospores often serve as sources of primary inoculum in spring and summer by virtue of long-distance dispersal by wind. The annual progression of urediniospores across continents is well documented. Thus, teliospores and al ternate hosts are required for the completion of pathogen life cycles but not for disease initiation. P. tritici-duri epidemics start with airborne aeciospores from its alternate host, Anchusa italica, growing near durum wheat. A few urediniospores are produced, which can re-infect wheat, but abundant teliospores are also produced, and they can germinate immediately, pro ducing basidiospores, which re-infect A. italica, resulting in another generation of aeciospores. Alternate hosts support the sexual stages of rust fungi and thereby are sources of new virulence combinations and of early spring inoculum (aeciospores). It may be possible for new races of rust fungi to develop apart from alternate hosts, through mu tation and parasexual mechanisms in the uredinial stage. 51

Management

Planting resistant cultivars is the best method of control足 ling wheat rusts. The heritability of rust resistance in wheat has been known for over 100 years and has been widely used

by breeders to develop resistant cultivars. However, resistance based on a single gene of the host is often rendered ineffective by shifts in pathogen virulence. Destroying alternate hosts in足 terrupts the life cycle of rust fungi, limits their diversity, indi足

Fig. 80. Urediniospores of (left to right) Puccinia triticina, P. graminis f. sp. tritici, and P. striiformis f. sp. tritici. (Cour足tesy R. L. Bowden)

rectly increases the stability of resistant cultivars, and prevents the production of early spring inoculum (aeciospores). In the United States, a program to remove barberry, the alternate host of the stem rust fungus, has achieved these goals. Protective or eradicative fungicides have been used for rust control. They are applied as foliar sprays where cost-benefit analyses show that they are profitable. Systemic foliar fungi cides are used in some regions, and systemic seed treatment show promise for controlling rust in seedlings. Early-maturing cultivars should be grown where possible. Spring wheat should be sown as early as possible and given ade quate phosphorus to ensure early maturity and perhaps escape peak rust periods. Autumn rust infections can be reduced by late-autumn seeding. Self-sown or volunteer wheat is a major source of urediniospores, which serve as inoculum in the next crop, and therefore volunteer plants should be destroyed. Selected References Anikster, Y., Bushnell, W. R., Roelfs, A. P., Eilam, T., and Manister ski, J. 1997. Puccinia recondita causing leaf rust on cultivated wheats, wild wheats, and rye. Can. J. Bot. 75:2082–2096. Chen, X. M. 2005. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] wheat. Can. J. Plant Pathol. 27:314–337. Kolmer, J. A. 2005. Tracking wheat rust on a continental scale. Curr. Opinion Plant Biol. 8:441–449. McIntosh, R. A., Wellings, C. R., and Park, R. F., eds. 1995. Wheat Rusts: An Atlas of Resistance Genes. Plant Breeding Institute, Uni versity of Sydney, CSIRO, Melbourne, Australia, and Kluwer Aca demic Publishers, Dordrecht, Netherlands. Nagarajan, S., Singh, H., Joshi, L. M., and Saari, E. E. 1976. Meteoro logical conditions associated with long-distance dissemination and deposition of Puccinia graminis tritici uredospores in India. Phyto pathology 66:198–203. Roelfs, A. P. 1985. Wheat and rye stem rust. Pages 3–37 in: The Cereal Rusts. Vol. 2. A. P. Roelfs and W. R. Bushnell, eds. Academic Press, Orlando, Fla. Roelfs, A. P., Singh, R. P., and Saari, E. E. 1992. Rust Diseases of Wheat: Concepts and Methods of Disease Management. CIMMYT, Mexico City. Samborski, D. J. 1985. Wheat leaf rust. Pages 39–59 in: The Cereal Rusts. Vol. 2. A. P. Roelfs and W. R. Bushnell, eds. Academic Press, Orlando, Fla. Stubbs, R. W. 1985. Stripe rust. Pages 61–101 in: The Cereal Rusts. Vol. 2. A. P. Roelfs and W. R. Bushnell, eds. Academic Press, Or lando, Fla.

(Prepared by Alan P. Roelfs)

Fig. 81. Urediniospores of Puccinia triticina erupting through the epidermis of a leaf. (Photo by M. F. Brown and H. G. Brotzman, reprinted from D. M. Rizzo, comp., 1997, Phytopathogenic Fungi: Scanning Electron Micrographs, APS Press Slide Collections, American Phytopathological Society, St. Paul, Minn.)

Leaf Rust Leaf rust (also called brown rust and orange rust) may be the most widely distributed disease of wheat. It is most prevalent in climates where wheat matures at temperatures of 25–30°C, as in the Great Plains of North America and the steppes of central Asia. Yield losses due to leaf rust can vary from trace levels to over 50%, depending on the stage of plant development when the initial infection occurs and the resistance of the wheat cultivar. The causal organism is the fungus Puccinia triticina Erikss. (syns. P. recondita Roberge ex Desm. f. sp. tritici (Erikss. & E. Henn.) D. M. Henderson, P. rubigo-vera (DC.) G. Winter). It produces orange red, round to ovoid uredinia, up to 1.5 mm in diameter, which are scattered or clustered primarily on the upper surface of leaf blades (Figs. 77 and 81). They are erum pent, but unlike the uredinia of the stem rust pathogen (Fig. 76), they do not cause conspicuous tears in the epidermal tissues at the uredinium margins (Fig. 77). Urediniospores are subgloboid, 15–30 µm in diameter, and red brown, with three to eight germ pores scattered in their thick, echinulate walls (Figs. 80 and 81). The optimum temperature for the germination of urediniospores and infection is 18°C, with free moisture on the leaf surface for at least 6 h. Temperatures in the range of 20–25°C are best for the development of uredinia. Telial sori develop beneath the epidermis, principally on leaf sheaths and blades. Telia are the size of uredinia, glossy black, and not erumpent. Teliospores are round or flattened at the apex, like those of P. striiformis. They are sometimes not produced in some environments or if plants become infected near maturity. Teliospore germination requires alternating pe riods of wet and dry. P. triticina reproduces in almost all wheat-growing regions by clonal production of urediniospores. The main alternate host, Thalictrum speciossimum, is found in Spain and Portugal. Isopyrum fumarioides has also been described as an alternate host in Siberia. Collections of P. triticina that are highly virulent to durum wheat and mostly avirulent to common bread wheats have been described. A leaf rust fungus affecting durum wheat and having an alternate host in the genus Anchusa has been described in Mo rocco; the pathogen is most likely a different species, P. recon dita, but it has been referred to as P. tritici-duri Viennot-Bourgin. Selected References Anikster, Y., Bushnell, W. R., Eilam, T., Roelfs, A. P., and Manister ski, J. 1997. Puccinia recondita causing leaf rust on cultivated wheats, wild wheats, and rye. Can. J. Bot. 78:2082–2095. Ben-Ze’ev, I. S., Levy, E., Eilam, T., and Anikster, Y. 2005. Whole-cell fatty acid profiles—A tool for species and subspecies classification in the Puccinia recondita complex. J. Plant Pathol. 87:187–197. Huerta-Espino, J., and Singh, R. P. 1994. First report of virulence to wheat with leaf rust resistance gene Lr19 in Mexico. Plant Dis. 78:640. Roelfs, A. P., Singh, R. P., and Saari, E. E. 1992. Rust Diseases of Wheat: Concepts and Methods of Disease Management. CIMMYT, Mexico City. Samborksi, D. J. 1985. Wheat leaf rust. Pages 39–59 in: The Cereal Rusts. Vol. 2. A. P. Roelfs and W. P. Bushnell, eds. Academic Press, Orlando, Fla. Sayre, K. D., Singh, R. P., Huerta-Espino, J., and Rajaram, S. 1998. Ge netic progress in reducing losses to leaf rust in CIMMYT-derived Mexican spring wheat cultivars. Crop Sci. 38:654–659. Singh, R. P., Huerta-Espino, J., Pfeiffer, W., and Figueroa-Lopez, P. 2004. Occurrence and impact of a new leaf rust race on durum wheat in northwestern Mexico from 2001 to 2003. Plant Dis. 88:703–708. Yehuda, P. B., Eilam, T., Manisterski, J., Shimoni, A., and Anikster, Y. 2004. Leaf rust on Aegilops speltoides caused by a new forma specialis of Puccinia triticina. Phytopathology 94:94–101.

(Prepared by James A. Kolmer) 53

Stem Rust Stem rust was recognized in classical Roman times as the “greatest of plant diseases.” However, detailed characteriza tion of the disease cycle did not begin until 1767. Stem rust of wheat (also called black rust and black stem rust) is caused by Puccinia graminis Pers.:Pers. f. sp. tritici Erikss. & E. Henn., which also parasitizes certain barley and rye cultivars and some grasses, especially wild barley (Hordeum jubatum) and goat grass (Aegilops spp.). The relationship between the various forms of P. graminis is uncertain. The species can be subdivided according to mor phology, pathology, and genetics; pathology and genetics pro vide the most similar classifications. The stem rust fungus is

Fig. 82. Aecial stage of Puccinia graminis f. sp. tritici, the wheat stem rust fungus, on a barberry leaf. (Courtesy B. J. Steffenson, reprinted from D. E. Mathre, ed., 1997, Compendium of Barley Diseases, 2nd ed., American Phytopathological Society, St. Paul, Minn.)

Fig. 83. Teliospores (above) and urediniospores (below) of Puccinia graminis f. sp. tritici, the wheat stem rust fungus. (Cour tesy A. P. Roelfs)

a specialized pathogen, with each forma specialis and race having a narrow host range. P. graminis f. sp. tritici completes part of its life cycle on alternate hosts, especially barberries (Berberis vulgaris and B. canadensis) and certain species of Mahonia, in addition to wheat. B. vulgaris is an erect woody shrub that reaches a height of 3 m. It bears prominent spines and clusters of two to six leaves at stem joints (Fig. 82). It has gray bark and yellow, inconspicu ous flowers in long, drooping clusters. Red berries, formed in late summer, overwinter on the plant. Barberries are cultivated as ornamentals or grow wild in clusters on uncultivated land. The Japanese barberry, B. thunbergii, appears to be immune to stem rust. The disease cycle of stem rust is depicted in Fig. 79. P. graminis f. sp. tritici forms uredinia on wheat stems, leaves, and leaf sheaths and occasionally on glumes, awns, and even seeds. The uredinia are conspicuously erumpent, with tat tered epidermal tissues at their margins (Fig. 76). They may erupt through both leaf surfaces, but they tend to be larger on the underside. The pustules are oval, elongate, or spindleshaped and up to 3 × 10 mm. Numerous infections on a stem can weaken it and cause the plant to lodge. Urediniospores are oval, oblong, or ellipsoidal, 15–24 × 21–40 µm, orange red, and dehiscent (Figs. 80 and 83). They have thick, spiny walls in dented with four median germ pores. Host maturity and the aging of uredinia initiate the formation of teliospores in uredinial sori or in separate erumpent telial sori. Teliospores are ellipsoidal to clavate, 15–20 × 40–60 µm, black brown, two-celled, and tapered at the apex, with smooth, thick walls and a slight constriction at the septum (Fig. 83). They have a terminal germ pore in the upper cell and a lateral germ pore in the lower cell. Teliospore germination normally follows a period of cold dormancy and yields a hyaline basidium (promycelium) on which four hyaline sporidia (basidiospores) develop on sterig mata. Basidiospores infect barberry and give rise to small, flask-shaped pycnia (spermagonia), which are sunken except for the ostiole (Fig. 84). The supporting leaf tissues are typi cally discolored yellow red. Pycnia exude slender, hyaline pyc niospores (spermatia) and receptive hyphae in small, sticky droplets that attract insects. Pycniospores fertilize compatible

Fig. 84. Pycnium (spermagonium) (top) and aecium (bottom) of Puccinia graminis f. sp. tritici, the wheat stem rust fungus, in a barberry leaf. (Courtesy W. W. Bockus)

receptive hyphae, which give rise to aecia on the underside of the leaf. Aecia on barberry leaves are yellow and hornlike, pro jecting up to 5 mm from the leaf surface (Figs. 82 and 84). Aeciospores are subglobose, 15–19 × 16–23 µm, smooth, light orange yellow, and formed in long, dry chains. They infect wheat and give rise to uredinia, completing the disease cycle. Urediniospores released from uredinia on wheat leaves initi ate new infections, from which new uredinia are formed, so that several cycles of urediniospores can be produced dur ing the growing season. In most areas, urediniospores are the major means of survival and spread of the pathogen and serve as inoculum in the development of epidemics. The optimum temperature for the development of stem rust is near 26°C. Disease development is seriously hampered below 15°C and above 40°C. The optimum conditions for infection by urediniospores are a temperature of 18°C and the presence of dew (free water) for 6–8 h, followed by a 3-h gradual warming with light, while free water is present. Delayed crop maturity especially favors stem rust develop ment, so late planting and growing late-maturing cultivars in creases the risk of stem rust. Stem rust has been controlled by planting resistant cultivars. However, sexual reproduction where barberry is present and mutation during the urediniospore cycle generate new viru lence combinations, which can result in epidemics in previously resistant cultivars.

chlorotic areas. Each uredinium contains thousands of yel low orange, spherical urediniospores, 20–30 µm in diameter, with thick, echinulate walls and six to 12 scattered germ pores. Urediniospores are yellow to orange in mass and powdery (Fig. 85A, B, and D–F). Distinct stripes are not formed on seedling leaves (Fig. 85B), but they develop on upper leaves after stem elongation (Fig. 85D and E). Depending on temperature and the resistance of the host plant, chlorotic or necrotic spots or stripes of vari ous sizes develop, with or without sporulation (Fig. 85G). In

Selected References Abbasi, M., Goodwin, S. B., and Scholler, M. 2005. Taxonomy, phylog eny, and distribution of Puccinia graminis, the black stem rust: New insights based on rDNA sequence data. Mycoscience 46:241–247. Bhardwaj, S. C., Nayar, S. K., Prashar, M., Kumar, J., Menon, M. K., and Singh, S. B. 1990. A pathotype of Puccinia graminis f. sp. trit ici on Sr24 in India. Cer. Rusts Powdery Mildews Bull. 18:35–37. Leonard, K. J., and Szabo, L. J. 2005. Stem rust of small grains and grasses caused by Puccinia graminis. Mol. Plant Pathol. 6:99–111. McIntosh, R. A., Wellings, C. R., and Park, R. F., eds. 1995. Wheat Rusts: An Atlas of Resistance Genes. Plant Breeding Institute, Uni versity of Sydney, CSIRO, Melbourne, Australia, and Kluwer Aca demic Publishers, Dordrecht, Netherlands. Pretorius, Z. A., Singh, R. P., Wagoire, W. W., and Payne, T. S. 2000. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis. 84:203. Roelfs, A. P. 1985. Wheat and rye stem rust. Pages 3–37 in: The Cereal Rusts. Vol. 2. A. P. Roelfs and W. R. Bushnell, eds. Academic Press, Orlando, Fla. Roelfs, A. P., and McVey, D. V. 1979. Low infection types produced by Puccinia graminis f. sp. tritici and wheat lines with designated genes for resistance. Phytopathology 69:722–730. Roelfs, A. P., Singh, R. P., and Saari, E. E. 1992. Rust Diseases of Wheat: Concepts and Methods of Disease Management. CIMMYT, Mexico City.

(Prepared by Alan P. Roelfs)

Stripe Rust Stripe rust (also called yellow rust) has been reported in more than 60 countries and on all continents except Antarctica. In the United States, the disease occurred mainly in the Pacific Northwest and California until 2000. Since then, it has become increasingly important in the South Central states and the cen tral Great Plains. The disease thrives where winters are mild and summers are cool.

Symptoms Infection can occur throughout the life of a plant. Symp toms first appear as chlorotic patches on leaves. Tiny, yellow to orange uredinia (0.3–0.5 × 0.5–1 mm) then develop in these

Fig. 85. Stripe rust of wheat. A, Infected seedlings in the field. B, Uredinial pustules on a seedling leaf, not forming stripes. C, Stripe rust foci early in the disease season. D, Uredinial pustules forming a stripe on a mature leaf. E, Heavy sporulation on leaves of mature plants, with few obvious stripes. F, Infected glumes and immature kernels. G, Necrotic stripes with few or no uredinial pustules on a wheat cultivar with durable, high-temperature adult-plant resistance. H, Black telial pustules on a leaf sheath. (Courtesy R. F. Line; composite by J. Foltz)

wheat heads, uredinia normally occur on the ventral surface of the glumes, and immature seeds are sometimes infected (Fig. 85F). The pathogen utilizes water and nutrients from the host plant and can desiccate the plant quickly. Dark brown to black telial pustules, which are persistently subepidermal and often form streaks on leaves and leaf sheaths (Fig. 85H), appear late in the crop season under moist condi tions. Teliospores can germinate without cold treatment to pro duce basidiospores under laboratory conditions.

Causal Organism Stripe rust is caused by Puccinia striiformis Westend. (syn. P. glumarum Erikss. & E. Henn.). It is not known to have an alternate host or to complete a sexual cycle. P. striiformis is subdivided into formae speciales based on virulence to different genera and species of cereal crops and grasses. For example, P. striiformis f. sp. tritici Erikss., the wheat stripe rust pathogen, mainly infects wheat and sometimes species of Aegilops, Agropyron, Elymus, and wild Hordeum, but rarely infects cultivated barley. P. striiformis f. sp. hordei, the barley stripe rust pathogen, mainly infects barley and occa sionally infects wheat and some grasses. The wheat and barley stripe rust pathogens do not cause disease in bluegrass or or chard grass, and the bluegrass and orchard grass pathogens (P. striiformis f. sp. poae and P. striiformis f. sp. dactylidis) do not cause disease in wheat and barley. Numerous races of the wheat stripe rust pathogen have been identified, distinguished by their differential ability to infect wheat cultivars with different genes for resistance.

Disease Cycle Stripe rust of wheat originates from mycelium that overwin ters in leaf tissues and, especially, from urediniospores that survive locally or are windborne from distant hosts. Infection may occur throughout autumn and winter, because mycelium remains viable to –5°C. Urediniospores lose viability rapidly at temperatures above 15°C. Neither urediniospores nor mycelia survive temperatures above 32°C. The optimum temperature for urediniospore germination is between 7 and 12°C, with lim its near 0 and 21°C. Disease development is most rapid between 10 and 18°C with intermittent rain or dew.

Septoria tritici Blotch Septoria tritici blotch is one of several leaf spot diseases of wheat occurring in most wheat production areas. It tends to be more severe in wet areas, particularly when the weather is cool and rain is frequent during the vegetative and early reproduc tive growth stages. Mycelium of the fungus proliferates within the apoplast of the wheat leaf, where it establishes a parasitic relationship. Lesions eventually become necrotic. The disease normally does not become severe until after flowering, so para sitism and destruction of photosynthetic area impede grain filling rather than reduce the number of heads or number of grains per head. Shriveled grain results in lower yield and test weight.

Symptoms In winter wheat, lesions appear in early spring on the blades of lower leaves, which emerged the previous autumn. Lesions often appear first on areas of leaves that are in contact with the surface of the soil. Lesions on these seedling leaves are broadly 56

Management Stripe rust can be managed by growing resistant cultivars, the use of fungicide seed treatment, timely application of fungi cides, and appropriate cultural practices, such as late planting, eliminating volunteer plants, and avoiding excessive water and fertilizer. High-temperature, adult-plant resistance, which is non-race-specific and durable, may provide sustainable control of stripe rust. Selected References Chen, X. M. 2005. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Can. J. Plant Pathol. 27:314–337. Chen, X. M., Line, R. F., and Leung, H. 1995. Virulence and poly morphic DNA relationships of Puccinia striiformis f. sp. hordei to other rusts. Phytopathology 85:1335–1342. Chen, X. M., Moore, M., Milus, E. A., Long, D. L., Line, R. F., Marshall, D., and Jackson, L. 2002. Wheat stripe rust epidemics and races of Puccinia striiformis f. sp. tritici in the United States in 2000. Plant Dis. 86:39–46. Coakley, S. M., Line, R. F., and Boyd, W. S. 1983. Regional models for predicting stripe rust on winter wheat in the Pacific Northwest. Phytopathology 73:1382–1385. Line, R. F. 2002. Stripe rust of wheat and barley in North Amer ica: A retrospective historical review. Annu. Rev. Phytopathol. 40:75–118. Mares, D. J. 1979. Light and electron microscope study of the inter action of yellow rust with a susceptible wheat cultivar. Ann. Bot. 43:183–189. Milus, E. A., and Line, R. F. 1986. Number of genes controlling hightemperature, adult-plant resistance to stripe rust in wheat. Phyto pathology 76:93–96. Mulder, J. L., and Booth, C. 1971. Puccinia striiformis. Descriptions of Pathogenic Fungi and Bacteria, no. 291. Commonwealth Myco logical Institute and Association of Applied Biologists, Kew, Sur rey, England. Rapilly, F. 1979. Yellow rust epidemiology. Annu. Rev. Phytopathol. 17:59–73. Stubbs, R. W. 1985. Stripe rust. Pages 61–101 in: The Cereal Rusts. Vol. 2. A. P. Roelfs and W. R. Bushnell, eds. Academic Press, Or lando, Fla.

(Prepared by Xianming Chen)

elliptical with a tan center (Fig. 86) and usually have a dis tinct yellow margin. Pycnidia are readily visible as small, black specks in the necrotic area of the lesion. If the weather remains conducive to infection during stem elongation and flowering, lesions develop on successively higher leaves. Lesions on upper leaf blades tend to be straightsided (Fig. 87), without a distinct chlorotic halo. Lesions may coalesce to kill large areas of leaves or entire leaf blades. Le sions also develop on leaf sheaths. In spring wheat at higher latitudes, the disease may not ap pear until the plants are in the boot stage, and then lesions will form simultaneously on several layers of leaves. When the relative humidity is high but the leaf surface is not actually wet, a curved cirrhus extrudes from the ostiole of the pycnidium (Fig. 88). Cirrhi are easily visible with a hand lens and can often be seen with the unaided eye as coiled, translu cent bands. When rain or dew wets the cirrhi, the gel matrix dissolves quickly. It can be difficult to distinguish Septoria tritici blotch from Stagonospora nodorum blotch, tan spot, and other leaf spots late in the season, when necrosis is extensive. Microscopic ex

Primary infection of winter wheat occurs in the fall, mainly from ascospores produced on residue from the previous sea son’s crop. Germ tubes grow over the leaf surface, at random, and penetrate stomates. Depending on the climate where wheat is grown, these primary infections produce lesions in early win ter or not until the following spring. As the air and soil surface become warmer in the spring, lesions on overwintered leaves mature and produce pycnidia.

Septoria tritici blotch is a polycyclic disease. Rain splashes spores produced on lower leaves, carrying them to upper leaves. Thus, the disease typically shows a vertical gradient, with the amount of leaf area with symptoms being greater on lower leaves. If weather favorable for infection persists through the development of the flag leaf, all leaves eventually become severely blighted. By then the lower leaves have shriveled. Pseudothecia may develop on these lower leaves and contribute ascospores to the pool of secondary inoculum. Hyphae grow intercellularly until the onset of necrosis, about 10 days after infection. By that time, mesophyll cells in the infection site become disorganized and collapse. From about 10 to 14 days after infection, pycnidia develop in substomatal cavities in the lesion. The ostiole of the pycnidium develops be neath a stomatal opening. The minimum latent period is about 11 days when daily temperatures are in the range of 15–25°C but is substantially longer at lower temperatures. Plants inoculated in a greenhouse or growth chamber must remain in a moist chamber for at least 48 h for lesions to de velop. Very few lesions develop when the moist period is only 24 h long. A moist period of 72 h will usually result in more lesions than a 48-h moist period. Leaves need not be wet dur ing the moist period, but the relative humidity must be very high. Rain falling for more than a few consecutive hours is rare in nature. However, infection will occur if a “wet” period (in which the humidity is very high) is broken by a period of lower humidity (50 or 75%) followed by an additional wet period. In nature, if rain falls on two or more days, even though not continuously, the relative humidity may be sufficiently high for at least 48 h to allow infection to occur. This may explain why epidemics develop when there are several periods of rainy

Fig. 86. Young, oblong lesion with black spots (pycnidia) on a leaf with Septoria tritici blotch. (Courtesy W. W. Bockus)

Fig. 88. Cirrhi emerging from the ostioles of pycnidia of Septoria tritici. (Courtesy W. W. Bockus)

Fig. 87. Old, straight-sided lesions with black spots (pycnidia) on a leaf with Septoria tritici blotch. (Courtesy W. W. Bockus)

Fig. 89. Spores released from pycnidia of Septoria tritici. (Cour tesy W. W. Bockus)

amination of necrotic tissue will readily distinguish Septoria tritici blotch from other diseases. A small piece of necrotic tis sue can be placed in water on a microscope slide. The mor phology of the spores that are extruded from the pycnidia will permit reliable identification of the pathogen (Fig. 89).

Causal Organism The pathogen is Mycosphaerella graminicola (Fuckel) J. Schröt., a fungus present in most wheat-producing areas. The anamorph, Septoria tritici Roberge in Desmaz., is more commonly found in living wheat, although the teleomorph may be found on necrotic lower leaves. Pycnidia are 60–200 µm in diameter and form in substomatal chambers with the ostiole beneath the stomate. Conidia are long and slender (20–98 × 1.4–3.8 µm) and multiseptate, with tapered ends (Fig. 89). The fungus is heterothallic. Pseudothecia become laterally compressed, measuring 76–80 × 77–100 µm. Asci are bitunicate and obpyriform (34–41 × 11–13 µm). Each ascus contains eight ascospores, which are hyaline, ellipsoidal (10–15 × 2.5–3 µm), and one-septate, generally with one cell larger than the other.

Disease Cycle

weather that last for more than 1 day. Looked at from the op posite way, the severity of Septoria tritici blotch is inversely related to the number of 2-day periods in which no rain falls during early spring.

Management Resistant cultivars provide control of Septoria tritici blotch. Several major race-specific genes confer a high degree of re sistance to avirulent races. Although this resistance is racespecific, there has been less dramatic loss of effective resistance because of the adaptation of races of the pathogen, as com monly occurs with rusts and powdery mildew. There is also a partial, quantitative resistance. Resistance to Septoria tritici blotch may be obscured in the field by the presence of other leaf spot diseases, particularly Stagonospora nodorum blotch and tan spot, because all three often constitute a disease complex. Fungicides provide effective control if used in a timely man ner. They have the advantage of controlling several diseases simultaneously, but they add to the cost of production of wheat. Application at flag leaf emergence or shortly after is generally most effective, but if a period particularly favorable for infec tion precedes fungicide application by a few days, control may not be satisfactory. Selected References Chungu, C., Gilbert, J., and Townley-Smith, F. 2001. Septoria tritici blotch development as affected by temperature, duration of leaf wetness, inoculum concentration, and host. Plant Dis. 85:430–435. Coakley, S. M., McDaniel, L. R., and Shaner, G. 1985. Model for pre dicting severity of Septoria tritici blotch on winter wheat. Phytopa thology 75:1245–1251. Cunfer, B. M., and Ueng, P. P. 1999. Taxonomy and identification of Septoria and Stagonospora species on small-grain cereals. Annu. Rev. Phytopathol. 37:267–284. Eriksen, L., Shaw, M. W., and Østergård, H. 2001. A model of the effect of pseudothecia on genetic recombination and epidemic de velopment in populations of Mycosphaerella graminicola. Phyto pathology 91:240–248, 519 (erratum). Eyal, Z. 1999. The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. Eur. J. Plant Pathol. 105:629–641. Kema, G. H. J. 1996. Mycosphaerella graminicola on wheat: Genetic variation and histopathology. Ph.D. thesis, Wageningen Agricul tural University, Wageningen, Netherlands. Sanderson, F. R. 1972. A Mycosphaerella species as the ascogenous state of Septoria tritici Rob. and Desm. N.Z. J. Bot. 10:707–710. Scott, P. R., Sanderson, F. R., and Benedikz, P. W. 1988. Occurrence of Mycosphaerella graminicola, teleomorph of Septoria tritici, on wheat debris in the UK. Plant Pathol. 37:285–290. Shaw, M. W. 1991. Interacting effects of interrupted humid periods and light on infection of wheat leaves by Mycosphaerella gramini cola (Septoria tritici). Plant Pathol. 40:595–607. Shaw, M. W., and Royle, D. J. 1989. Airborne inoculum as a major source of Septoria tritici (Mycosphaerella graminicola) infections in winter wheat crops in the UK. Plant Pathol. 38:35–43.

Infection early in the growing season, after prolonged cool, wet, overcast weather or snow cover, results in spring blight (also called winter-k ill), with symptoms resembling those of snow mold. The disease can severely reduce stands and yields of winter cereals. With the increased control of eyespot (strawbreaker foot rot) in Europe and the United States, sharp eyespot has become more common. Spring blight has been a primary reason for the abandonment of 10–40% of the winter wheat planted in the U.S. Midwest in some years.

Symptoms Symptoms of sharp eyespot, like those of eyespot, usually appear first on an outer leaf sheath near the base of the plant. A circular or elliptical, light brown area circumscribed by a thin, necrotic, dark brown border develops on the leaf sheath. Af fected leaf sheaths may rot, and the rotted tissues leave a char acteristic hole (rather than a fibrous net, as with eyespot), but generally the leaf sheaths remain intact. Several lesions, ranging up to 1 cm in diameter, may occur on the lower leaf sheaths of the same plant and, in contrast to eyespot lesions, can occur up to 30 cm above the soil line. Severe infection causes the death of late tillers or seedling blight of late-seeded winter wheat, but most main culms of infected plants survive to maturity. Lesions on culms are light brown or straw-colored with a sharply defined, dark brown border (Fig. 90). The lesions may resemble those of eyespot but are more superficial, less lensshaped, and more sharply delineated. On maturing culms, the area beneath a lesion is often covered with abundant ash white mycelium, in which small, light brown sclerotia are sometimes present. Severe infection causes a loss of tillers, premature rip ening, and lodging. The culms of lodged plants often bend at the second or third internode as they attempt to right them selves. The sharp eyespot pathogen is less able to mechanically weaken infected culms than the eyespot pathogens. Spring blight lesions are initially small, water-soaked, ne crotic spots, which then expand to rot carbohydrate-depleted leaves (Fig. 91). These initial symptoms are similar to those of snow mold. The disease is sometimes referred to as winter-k ill, but it is independent of the temperature-hardiness of a cultivar. Under optimal conditions for disease development, all foliage may be killed, but some plants may recover as temperatures rise and photosynthesis resumes, unless the crown tissue has been completely destroyed. Late-seeded winter wheat plants that fail to develop adequate crown carbohydrate reserves for prolonged respiration during the winter are especially suscepti ble. Losses due to spring blight, as in the case of sharp eyespot, are generally due to the death of tillers and thinner stands, but the disease may make entire fields unprofitable to harvest. The sharp eyespot pathogen is a common rhizosphere colo nizer, but it rarely causes significant damage to root systems, and it has been promoted as a biological control for other soil borne root pathogens, including Rhizoctonia solani.

(Prepared by Gregory Shaner)

Sharp Eyespot Sharp eyespot is a disease of wheat, barley, and rye in China, Europe, North America, and most other temperate wheatgrowing regions. Strains of the sharp eyespot pathogen also cause yellow patch of turfgrass and spring blight of winter wheat. Severe sharp eyespot in wheat causes the death of late tillers, premature ripening (formation of whiteheads), and lodging. Sharp eyespot lesions are often superficial and inconsequential when spring weather is optimal for plant growth, and thus con trol measures are generally not justified. 58

Fig. 90. Sharp eyespot lesion on a stem. (Courtesy D. M. Huber)

Causal Organism Rhizoctonia cerealis E. P. Hoeven, a widespread soilborne plant pathogen, causes sharp eyespot. It forms no spores and produces characteristically binucleate mycelium (Fig. 92). Its hyphae are white to gray brown and 4–15 µm wide, and they tend to branch at right angles (see Rhizoctonia Root Rot). The teleomorph of R. cerealis is the basidiomycete Ceratobasidium cereale D. Murray & L. L. Burpee. It is rare in nature and is not observed in association with sharp eyespot symptoms. R. cerealis mycelium grows on many media and forms abun dant sclerotia. The sclerotia are irregular in shape and light to dark brown, and they lack a distinct rind. They often occur under lesions on wheat leaf sheaths.

Disease Cycle Culm infection originates from soilborne mycelium or scle rotia. Infection depends on cool, moist conditions near the base of the plant. After invading seedling leaf sheaths, the patho gen spreads by mycelial growth on and within the plant during the early growing season. Spring blight starts with infection

of leaf tips or leaves near the soil or by soilborne inoculum splashed onto them during prolonged cool, wet, or heavily over cast weather or after prolonged snow cover in late winter and early spring. Sharp eyespot especially affects cereals grown continuously on the same land and is more severe in crops grown in untilled or acidic soils. R. cerealis is difficult to isolate from lesions later in the season. Sclerotia develop during the summer and are a principal source of inoculum in residue returned to the soil after harvest. The importance of the teleomorph, C. cereale, in the epide miology of sharp eyespot is unknown.

Management Several wheat cultivars are resistant to sharp eyespot, and various degrees of tolerance of spring blight are known. Toler ance of spring blight is not related to winterhardiness. Early autumn seeding of winter wheat results in less disease but may also favor take-all. Late seeding of spring-sown wheat may avoid seedling development under environmental condi tions conducive to severe disease. Manuring and fertilization to ensure that sufficient zinc is available to enable carbohydrate storage in crown tissues dur ing a long winter period increases tolerance of spring blight and sharp eyespot. Early autumn seeding is associated with mycor rhizal infection and high tissue levels of zinc conducive to car bohydrate storage in crown tissues. The application of zinc to foliage after seedling emergence has no effect on the incidence or severity of sharp eyespot. Rotation with a legume or other nonhost crops is beneficial. No effective and economical chemical controls are available. Selected References

Fig. 91. Wheat killed and damaged by spring blight after the weather has become drier and warmer in the spring. (Courtesy D. M. Huber)

Fig. 92. Binucleate mycelium of Rhizoctonia cerealis, the cause of sharp eyespot and spring blight. (Courtesy R. W. Smiley and J. L. Dale, reprinted from R. W. Smiley, P. H. Dernoeden, and B. B. Clarke, 2005, Compendium of Turfgrass Diseases, 3rd ed., American Phytopathological Society, St. Paul, Minn.)

Clarkson, J. D. S., and Cook, R. J. 1983. Effect of sharp eyespot (Rhizoctonia cerealis) on yield loss in winter wheat. Plant Pathol. 32:421–428. Clarkson, J. D. S., and Griffin, M. J. 1977. Sclerotia of Rhizoctonia solani in wheat stems with sharp eyespot. Plant Pathol. 26:98. Hollins, T. W., and Scott, P. R. 1985. Differences between wheat cul tivars in resistance to sharp eyespot caused by Rhizoctonia cere alis. Tests of Agrochemicals and Cultivars, No. 6. Ann. Appl. Biol. 106(Suppl.):166–167. Huber, D. M. 1981. Yield and quality of soft red winter wheat infected with Rhizoctonia spring blight. (Abstr.) Phytopathology 71:227. Huber, D. M., Baird, R. E., and McCay-Buis, T. S. 1992. Environmen tal conditions associated with Rhizoctonia “winter-k ill” of wheat in Indiana. (Abstr.) Phytopathology 82:1114. Huber, D. M., McCay-Buis, T. S., Riegel, C., Graham, R. D., and Robinson, N. 1993. Correlation of zinc sufficiency with resistance of wheat to Rhizoctonia winter-k ill. Abstr. 115. Int. Congr. Plant Pathol., 6th. Lipps, P. E., and Herr, L. J. 1982. Etiology of Rhizoctonia cerealis in sharp eyespot of wheat. Phytopathology 72:1574–1577. Murray, D. I. L., and Burpee, L. L. 1984. Ceratobasidium cereale sp. nov., the teleomorph of Rhizoctonia cerealis. Trans. Br. Mycol. Soc. 82:170–172. Ogoshi, A., and Ui, T. 1985. Anastomosis groups of Rhizoctonia so lani and binucleate Rhizoctonia. Pages 57–58 in: Ecology and Man agement of Soilborne Plant Pathogens. C. A. Parker, A. D. Rovira, K. J. Moore, P. T. W. Wong, and J. F. Kollmorgen, eds. American Phytopathological Society, St. Paul, Minn. Richardson, M. J., and Cook, R. J. 1985. Rhizoctonia on small-grain cereals in Great Britain. Pages 63–65 in: Ecology and Manage ment of Soilborne Plant Pathogens. C. A. Parker, A. D. Rovira, K. J. Moore, P. T. W. Wong, and J. F. Kollmorgen, eds. American Phyto pathological Society, St. Paul, Minn.

(Prepared by Don M. Huber)