H. H. Prell· P. R. Day Plant-Fungal Pathogen Interaction Springer-Verlag Berlin Heidelberg GmbH Hermann H. Prell . Peter R. Day Plant-Fungal Pathogen Interaction A Classical and Molecular View With 15 Figures and 12 Tables Springer Professor em. Dr. HERMANN H. PRELL Institut fur Pflanzenpathologie und Pflanzen schutz Universitat Gottingen GrisebachstraBe 6 37077 Gottingen, Germany Professor Dr. PETER DAY Rutgers, The State University of New Jersey Biotechnology Center for Agriculture and the Environment Foran Hall, Cook College 59 Dudley Road New Brunswick, NJ 08901-8520, USA Title of the original German edition. Hermann H. Prell: Interaktionen von Pflanzen und phytopathogenen Pilzen. ISBN 3-437-35028-5; © Gustav Fischer Verlag, Jena 1996 Cover illustration: Telium with teieutospores of Puccinia graminis on a leaf. - Institute for Plant Pathology and Plant Protection, University of Gottingen, Dr. Helga Nirenberg. ISBN 978-3-642-08601-4 ISBN 978-3-662-04412-4 (eBook) DOI 10.1007/978-3-662-04412-4 Die Deutsche Bibliothek - CIP-Einheitsaufnahme Prell, Hermann H.: Plant fungal pathogen interaction: a classical and molecular view / Hermann H. Prell; Peter R. Day. - Heidelberg; New York; Barcelona; Hong Kong; London; Milan; Paris; Singapore; Tokyo: Springer, 2000 Einheitssacht.: Interaktionen von Pflanzen und phytopathogenen Pilzen <engl.> This work is subject to copyright. All rights reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcast- ing, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. © Springer-Verlag Berlin Heidelberg 2001 Originally published by Springer-Verlag Berlin Heidelberg New York in 2001. Softcover reprint of the hardcover 1st edition 2001 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant pro- tective laws and regulations and therefore free for general use. Cover design: Design & Production, Heidelberg Typesetting: Mitterweger & Partner GmbH, Plankstadt SPIN 10569959 3113130 - 5 4 3 2 1 0 - Printed on acid-free paper Preface This book has been written for scientists and graduate students in plant pathol- ogy, biology, biochemistry, genetics and molecular genetics, for practitioners in plant protection and plant breeding, and for the interested layman. We have tried to produce a concise survey of the diversity of interactions between plants and phytopathogenic fungi. Our main objective has been to help the reader to com- prehend the complexity of these interactions and the many different approaches used to analyse them. Some recent developments are also presented to demon- strate the close connections between plant pathology and basic research in biol- ogy. Within the last 20 years many exhaustive reviews have been published, that deal with particular aspects of plant-pathogen interactions. However, it is diffi- cult to obtain from them a coherent picture comprising all or most of their im- portant features. Also the technical terms employed in the literature may be un- familiar to many readers and definitions are often difficult to find. This book provides definitions, attempts to bring together the recent literature on host- parasite interactions, and discusses the range of experimental approaches that have been used to explore them. We have relied fairly heavily on the review papers listed at the end of each chapter. More recent and particularly interesting results from original papers are also cited in the text and the references given at the ends of chapters under "relevant papers". Since we wished to keep relevant references together at the end of each chapter some references are repeated in other chapters. The first edition of this book appeared in German in the Fischer-Verlag. (Prell, Hermann, H.: Interaktionen von Pflanzen und phytopathogenen Pilzen: Paras i- tierung, und Resistenz, Genetik und molekulare Phytopathologie. - Jena; Stutt- gart: G. Fischer, 1996). This English translation of the German book is a revised and updated version of the German publication. Translation and improvements of this second edition were prepared by both authors, H.P. and P.D .. Both appreciate the revision of the first English draft of H.P. carried out by the Springer-Verlag and the publisher'S patience in waiting for the complete manuscript. - H.P. appreciates very much the support given by Dr. B. Koop- mann, Inst. for Plant Pathology and Plant Protection, University G6ttingen, for some literature searches and for assistance in delivering, receiving and converting emails, and the efforts by Mr. W. Eisenberg, M.A., Institute of VI Preface Subtropical Agriculture, University G6ttingen, for help in preparing figures on the PC. H.P. is especially indebted to his wife for her many helpful and elucidating discussions, and for her patience and encouragement during the years when writ- ing the book. G6ttingen and New Brunswick, Hermann H. Prell December 2000 Peter R. Day Contents 1 Introduction .......................................... 1 2 Recognition, the First Step in Interaction Between Plant and Pathogen ......................................... 9 3 Activities of Phytopathogenic Fungi when Colonizing Their Host Plants ...................................... 17 3.1 Putative Evolution of Fungal Phytopathogenicity ........ 25 4 Taxonomy of Phytopathogenic Fungi . . . . . . . . . . . . . . . . . . . . . . .. 29 5 Plant Defense Strategies Against Phytopathogenic Fungi ......... 31 6 Basic Resistance: The Absence of Parasitism of Non-Host Plants by Phytopathogenic Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 41 6.1 The Origins of Basic Resistance ..................... 48 7 Basic Compatibility: The Colonization of Host Plants by Pathogenic Fungi .................................... 51 8 Phytotoxins: The Weapons of Necrotrophic Phytopathogenic Fungi .................................. 57 8.1 Non-Host-Selective Toxins .. . . . . . . . . . . . . . . . . . . . . . .. 58 8.2 Host-Selective Toxins. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 60 8.3 Genetics of Toxin Biosynthesis and Toxin Resistance ..... 65 9 Host Plant Resistance: Cultivar- or Parasite-Specific Resistance .... 71 9.1 Race-Specific, or Vertical, Resistance ................. 75 9.1.1 The "Gene-for-Gene" Hypothesis .................... 79 9.1.2 The Properties of Race-Specific Resistance ............. 99 9.1.3 Hypothetical Mechanisms Responsible for Triggering Race-Specific Resistance ........................... 102 9.1.3.1 The Elicitor-Receptor Model ....................... 103 9.1.3.2 The Dimer Model ............................... 118 VIII Contents 9.1.3.3 The Ion Channel Defense Model .................... 120 9.1.3.4 The Suppresser-Receptor Model ..................... 128 9.1.4 Plant Genes Conditioning Receptor Function ........... 129 9.1.5 Coevolution of Resistant Host Plants and Their Specific Virulent Pathogens in Agriculture ............. 151 9.1.6 Preservation of Avr Genes in Pathogen Populations and Their Possible Function ........................ 157 9.1.7 The Evolution of Race-Specific Resistance in Natural Ecosystems ............................ 161 9.1.8 Deviations from Strict Gene-for-Gene Relationships ...... 165 9.2 Race-Non-Specific, or Horizontal, Resistance ........... 174 10 Host Plant Tolerance .................................... 183 11 Induced Resistance ..................................... 185 12 Evolution of Plant-Pathogen Interaction - Its Influence on Breeding of Disease Resistant Crops in Agriculture . . . . . . . . . . . 195 13 Glossary: Explanation of some Terms Utilized in Biology and Plant Pathology .................................... 197 Subject Index ......................................... 205 List of Tables Table 1 Comparison of physiological properties of necrotrophs, biotrophs, and their host plants .................... 20 Table 2 Comparison of basic and host resistence .... . . . . . . . . .. 32 Table 3 Concerted action of pathogenicity genes .............. 52 Table 4 Quadratic check for toxin sensitivity .. . . . . . . . . . . . . . .. 62 Table 5 Comparison of host-selective toxins of Cochliobolus spp. .. 67 Table 6 Quadratic check for race-specific resistance . . . . . . . . . . .. 86 Table 7 Independent interaction of corresponding gene pairs for race specific resistance and epistasis of incompatibility over compatibility. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 91 Table 8 Dominance of genes determining race-specific resistance and avirulence ................................. 93 Table 9 Reciprocal check demonstrating independent expression of race specific resistance . . . . . . . . . . . . . . . . . . . . . . . . .. 94 Table 10 Quadratic check demonstrating dominance, epistasis, and independence among different gene pairs . . . . . . . . .. 96 Table 11 Constant ranking of race-non-specific (horizontal) and differential ranking of race-specific (vertical) resistant cultivars ...................................... 176 Table 12 Comparison of race-non-specific (horizontal) and race-non -specific (vertical) resistance ................ 177 list of Figures Figure 1 Basic incompatibility. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 46 Figure 2 Basic compatibility ............................... 53 Figure 3 Melampsora lini: Life cycle ........................ 81 Figure 4a,b Gene-for-gene recognition. . . . . . . . . . . . . . . . . . . . . . . .. 89 Figure 5 Inducible plant defense reactions ................... 101 Figure 6 Elicitor-receptor model ........................... 104 Figure 7 Dimer model .................................. 119 Figure 8 Ion channel defense model ........................ 122 Figure 9 Pathogen-induced signal cascades ................... 126 Figure 10 Receptor proteins for race-specific resistance ........... 145 Figure 11 Coevolution of race-specific resistance and specific virulence 153 Figure 12 Gene-for-gene pathway ........................... 167 Figure 13a,b Gene-for-gene pathway with dominant suppressor ....... 169 Figure 14 Gene-for-gene pathway with recessive suppressor ........ 170 Figure 15 Connection between race-specific resistance and systemic acquired resistance (SAR) ......................... 189