Plant Virology Second Edition R. E. F. MATTHEWS Department of Cell Biology The University of Auckland Auckland, New Zealand ACADEMIC PRESS A Subsidiary of Harcourt Brace Jovanovich, Publishers New York London Toronto Sydney San Francisco COPYRIGHT © 1981, BY ACADEMIC PRESS, 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. ACADEMIC PRESS, INC. 111 Fifth Avenue, New York, New York 10003 United Kingdom Edition published by ACADEMIC PRESS, INC. (LONDON) LTD. 24/28 Oval Road, London NW1 7DX Library of Congress Cataloging in Publication Data Matthews, R. E. F. (Richard Ellis Ford), Date. Plant virology. Bibliography: p. Includes index. 1. Virus diseases of plants. 2. Plant viruses. I. Title. SB736.M37 1981 632'.8 81-1149 ISBN 0-12-480560-4 PRINTED IN THE UNITED STATES OF AMERICA 81 82 83 84 9 8 7 6 5 4 3 2 1 Preface There have been substantial developments in many areas of plant virology since the first edition was published. Advances have been made in all branches of the subject, but these have been most far reaching with respect to the structure of viruses and of their components, and in our understanding of how viral genomes are organized and how viruses replicate in cells. Significant develop­ ments have also occurred in our understanding of how viruses are transmitted by invertebrates and in the application of control measures for specific diseases. The taxonomy of viruses has advanced significantly, and there are now 25 internationally approved families and groups of plant viruses. All these developments have required that most sections be entirely rewritten. The extent of the changes can be gauged from the fact that 1881 of the 2667 references in the bibliography did not appear in the first edition. As with the first edition, this volume is written to cover all aspects of the field, and is intended primarily for graduate students in plant pathology, plant virology, general virology, and microbiology, and for teachers and research workers in these fields. It should also prove useful to some people in related disciplines—molecular biologists, biochemists, plant physiologists, and entomologists. Preface to First Edition As in many other areas of biology, there has been rapid growth over the past few years in our knowledge of plant viruses and the diseases they cause. Thus there was a substantial need for a new text covering all aspects of the subject. This book was written primarily for graduate students in plant pa­ thology, plant virology, general virology, and microbiology and for teach­ ers and research workers in these fields. I hope that it will also prove useful as a reference work for those in disciplines related to plant virology—molecular biologists, biochemists, plant physiologists, and en­ tomologists. I have attempted to cover, to some degree at least, all aspects of the subject, a difficult task in view of the wide range of disciplines involved. There is a brief historical account of the development of plant virology in the first chapter, but the general approach is not a historical one. Those interested will find this aspect well covered in earlier texts. Topics dealt with include the structure of viruses and viral compo­ nents; the replication of viruses; their macroscopic, cytological, and bio­ chemical effects on the host plant; the nature of virus mutation; relationships with invertebrate vectors; and a discussion of ecology and control. Throughout I have attempted to indicate how progress in any particular area has been dependent on the development and applica­ tion of appropriate experimental methods. Specific details of method­ ology have not been given since these are available elsewhere. The subject has grown to the extent that it would be impossible to quote all papers on any given topic in a book of this size. In general I have referred to important early papers and to the most important or most suitably illustrative recent papers. From these the reader should be able to gain rapid access to the literature on any relevant topic. In a text on a subject that draws on a wide range of scientific disci­ plines, I believe that illustrative material is most important, particularly for students or newcomers to the field. For this reason I have gone to some pains, and have had the support of many colleagues, in selecting graphs and photographs to highlight and supplement the text. xiii xiv Preface to First Edition In certain areas, particularly the molecular biology of viral replica­ tion, our knowledge of plant viruses lags behind that of animal and bacterial viruses. I have therefore drawn on information about these viruses where it seemed appropriate to set the stage for considering more fragmentary facts about plant viruses. One recent development that created problems was the discovery that many diseases previously thought to be caused by unstable viruses are very probably caused by mycoplasma-like organisms. Although, in gen­ eral, I have not included diseases in which the probability of a myco­ plasma-like organism being involved is high, one chapter on agents causing virus-like diseases is devoted mainly to a consideration of such organisms in plant disease. Other recent work of considerable general interest has resulted in the discovery that several plant viruses have their genetic material divided up between two or more particles. Thus I have devoted a chapter to the consideration of defective virus particles, dependent viruses, and multiparticle viruses. I have followed the Commonwealth Mycological Institute list of "Plant Virus Names" (Martyn, 1968). I have not attempted to deal with indi­ vidual viruses or virus diseases in any systematic or comprehensive way, so that the list of "Plant Virus Names" should be regarded as a valuable companion book for the present text, especially for those inter­ ested in the tremendous amount of literature on the plant pathological aspects of virus diseases. In the last chapter I have outlined the various viewpoints regarding nomenclature and classification. Since, from the long-term point of view, at least, classification of viruses must take origins into consideration, some space is given to speculation on the origins of viruses. Acknowledgments I am much indebted to the following colleagues who critically read and commented upon sections of the manuscript: A. R. Bellamy, P. J. G. Butler, R. I. B. Francki, P. R. Fry, M. Hollings, A. Klug, H. E. D. Lane, J. Marbrook, L. van Vloten-Doting, and A. van Zaayen. I also wish to thank the colleagues in many countries who gave information by corre­ spondence, who sent me manuscripts prior to publication, and who pro­ vided photographs for illustrations. Photographs are acknowledged in­ dividually in the text. I also thank editors and publishers for permission to reproduce figures and photographs. Many of the graphs and line drawings were drawn or redrawn by Jeannette Keeling. I thank her for these, and also for the many other ways in which she assisted with the preparation of the text. Finally I wish to thank Pat Glenn and Irene Henderson for typing the manuscript. XV List of Abbreviations Virus name abbreviations as used throughout the text. AMV Alfalfa mosaic virus BMV Brome mosaic virus BYDV Barley yellow dwarf virus BYV Beet yellows virus CaMV Cauliflower mosaic virus CMV Cucumber mosaic virus CPMV Cowpea mosaic virus FDV Fijidisease virus LNYV Lettuce necrotic yellows virus MCDV Maize chlorotic dwarf virus PEMV Pea enation mosaic virus PVX Potato virus X PVY Potato virus Y SBMV Southern bean mosaic virus STNV Satellite tobacco necrosis virus TBSV Tomato bushy stunt virus TMV Tobacco mosaic virus TNV Tobacco necrosis virus TRSV Tobacco ringspot virus TRV Tobacco ringspot virus TSV Tobacco streak virus TYMV Turnip yellow mosaic virus WTV Wound tumor virus xvii Introduction I. HISTORICAL Although virus diseases in plants were not recognized as distinct from other kinds of infectious disease until about 80 years ago, much earlier pictorial and written records exist that present clear evidence for plant virus infections. In the period from about 1600 to 1660 many paintings or drawings were made of tulips that demonstrate symptoms of virus disease. During this period, blooms featuring such striped patterns were prized as special varieties. One of the earliest written accounts of an unwitting experimental transmission of a virus, is that of Lawrence (1714). He described in detail the transmission of a virus disease of jasmine by grafting. This description was incidental to the main purpose of his experiment which was to prove that sap must flow within plants. The following quotation from Blair (1719) describes the procedure, and demonstrates, rather sadly, that even at this protoscientific stage, experi­ menters were already indulging in arguments about priorities of discovery. The inoculating of a strip'd Bud into a plain stock and the consequence that the Stripe or Variegation shall be seen in a few years after, all over the shrub above and below the graft, is a full demonstration of this Circulation of the Sap. This was first observed by Mr. Wats at Kensington, about 18 years ago: Mr. Fairchild performed it 9 years ago; Mr. Bradly says he observ'd it several years since; though Mr. Lawrence would insinuate as if he had first discovered it. *The experiment perform'd in a Jessamine, is now to be seen in Mr. Fairchild's garden. In July 1717 having a plain Jessamine which mounted pretty high upon the wall, being an old shrub with two large trunks arising from the Root at one Foot distance, where both were covered with Earth. He inoculated a strip'd Bud in one of the Stocks which was four foot high. Last year it put forth several shoots very elegantly strip'd; and this Season, several Stripes and Variegations appeared upon the other Trunk, which is above six Foot high. This not only proves the Ascent and Descent of Sap in the same Trunk, but also that it circulates throughout the whole plant to a great distance. *Lawrence (1914). 1 2 1. Introduction In the latter part of the nineteenth century, the idea that infectious disease was caused by microbes was well established, and filters were available which would not allow the known bacterial pathogens to pass. Mayer (1886) described a disease of tobacco which he called Mosaikkrankheit. He showed that the disease could be transmitted to healthy plants by inoculation with extracts from diseased plants. Iwanowski (1892) showed that sap from tobacco plants displaying the disease described by Meyer was still infective after it had been passed through a bacteria- proof filter candle. This work did not attract much attention until it was repeated by Beijerinck (1898). Baur (1904) showed that the infectious variegation of Abutilon could be transmitted by grafting, but not by mechanical inoculation. Beijerinck and Baur used the term virus in de­ scribing the causative agents of these diseases to contrast them with bac­ teria. The term virus had been used as more or less synonymous with bacteria by earlier workers. As more diseases of this sort were discovered the unknown causative agents came to be called "filterable viruses." Between 1900 and 1935, many plant diseases thought to be due to filterable viruses were described, but considerable confusion arose be­ cause adequate methods for distinguishing one virus from another had not yet been developed. One important step forward was the recognition that some viruses could be transmitted from plant to plant by insects. For example, Smith and Boncquet (1915) confirmed earlier suggestions that sugar beet curly top disease could be transmitted by the leafhopper Eutettix tenella (Baker), and showed that a single insect from an infected plant could induce the disease in a healthy one by only 5 minutes feed­ ing. However, they did not at that time put forward the view that sugar beet curly top was due to a virus. The original criterion of a virus was an infectious entity that could pass through a filter with a pore size small enough to hold back all known cellular agents of disease. However, diseases were soon found that had virus-like symptoms not associated with any pathogen visible in the light microscope, but which could not be transmitted by mechanical inocula­ tion. With such diseases, the criterion of filterability could not be applied. The infectious nature was established by graft transmission and sometimes by insect vectors. Thus it came about that certain diseases of the yellows and witches'-broom type, such as aster yellows, came to be considered as due to viruses on quite inadequate grounds. Many such diseases are now known to be caused by mycoplasmas and spiroplasmas. During most of the period between 1900 and 1935, attention was focused on description of diseases, both macroscopic symptoms and cytological abnormalities as revealed by light microscopy, and on the host ranges and methods of transmission of the disease agents. Rather I. Historical 3 ineffective attempts were made to refine filtration methods in order to define the size of viruses more closely. These were almost the only as­ pects of virus disease that could be studied with the techniques that were available. The influence of various physical and chemical agents on virus infectivity was investigated, but methods for the assay of infective mate­ rial were primitive. Holmes (1929) showed that the local lesions pro­ duced in some hosts following mechanical inoculation could be used for the rapid quantitative assay of infective virus. This technique enabled properties of viruses to be studied much more readily and paved the way for the isolation and purification of viruses a few years later. Until about 1930, there was serious confusion by most workers be­ tween the diseases produced by viruses and the viruses themselves. This was not surprising, since virtually nothing was known about the viruses except that they were very small. Smith (1931) made an important con­ tribution that helped to clarify this situation. Working with virus diseases in potato he realized the necessity of using plant indicators—plant species other than potato, which would react differently to different viruses present in potatoes. Using several different and novel biological methods to separate the viruses, he was able to show that many potato virus diseases were caused by a combination of two viruses with different properties, which he named X and Y. Virus X was not transmitted by the aphid Myzus persicae (Sulz.), while virus Y was. In this way, he obtained virus Y free of virus X. Both viruses could be transmitted by needle inoculation, but Smith found that certain solanaceous plants were resis­ tant to virus Y. For example, by needle inoculation of the mixture to Datura stramonium, he was able to obtain virus X free of virus Y. Fur­ thermore, Smith observed that virus X from different sources fluctuated markedly in the severity of symptoms it produced in various hosts. To quote from Smith (1931), "There are two factors, therefore, which have given rise to the confusion which exists at the present time with regard to potato mosaic diseases. The first is the dual nature, hitherto unsus­ pected, of so many of the potato virus diseases of the mosaic group, and the second is the fluctuation in virulence exhibited by one constitutent, i.e., X, of these diseases." Another discovery that was to become important was Beale's (1928) recognition that plants infected with tobacco mosaic contained a specific antigen. Gratia (1933), showed that plants infected with different viruses contained different specific antigens. Chester (1935, 1936) showed that different strains of tobacco mosaic virus (TMV) and potato virus X could be distinguished serologically. He also showed that serological methods could be used to obtain a rough estimate of virus concentration. Since Fukushi (1940) first showed that rice dwarf virus could be