F i f t h E d i t i o n PLANT PATHOLOGY F i f t h E d i t i o n PLANT PATHOLOGY GEORGE N. AGRIOS Department of Plant Pathology University of Florida Amsterdam • Boston • Heidelberg • London • New York • Oxford Paris • San Diego • San Francisco • Singapore • Sydney • Tokyo Publisher Dana Dreibelbis Associate Acquisitions Editor Kelly D. Sonnack Project Manager Troy Lilly Marketing Manager Linda Beattie Cover Design Eric DeCicco Composition SNP Best-set Typesetter Ltd., Hong Kong Cover Printer RR Donnelley & Sons Company Interior Printer RR Donnelley & Sons Company Elsevier Academic Press 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, California 92101-4495, USA 84 Theobald’s Road, London WC1X 8RR, UK This book is printed on acid-free paper. Copyright © 2005, 1997, 1988, 1978, 1969 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone: (+44) 1865 843830, fax: (+44) 1865 853333, e-mail: [email protected]. You may also complete your request on-line via the Elsevier homepage (http://elsevier.com), by selecting “Customer Support” and then “Obtaining Permissions.” Library of Congress Cataloging-in-Publication Data Agrios, George N., 1936– Plant pathology / George Agrios.—5th ed. p. cm. Includes bibliographical references and index. ISBN 0-12-044565-4 (hardcover: alk. paper) 1. Plant diseases. I. Title. SB731.A35 2004 571.9¢2—dc22 2004011924 British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library For all information on all Elsevier Academic Press Publications visit our Web site at www.books.elsevier.com Printed in the United States of America 04 05 06 07 08 09 9 8 7 6 5 4 3 2 1 This, the 5th and probably the last edition of Plant Pathology by me, is dedicated: To the memory of my parents, Nikolas and Olga, who, in spite of their limited education, sacrificed everything to give me the most and best education possible. To the memory of Dr. Walter F. Buchholtz, my major professor at Iowa State University, who challenged me before I had even taught my first lecture to “write my own textbook on Plant Pathology”. To my sisters, Dimitra and Evangelia, who have been there for me forever and who also sacrificed some of their interests for my benefit. To my wife, Annette, whose love and support have been the most precious things to me throughout our life together, and who helped me in many facets of preparation of this and of previous editions of Plant Pathology. To my daughters-in-law, Betsy and Vivynne, who, by joining our family, added beauty, love, enjoyment, and four wonderful grandchildren. Finally, to Mark and Maximos, our youngest grandchildren, who, someday, when they read their names in the book, may be reassured of “Granpa’s” love for them, and may feel proud of their grandfather. C o n t e n t s Preface xxi The Expanding Role of Fungi as Causes of Plant Photo credits xxiii Disease 21 About the Author xxvi The Discovery of the Other Causes of Infectious Diseases 23 part one Nematodes 23; Protozoan Myxomycetes 24; Bacteria 24; Viruses Protozoa 25; Mollicutes 26; Viroids 26; Serious Plant GENERAL ASPECTS Diseases of Unknown Etiology 26; Koch’s Postulates 26; Viruses, Viroids, and Prions 27 Losses Caused by Plant Diseases 29 chapter one Plant diseases reduce the quantity and quality of plant produce 29 INTRODUCTION White, Downey, and Dry Vineyards—Bring on the Prologue: The Issues 4 Bordeaux! 30 Plants and Disease 4 Plant diseases may limit the kinds of plants and The Concept of Disease in Plants 5 industries in an area 32 Types of Plant Diseases 7 Familiar trees in the landscape: going, going, gone History of Plant Pathology and Early (Box) 32 Chestnuts, Elms, and Coconut Palm Trees—Where have Significant Plant Diseases 8 they gone? 32–35 Introduction 8 Plant diseases may make plants poisonous to Plant Diseases as the Wrath of Gods—Theophrastus humans and animals 37 (Box) 9; Mistletoe Recognized as the First Plant Ergot, Ergotism, and LSD: a Bad Combination (Box) 37; Pathogen (Box) 14; Plant Diseases as the Result of Mycotoxins and Mycotoxicoses (Box) 39 Spontaneous Generation (Box) 16; Biology and Plant Pathology in Early Renaissance (Box) 16; Plant diseases may cause financial losses 41 Potato Blight—Deadly Mix of Ignorance and Politics The Insect—Pathogen Connection: Multifaceted and (Box) 19 Important (Box) 42 vii viii CONTENTS Plant Pathology in the 20th Century 45 Identification of a Preciously Unknown Disease: Early Developments 45 Koch’s Postulates 74 The Descriptive Phase 45; The Experimental Phase 46; The Etiological Phase 46; The Search chapter two for Control of Plant Diseases 46 The Main Areas of Progress 47 PARASITISM AND DISEASE Chemical Control of Plant Diseases 47; Appearance DEVELOPMENT of Pathogen Races Resistant to Bactericides and Parasitism and Pathogenicity 77 Fungicides 48; Public Concern about Chemical Pesticides 48; Alternative Controls for Plant Host Range of Pathogens 78 Diseases 49; Interest in the Mechanisms by Which Development of Disease in Plants 79 Pathogens Cause Disease 50; The Concept of Stages in the Development of Disease: Genetic Inheritance of Resistance and Pathogenicity 52; The Disease Cycle 80 Epidemiology of Plant Disease Comes of Age 53 Plant Pathology Today and Future Inoculation 80 Inoculation 80; Types of Inoculum 80; Sources of Directions 54 Inoculum 80; Landing or Arrival of Inoculum 81 Molecular Plant Pathology 54 Prepenetration Phenomena 82 Aspects of Applied Plant Pathology 56 Attachment of Pathogen to Host 82; Spore Plant Biotechnology—The Promise and the Objections Germination and Perception of the Host Surface 82; (Box) 56; Food Safety (Box) 58; Bioterrorism, Appressorium Formation and Maturation 85; Agroterrorism, Biological Warfare, etc. Who, What, Recognition between Host and Pathogen 86; Why (Box) 59 Germination of Spores and Seeds 86; Hatching of Worldwide Development of Plant Pathology as Nematode Eggs 87 a Profession 60 Penetration 87 International Centers for Agricultural Research 60; Direct Penetration through Intact Plant Surfaces 87; Trends in Teaching and Training 61; Plant Disease Penetration through Wounds 88; Penetration Clinics 62; The Practice and Practitioners of Plant through Natural Openings 88 Pathology 63; Certification of Professional Plant Infection 89 Pathologists 63; Plant Pathology as a Part of Plant Infection 89; Invasion 91; Growth and Medicine; the Doctor of Plant Medicine Program Reproduction of the Pathogen (Colonization) 91 (Box) 64 Dissemination of the Pathogen 96 Plant Pathology’s Contribution to Crops Dissemination by Air 96; Dissemination by Water 97; and Society 65 Dissemination by Insects, Mites, Nematodes, and Other Some Historical and Present Examples of Losses Vectors 97; Dissemination by Pollen, Seed, Transplants, Budwood, and Nursery Stock 100; Caused by Plant Diseases 65 Dissemination by Humans 100 Plant Diseases and World Crop Production 65 Overwintering and/or Oversummering of Crop Losses to Diseases, Insects and Pathogens 100 Weeds 66 Relationships between Disease Cycles and Pesticides and Plant Diseases 69 Epidemics 102 Basic Procedures in the Diagnosis of Plant Diseases 71 chapter three Pathogen or Environment 71 EFFECTS OF PATHOGENS ON PLANT Infectious Diseases 72 Parasitic Higher Plants 72; Nematodes 72; Fungi PHYSIOLOGICAL FUNCTIONS and Bacteria: Fungi 72; Bacteria and Effects of Pathogens on Photosynthesis 106 Mollicutes 72; Viruses and Viroids 73; More than One Pathogen 73 Effect of Pathogens on Translocation of Water Noninfectious Diseases 73 and Nutrients in the Host Plant 106 CONTENTS ix Interference with Upward Translocation of Water Apparent Resistance 137 and Inorganic Nutrients 106 Disease Escape 137; Tolerance to Disease 139 Genetics of Virulence in Pathogens and of Effect on Absorption of Water by Roots 108 Resistance in Host Plants 139 Effect on Translocation of Water through the Xylem 108 The Nature of Resistance to Disease 142 Effect on Transpiration 108 Pathogenicity Genes in Plant Pathogens 142 Genes Involved in Pathogenesis and Virulence by Interference with the Translocation of Organic Pathogens 142 Nutrients through the Phloem 113 Pathogenicity Genes of Fungi controlling: Effect of Pathogens on Host Plant Production of Infection Structures 144 Respiration 115 Degradation of Cuticle and Cell Wall 144 Respiration of Diseased Plants 117 Secondary Metabolites 145 Effect of Pathogens on Permeability of Cell Fungal Toxins 146 Membranes 118 Pathogenicity Signaling Systems 146 Effects of Pathogens on Transcription and Pathogenicity Genes in Plant Pathogenic Translation 118 Bacteria 146 Effect on Transcription 119; Effect on Translation 119 Bacterial Adhesion to Plant Surfaces 146 Effect of Pathogens on Plant Growth 119 Secretion Systems 147 Effect of Pathogens on Plant Enzymes that Degrade Cell Walls 147 Reproduction 121 Bacterial Toxins as Pathogenicity Factors 148 Extracellular Polysaccharides as Pathogenicity Factors 148 chapter four Bacterial Regulatory Systems and GENETICS OF PLANT DISEASE Networks 148 Introduction 125 Sensing Plant Signaling Components 149 Genes and Disease 126 Other Bacterial Pathogenicity Factors 149 Variability in Organisms 128 Pathogenicity Genes in Plant Viruses 149 Mechanisms of Variability 128 Functions Associated with the Coat Protein 149 General Mechanisms: Mutation 129; Viral Pathogenicity Genes 150 Recombination 129; Gene and Genotype Flow Nematode Pathogenicity Genes 150 among Plant Pathogens 130; Population Genetics, Genetics of Resistance through the Hypersensitive Genetic Drift, and Selection 130; Life Cycles — Reproduction — Mating Systems — Out- Response 151 crossing 131; Pathogen Fitness 131; Specialized Pathogen-Derived Elicitors of Defense Responses in Mechanisms of Variability in Pathogens 131; Plants 151; Avirulence (avr) Genes: One of the Sexual-like Processes in Fungi Heterokaryosis 131; Elicitors of Plant Defense Responses 151; Parasexualism 132; Vegetative Characteristics of avr Gene-Coded Proteins 153; Incompatibility 132; Heteroploidy 132; Their Structure and Function Role of avrGenes in Sexual-like Processes in Bacteria and Horizontal Pathogenicity and Virulence 154; hrpGenes and the Gene Transfer 132; Genetic Recombination in Type III Secretion System 155 Viruses 133; Loss of Pathogen Virulence in Resistance (R) Genes of Plants 155 Culture 133 Examples of R Genes 156 Stages of Variation in Pathogens 134 How Do R Genes Confer Resistance? 157 Types of Plant Resistance to Pathogens 134 Evolution of R Genes 157 True Resistance: Partial, Quantitative, Polygenic, or Other Plant Genes for Resistance to Horizontal Resistance—R-Gene Resistance, Monogenic, or Vertical Resistance 136 Disease 158