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SECTIONI INTRODUCTION TO PLANT VIRUSES This page intentionally left blank CHAPTER 1 What Is a Virus? This chapter discusses broad aspects of virology and highlights how plant viruses have led the subject of virology in many aspects. OUTLINE I. Introduction 3 V. Viruses of Other Kingdoms 20 II. History 3 VI. Summary 21 III. Definition of a Virus 9 IV. Classification and Nomenclature of Viruses 13 I. INTRODUCTION they do to food supplies has a significant indi- rect effect. The study of plant viruses has led Plant viruses are widespread and economi- the overall understanding of viruses in many cally important plant pathogens. Virtually all aspects. plants that humans grow for food, feed, and fiber are affected by at least one virus. It is the viruses of cultivated crops that have been most II. HISTORY studied because of the financial implications of the losses they incur. However, it is also impor- Although many early written and pictorial tant to recognise that many “wild” plants are records of diseases caused by plant viruses also hosts to viruses. Although plant viruses are available, they are do not go back as far as do not have an immediate impact on humans records of human viruses. The earliest known to the extent that human viruses do, the damage written record of what was very likely a plant Comparative Plant Virology, Second Edition 3 Copyright # 2009, Elsevier Inc. All rights reserved. 4 1. WHAT IS A VIRUS? virus disease is a Japanese poem that was writ- determining exactly what a virus was. In the latter ten by the Empress Koken in A.D. 752 and part of the nineteenth century, the idea that infec- translated by T. Inouye: tious disease was caused by microbes was well established, and filters were available that would In this village not allow the known bacterial pathogens to pass It looks as if frosting continuously through. In 1886, Mayer (see Figure 1.2A) For, the plant I saw In the field of summer described a disease of tobacco that he called The colour of the leaves were yellowing Mosaikkrankheit , which is now known to be caused by the Tobacco mosaic virus (TMV). Mayer demon- The plant, which has since been identified as strated that the disease could be transmitted to Eupatorium lindleyanum, has been found to be healthy plants by inoculation with extracts from susceptible to Tobacco leaf curl virus, which diseased plants. A major observation was made causes a yellowing disease. in 1892 by Iwanowski, who showed that sap from In Western Europe in the period from about tobacco plants displaying the disease described 1600 to 1660, many paintings and drawings by Mayer was still infective after it had been were made of tulips that demonstrate flower passed through a bacteria-proof filter candle. symptoms of virus disease. These are recorded However, based on previous studies, it was in the Herbals of the time and some of the ear- thought that this agent was a toxin. Iwanowski’s liest in the still-life paintings of artists such as experiment was repeated in 1898 by Beijerinck Ambrosius Bosschaert. During this period, (see Figure 1.2B), who showed that the agent mul- blooms featuring such striped patterns were tiplied in infected tissue and called it contagium prized as special varieties, leading to the phe- vivum fluidum (Latin for “contagious living fluid”) nomenon of “tulipomania” (Box 1.1). to distinguish it from contagious corpuscular Because of their small genomes, viruses have agents (Figure 1.2C). played a major role in elucidating many of the Beijerinck and other scientists used the term concepts in molecular biology, and the study of virus to describe the causative agents of such plant viruses has produced several of the major transmissible diseases to contrast them with findings for virology in general. The major steps bacteria. The term virus had been used more in reaching the current understanding of viruses or less synonymously with bacteria by earlier are shown in the timeline in Figure 1.1. workers, but as more diseases of this sort were Details of these “breakthroughs” can be found discovered, the unknown causative agents in Hull (2002; plant viruses), Fenner, (2008; verte- came to be called “filterable viruses.” Similar brate viruses), and Ackermann (2008; bacterial properties were soon after reported for some viruses). Plant viruses played a major role in viruses of animals (e.g., the filterable nature of BOX 1.1 TULIPOMANIA Tulips were introduced into the Netherlands in the late sixteenth century. Bulbs that produced ”broken- coloured” flowers were in great demand and created a rapidly expanding market, leading to hyperinflation. (continued) I. INTRODUCTION TO PLANT VIRUSES II. HISTORY 5 BOX 1.1 (continued) Semper Augustus tulip with flower colour break (one of the most favoured varieties) One bulb cost 1,000 Dutch florins (guilders) in 1623, and by 1635, 6,000 florins. To understand the value of this, one Viceroy tulip bulb was exchanged for goods that were valued at almost 2,400 florins: 4 tons of wheat (448 florins) 4 barrels of beer (3 florins) 8 tons of rye (558 florins) 2 barrels of butter (192 florins) 4 fat oxen (480 florins) 1,000 lbs cheese (120 florins) 8 fat pigs (240 florins) 1 bed with accessories (100 florins) 12 fat sheep (120 florins) 1 silver goblet (60 florins) 2 hogsheads of wine (70 florins) By 1636 there was much speculation, and futures were being taken out on these bulbs. In early 1637 one bulb was valued at 10,000 florins, but a few weeks later, the bubble burst and many people were left bankrupt. It was not until the 1920s that the viral aetiology of tulip flower breaking was discovered and that the symptoms were caused by an aphid-transmitted potyvirus. Today, 100 flor- ins is equivalent to about U.S. $30,000. I. INTRODUCTION TO PLANT VIRUSES 6 1. WHAT IS A VIRUS? Plant Animal Bacteria Prehistory 752 AD Plant virus in Japanese 1350 BC Smallpox recorded in Egypt poem 1600-1637 Tulipomania 1796 Jenner developed smallpox vaccine Recognition of viral entity 1886 Meyer Transmission of TMV 1892 Iwanowski Filterability of TMV 1898 Beijerink Viruses as an 1898 Filterability of PV and FMDV entity 1915. Filterability of phage Biological age 1900-1935 Descriptions of 1900– Descriptions of many viruses 1915- Descriptions of many many viruses viruses 1901 Mosquito transmission of YFV Early 1920s Infection cycle understood Biophysical/biochemical age 1935 Purification of TMV 1936 TMV contains pentose nucleic acid 1939 EM TMV rod-shaped 1940 VACV contains DNA particles 1949 PV grown in cultured cells 1940-1970 Phage genetics 1951 TYMV RNA in protein shell 1956 Virus particles made of identical protein subunit 1955/56 Infectious nature of TMV RNA 1962 Structure of isometric particles 1983 Structure of TBSV to 2.9Å 1985 Structure of poliovirus to 2.9Å Molecular age 1960 Sequence of TMV coat 1979 Sequence of PV VPg protein 1970 Recognition of reverse transcriptase 1981 Infectious transcript of PV 1978 Infectious transcript of Qβ 1980 Sequence of CaMV DNA genome 1982 Sequence of TMV RNA 1981 Sequence of poliovirus RNA genome genome 1984 Infectious transcripts of multicomponent BMV 1986 Transgenic protection of plants against TMV 1996 Recognition of RNA silencing 1997 Recognition of virus suppressors of silencing Abbreviations: BMV, Brome mosaic virus; CaMV, Cauliflower mosaic virus; FMDV, Foot and mouth disease virus; PV, Poliovirus; TBSV, Tomato bushy stunt virus; TMV, Tobacco mosaic virus; TYMV, Turnip yellow mosaic virus; VACV, Vaccinia virus; YFV, Yellow fever virus. FIGURE 1.1 Timeline of development of virology. I. INTRODUCTION TO PLANT VIRUSES II. HISTORY 7 FIGURE 1.2 A. Adolf Eduard Mayer (1843–1942); B. Martinus Willem Beijerinck (1851–1931); C. Page from lab journal of W.M. Beijerinck from 1898 relating to TMV. A and B courtesy of the historical collection, Agricultural University, Wageningen, Netherlands; C. ( # Kluyver Institute) Courtesy Cura- tor Kluyver Laboratory Collection, Delft School of Microbiology Archive, Delft University of Technology. A B C I. INTRODUCTION TO PLANT VIRUSES 8 1. WHAT IS A VIRUS? the agent causing foot and mouth disease in In 1935, Stanley announced the isolation of this 1898) and of bacteria in 1915. Over the course virus in an apparently crystalline state but con- of time, the word filterable has been dropped, sidered that the virus was a globulin containing leaving just the term virus. no phosphorus. In 1936, however, Bawden and As shown in the timeline in Figure 1.1, in the his colleagues described the isolation from subsequent development of virology, many of TMV-infected plants of a liquid crystalline nucle- the studies ran in parallel for viruses of plants, oprotein containing nucleic acid of the pentose vertebrates, invertebrates, and bacteria. In fact, type. Around 1950, Markham and Smith showed when viewed overall, there is evidence of much that the RNA of Turnip yellow mosaic virus was cross-feeding between the various branches of encapsidated in a protein shell and was impor- virology. However, there were differences tant for biological activity. This led to the classic mainly due to the interactions that these experiments of Gierer, Schramm, Fraenkel-Con- viruses have with their hosts. For instance, ver- rat, and Williams in the mid-1950s that demon- tebrates produce antibodies that counter strated the infectivity of naked TMV RNA and viruses, whereas plants, invertebrates, and bac- the protective role of the protein coat. teria do not. Another factor that has contribu- In parallel with these biochemical studies, ted to advances is the simplicity of the system physical studies in the late 1930s using X-ray exemplified by studies on bacteriophage being analysis and electron microscopy confirmed that linked to studies on bacterial genetics.

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