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The challenge of controlling plant viruses

2014; Wiley; Volume: 164; Issue: 3 Linguagem: Inglês

10.1111/aab.12125

1744-7348

Jari P. T. Valkonen,

Plant Parasitism and Resistance

Viruses are challenging pathogens to control, as they reveal themselves only via the symptoms they cause and cannot, with rare exceptions, be controlled through the application of pesticides or other chemicals in the field (Mowry, 2005; Vidal et al., 2013). Because of the yield losses caused by viruses, their detection, mode of transmission between plants and control have been the subjects of a vast number of scientific investigations (Jones et al., 2010; Ferriol et al., 2013; Juarez et al., 2013). In this issue of Annals of Applied Biology (Annals), Roger A. C. Jones reviews the progress achieved in understanding the epidemiology of plant viruses, which provides the necessary basis for planning successful virus control strategies of arable and horticultural crops (Jones, 2014). His overview is based on a large amount of literature and also his own experience in the study of epidemiology and control of many types of plant viruses in different crops on three continents (Europe, South America and Australia). Roger Jones has published over 200 scientific papers concerning plant viruses and plays since many years an active role in the international societies that promote research into the epidemiology and control of plant viruses. Plant virology is one of the common themes in papers published by Annals, since the early days of the journal. On average, studies on viruses have been reported in one out of seven papers published in the journal. The Annals was established 16 years after Martinus W. Beijerinck reported his eye-opening observations on contagium vivum fluidum (Anon., 1898), which marked an exceptionally significant conceptual advance in understanding the causes of diseases. Beijerinck introduced viruses as the third class into the big picture of existing pathogens, in addition to the already known fungi and bacteria. While the physical and chemical nature of viruses remained enigmatic for some time, the concept of 'viruses' was found to explain many diseases in plants and opened up a completely new field of study. Demand for expertise in plant virology increased. In his discussion paper published in Annals, William Brierley (1927), the Editor-in-Chief of Annals of Applied Biology from 1921 to 1945, expressed worries that 'considering the importance of these diseases, deplorably little is being done in their study … it is imperative that such work should be done with a meticulous accuracy and impeccable technique such as have rarely been demanded in previous phytopathological studies, and, also, that it should be done with full cognisance of similar researches into virus diseases of animals and man'. Brierley was the head of the Mycology Department at Rothamsted Experimental Station, UK, where John Henderson Smith was the plant virologist at that time. Henderson Smith was later the head of the Department of Plant Pathology 1933–1940 at Rothamsted and President of the Association of Applied Biologists (AAB) in 1937–1938. It seems that the challenge put forward by Brierley was taken seriously, because in <10 years Rothamsted had developed into one of the most important international centres of excellence in plant virology, where F. C. (Fred) Bawden, N. W. (Bill) Pirie and co-workers (Bawden et al., 1936) were the first to solve the chemical nature of tobacco mosaic virus particles (Harrison, 1999). The increasingly active research on plant viruses has been reflected in the contents of Annals from the 1920s onwards. Yield degeneration of potato associated with the leaf roll disease (Whitehead, 1924), now known to be caused by the aphid-transmitted Potato leaf roll virus (PLRV), was one of the first topics investigated in many papers. Studies on the epidemiology of PLRV informed control programmes that can now be applied to reduce the spread of PLRV in the field (Mowry, 2005). Resistance breeding has produced potato varieties with high levels of resistance to PLRV (Solomon-Blackburn et al., 2008). Transmission of the reversion disease agent in blackcurrants represented another early virus-related research topic communicated by Annals. Lees (1925) clarified many important features of the reversion disease, such as transmission of the disease agent from diseased plants to healthy blackcurrants by grafting, in the absence of mites or other potential vectors, and slow and erratic appearance of symptoms in the graft-inoculated plants. However, it took over 70 years to fulfil Koch's postulates and show that black currant reversion is, indeed, caused by a virus (Jones et al., 1998; Lemmetty & Lehto, 1999). Many papers published in the Annals form a track of chronological progress made from the description of a disease, identification of the virus and its vector, studies on the epidemiology, through to the development of effective strategies to control the virus. The fact that plant virologists have regularly deemed the Annals as the most pertinent channel for publishing their applicable results is also reflected in the ranking of three plant virologists among the four authors who have published the largest number of papers in the Annals (Azevedo et al., 2014). They are, respectively, A. Teifion Jones, Bryan D. Harrison and Roger Jones who is the author of the Centenary Review included in this issue. All the three authors have shown a keen interest in the epidemiological aspects of plant viruses since the beginning of their career. Roger Jones started his research supervised by Bryan Harrison at the Scottish Horticultural Research Institute (now the James Hutton Institute) studying the epidemiology of Potato mop-top virus transmitted by soil microbe, Spongospora subterranea (Jones & Harrison, 1969). Harrison's early research on plant virus epidemiology at Rothamsted Experimental Station had revealed the role of nematodes as vectors of the Arabis mosaic virus, which infects a wide range of horticultural crops. His studies showed that both the vector and virus are common constituents of natural woodland in Britain (Harrison & Cadman, 1959; Harrison & Winslow, 1961) and introduced the topic of natural reservoirs of viruses and their vectors, which is an increasingly important topic in plant virus ecology and epidemiology (Jones, 2014). Teifion Jones worked for many years at the Scottish Crop Research Institute (also now the James Hutton Institute) on the control of virus diseases in horticultural crops, such as the pollen-transmitted raspberry bushy dwarf disease and other diseases caused by aphid-transmitted viruses in raspberry. He described new viruses and was involved in breeding for resistance against the viruses and their vectors (Murant et al., 1974; Jones, 1976; Jones et al., 1998, 2006). He also contributed to the conceptual understanding of the responses of plants to viruses and clarified the terminology with J. Ian Cooper (University of Oxford, UK), whose interest was in the ecological aspects of plant viruses (Cooper & Jones, 1983). The paper of Bedford et al. (1994) on geminiviruses and the biotypes of their whitefly vector Bemisia tabaci (Gennadius) is among the most cited and influential papers published in the Annals. It was published at the advent of the unprecedented, global virus disease epidemics which are still affecting crops grown in tropical and subtropical areas (Tsai et al., 2011, 2013; Soleimani et al., 2013; Martinez-Ayala et al., 2014). The epidemics were associated with whitefly populations able to transmit a wide range of previously unknown geminiviruses from wild plants to crops and between different crop species (Fargette et al., 1996; Nateshan et al., 1996; Harrison et al., 1997; Rojas et al., 2000). The unusual ability of geminiviruses to generate infective recombinants of their single-stranded circular DNA genomes was thought to be an important basis for success in infecting new hosts (Zhou et al., 1997). Epidemiology and control strategies applicable with geminiviruses are discussed elsewhere in this issue (Jones, 2014). The viruses of family Geminiviridae were found in Harrison's laboratory (Harrison et al., 1977) at the time when Roger Hull at the John Innes Institute, UK, was studying pararetroviruses, another novel group of plant viruses with DNA genomes (Covey & Hull, 1981). Both lines of research greatly advanced the understanding of gene expression, multiplication and evolution of viruses, and molecular and cellular biology in general. Harrison and Sir David C. Baulcombe (currently at University of Cambridge, UK; knighted by Queen Elizabeth II for his service to plant science) developed one of the first examples of genetically engineered resistance to viruses by transforming plants to express the satellite RNA of Cucumber mosaic virus (Baulcombe et al., 1986; Harrison et al., 1987). Studies on the mechanism of engineered resistance led to the realisation that transgenic resistance merely activated the so far unknown natural antiviral defence system, which is induced by double-stranded RNA, including the replicating viruses (Ratcliff et al., 1997; Hamilton & Baulcombe, 1999). Establishing the mechanism, termed RNA silencing or RNAi (Baulcombe, 2007), marked another exceptionally significant conceptual advance in our understanding of the cause of viral diseases and can be compared with the discovery of viruses one century earlier. When viruses obstruct the action of RNAi to prevent the degradation of their own genomes or gene transcripts, they also suppress as a side effect the natural gene regulation mechanism of plants based on RNAi. Hence, many developmental and growth anomalies and other symptoms of virus-infected plants find their explanation in disturbed RNAi-based gene regulation (Pumplin & Voinnet, 2013). Harrison and Hull advanced the control of plant viruses significantly, besides their pioneering studies in molecular virology. As Harrison, also Hull involved himself in the study of plant virus epidemiology at the beginning of his career (Hull, 1964; Hull & Adams, 1968) and published a large number of papers in the Annals. Both Harrison and Hull helped to solve virus problems in developing countries and to train local experts (Hull, 1964; Hull & Adams, 1968; Nateshan et al., 1996; Harrison et al., 1997; Zhou et al., 1997; Harper et al., 2002). Hull is also the author of the latest edition of Matthews' Plant Virology, the main textbook used for teaching plant virology in universities all over the world. AAB has recognised the extraordinary services of Harrison and Hull to plant virology and agriculture by establishing the Bryan Harrison Prize (best student talk) and the Raymond/Roger Hull Prize (best student poster), which are awarded at the AAB Advances in Plant Virology conferences. In addition, Harrison has been elected as an Honorary Member of AAB. In future, the method allowing universal detection of viruses may appear as one of the most applicable outputs from studies on RNAi (Kreuze et al., 2009). In infected tissues, the cellular RNAi mechanism degrades viral double-stranded RNA to small interfering RNA (siRNA; 21, 22 and 24 nucleotides in plants), which guides the RNAi mechanism to target also single-stranded viral RNA. On the other hand, dedicated virus-encoded proteins suppress RNAi. Hence, infected tissues sustain, simultaneously, amplification of viral RNA and its degradation to siRNA. For virus detection, siRNA can be isolated and subjected to deep sequencing. The assembly of the siRNA reads to longer contiguous sequences (contigs) using bioinformatics tools, and the use of contigs as queries in sequence databases allows the identification of homologous viral sequences and hence the viruses in the sample. When developed further, for example, by designing user-friendly computer software for data analysis, this new approach may revolutionise virus diagnostics. The advantages are that test plants, antibodies or probes are not needed, and all types of viruses will be detected in a single assay simultaneously. The method is economically attractive because tens to hundreds of samples can be pooled for analysis (Kreuze et al., 2009). siRNA deep sequencing analysis was first applied to detect five different RNA and DNA viruses in a single sweet potato plant. Three of the viruses were novel and detected for the first time (Kreuze et al., 2009). Another study used the method to detect a previously unknown virus in wild Arctium plants displaying virus-like symptoms (Bi et al., 2012). The method detects also unrelated viruses in animal tissues (Wu et al., 2010) and is practical and easy to adopt in routine use. Its applicability will be further enhanced by the results from the extensive on-going surveys of viruses in wild, symptomless plants based on other metagenomics approaches and the sequences of thousands of newly discovered viruses (MacDiarmid et al., 2013). Hence, the latest molecular discoveries in plant virology will contribute significantly to a more comprehensive understanding of the plant virome and plant virus epidemiology, which in turn will support the planning of better virus control strategies in crop plants.