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Keywords:

  • Agro-ecological interface;
  • biodiversity;
  • climate change;
  • ecology;
  • endangered species;
  • epidemics;
  • evolution;
  • field and molecular biology;
  • food security;
  • future prospects;
  • history;
  • plant virology;
  • progress;
  • technological innovation;
  • virus–vector interactions

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

After clarifying the relationship between the closely related concepts of ecology and epidemiology as they are used in plant virology, this article provides a historical perspective on the subject before discussing recent progress and future prospects. Ecology focuses on virus populations interacting with host populations within a variable environment, while epidemiology focuses on the complex association between virus and host plant, and factors that influence spread. The evolution and growth of plant virus ecology and epidemiology since its inception to the present day, and the major milestones in its development, are illustrated by examples from influential historical reviews published in the Annals of Applied Biology over the last 100 years. Original research papers published in the journal are used to illustrate important ecological and epidemiological principles and new developments in both fields. Both areas are multifaceted with many factors influencing host plants, and virus and vector behaviour. The highly diverse scenarios that arise from this process influence the virus population and the spatiotemporal dynamics of virus distribution and spread. The review then describes exciting progress in research in the areas of molecular epidemiology and ecology, and understanding virus–vector interactions. Application of new molecular techniques has greatly accelerated the rate of progress in understanding virus populations and the way changes in these populations influence epidemics. Viruses cause direct and plant-mediated indirect effects on insect vectors by modifying their life cycles, fitness and behaviour, and one of the most fascinating recent fields of research concerns plant-mediated indirect virus manipulation of insect vector behaviour that encourages virus spread. Next, the review describes the current state of knowledge about spread of plant viruses at the critical agro-ecological interface between managed and natural vegetation. There is an urgent need to understand how viruses move in both directions between the two and be able to anticipate these kinds of events. To obtain an understanding of, and ability to foresee, such events will require a major research effort into the future. The review finishes by discussing the implications of climate change and rapid technological innovation for the types of research needed to avoid virus threats to future world food supplies and plant biodiversity. There has been lamentably little focus on research to determine the magnitude of the threat from diseases caused in diverse plant virus pathosystems under different climate change scenarios. Increasing technological innovation offers many opportunities to help ensure this situation is addressed, and provide plant virus ecology and epidemiology with a very exciting future.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

Plant virus ecology and epidemiology are closely interrelated but distinct concepts, the former concentrating on the virus population within the environment, and the latter on the complex association between the virus and its host plant resulting in disease, and the factors that influence spread within the host plant population (Wilson 2014). Gibbs (1983) emphasised that there was more to understanding virus ecology than a study of life cycles of crop pathogens as in natural ecosystems there are mixed virus populations interacting with complex host populations in a variable environment. Hull (2002) defined ecology to be the study of factors influencing the behaviour of a virus in a given situation, and epidemiology to be the study of the determinants, dynamics and distribution of virus diseases in host populations. Wilson (2014) defined ecology as the study of virus behaviour in its habitat and the factors that influence this behaviour, and epidemiology as the study of virus disease within host populations. Waggoner & Aylor (2000) defined epidemiology as the study of patterns of disease within space and time, and within populations. Robert (2001) defined epidemiology as the cyclical development of virus diseases within plant populations in time and space. Thus, epidemiology deals with how and why a virus spreads in an ecosystem. Understanding its epidemiology is essential before a virus disease can be controlled effectively (e.g. Jones, 2004).

From its beginnings in the early 20th century, plant virus ecology gradually became disconnected from the wider field of plant ecology due to: (a) a widening separation between the disciplines of plant ecology and virology caused by technological and intellectual advances that began in the second half of the 20th century and caused most virology researchers to follow a reductionist approach focusing on virus molecular biology rather than taking an ecological perspective (Thresh, 1981a,b; Malmstrom et al., 2011); and (b) the frequent absence of obvious damage or symptoms within virus-infected, undisturbed natural plant communities resulting from a combination of co-evolution with their hosts over millennia and natural control measures that operate to limit virus epidemics in undisturbed vegetation (e.g. Thresh, 1980a, 1981a,b; Bos, 1981; Cooper & Jones 2006; Jones, 2006, 2009, 2014; Malmstrom et al., 2011; Prendeville et al., 2012; Roossinck, 2013). Thresh (1980a, 1991) recognised that ecological aspects had not been covered sufficiently in plant virus research and advocated an ecological approach to the epidemiology of plant virus diseases. Plumb & Thresh (1983) emphasised that epidemiology draws on ecological perspectives to understand and model complex pathosystems, especially those with deleterious effects on plants of economic importance. However, the terms ecology and epidemiology have often been used interchangeably in the plant virus literature (Hull 2002). Both terms are often used in papers dealing with virus spread in cultivated plants and weeds (e.g. Broadbent et al., 1951; Broadbent & Martini, 1959; Carter, 1961; Broadbent, 1965; Lister & Murant, 1967; Murant & Lister, 1967; Jones & Harrison, 1972; Cooper & Harrison, 1973; Thresh, 1974a, 1980a,b, 1983b, 1991, 2003, 2006a,b,c; Harrison, 1981; Jones, 1981, 1988a, 2004, 2014; Tomlinson, 1987; Cohen et al., 1988; Schlosser, 1988; Irwin & Thresh, 1990; Gallitelli, 2000; Thresh & Fargette, 2003; Morales & Jones, 2004; Coutts et al., 2008; Makkouk & Kumari, 2009; Adkins et al., 2011; Culbreath & Srinivasan, 2011; Hull, 2014). Similarly, the terms molecular ecology and molecular epidemiology are both used for studies on virus spread in cultivated plants and weeds (e.g. Garcia-Arenal et al., 2000; Fargette et al., 2006; Lecoq et al., 2009; Traore et al., 2009; Olarte-Castillo et al., 2011). However, the terms epidemiology and molecular epidemiology have rarely been applied in plant virus literature dealing with wild plants growing in natural vegetation (e.g. Bos, 1981; Thresh, 1981a,b; Cooper & Jones, 2006; Power, 2008; Malmstrom et al., 2011; Power et al., 2011; Roossinck, 2012, 2013).

Many general reviews, books and book chapters have been published on different aspects of the subject of plant virus ecology and epidemiology over the years (e.g. Matthews, 1970; Thresh, 1974a,b, 1976, 1980a,b, 1981a,b, 1982, 1983a,b,c, 1986, 1991, 2004, 2006a,b,c,d; Bos, 1981; Harrison, 1981; Gibbs, 1983; Tomlinson, 1987; McLean et al., 1986; Robert, 2001; Hull, 2002, 2014; Raybold et al., 2003; Cooper & Jones, 2006; Power, 2008; Jones, 2009, 2014; Malmstrom et al., 2011; Roossinck, 2013; Wilson, 2014). To commemorate the Centenary of the Annals of Applied Biology and provide a historical perspective on the subject, this review (a) summarises the contributions of influential review articles in the journal covering the period since the beginnings of plant virology as a discipline until the present, and (b) provides examples from original research papers in the journal that illustrate important ecological and epidemiological concepts and new developments. The review then summarises exciting recent progress in research in the areas of molecular epidemiology and ecology and understanding virus–vector interactions. It finishes by discussing the current state of knowledge about spread of viruses at the critical interface between managed and natural vegetation, the ways climate change is likely to alter plant virus ecology and epidemics in the future, and the many opportunities being provided to enhance future research in the discipline by rapidly increasing technological innovation.

Past Annals of Applied Biology review articles

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

Research on plant viruses and virus diseases has been a major theme of the Association of Applied Biologists (AAB) since its earliest years and the subject of many papers in the Annals of Applied Biology, including 152 papers on plant viruses since 2002. At the Golden Jubilee Meeting of the AAB in 1954, the topic was reviewed in four papers published in the following year. Smith (1955) reviewed trends in plant virus research from its beginnings, Bawden (1955) covered progress in research on the spread and control of plant viruses, Homes (1955) addressed host resistance to plant viruses, and van Slogteren (1955) discussed progress in serological diagnosis of plant viruses. At the meeting in 1979 commemorating the AAB's 75th Anniversary, advances in plant virus research made in the intervening quarter century were reviewed (Harrison, 1980), and, at the meeting commemorating the AAB's Centenary year in 2004, this practice was followed again for the next quarter century (Harrison & Robinson, 2005). All of these historical reviews were published in the journal. They emphasised major achievements and milestones in diverse aspects of plant virology since its inception, and, except for van Slogteren (1955), all included progress in research on plant virus ecology, epidemiology and/or control. This section summarises the relevant contents of these historical reviews, and then provides five examples of influential reviews also published in the journal that summarise diverse aspects of plant virus ecology or epidemiology research.

Historical reviews

Smith (1955) referred to the ‘dark age’ of plant virus research as the period before the 1930s after which a more scientific approach began. It was about this time that it started to involve other disciplines and it was from this concerted attack that much early fundamental knowledge of plant viruses accrued. In 1916, researchers in the Netherlands discovered the infectious nature of potato leaf roll disease. This gave a death-blow to the theory of senile-decay, leading to an understanding that degeneration of potatoes was due to spread of viruses within the crop. By 1939, the importance of insects as virus vectors became fully recognised and the relationship between insect-borne viruses and their vectors was defined as ‘persistent’ or ‘non-persistent’, according to the time insects retained infectivity without having access to a virus source. Transmission of Turnip yellow mosaic virus (TYMV, genus Tymovirus) by flea beetles provided an example of virus transmission by biting insects, and transmission of what is now called Potato virus M (genus Carlavirus) was shown to occur by plant-to-plant contact. Myzus persicae was shown to transmit more than 20 different plant viruses. The phenomenon of cross-protection between different strains of the same virus was discovered.

Homes (1955) emphasised that natural selection results in development of virus resistance in plants, but is offset by selection for increased virulence among virus variants. Crowding of plants under cultivation increases the need for high levels of virus resistance. He provided examples of strain specific resistance to Tomato spotted wilt virus (TSWV; genus Tospovirus) in tomato, and considerable detail over research then underway on different types of resistance to Tobacco mosaic virus (TMV; genus Tobamovirus) in tobacco.

Bawden (1955) emphasised that they were then still very ignorant about plant viruses, and, unless much more knowledge was obtained and applied to counter them, virus diseases were likely to become more important in the future. Factors likely to encourage their spread included (a) cultivation of large areas of uniformly susceptible crops; (b) transport of all kinds of plants around the world and the general increase in the speed and quantity of travel; (c) increasing use of clonal planting material; and (d) improving standards of manuring and cultivation – because this gave rise to bigger, actively growing plants that were more vulnerable to viruses and their vectors. Virus control measures identified by then included: crop hygiene; cleaning up vegetatively propagated material; heat treatment and apical meristem tip culture to free completely infected plant material; propagation of healthy planting material and field certification schemes; weed control to remove alternative hosts; isolation of seedling propagation areas from crops of the same species; planting virus resistant cultivars; and using insecticide sprays to kill vectors. However, he stressed that more information about virus ecology was needed to assess the effectiveness of controlling viruses by these and other means, for example altering sowing date or surrounding crops with non-host barriers. He finished by emphasising that ‘whoever talks on the control of plant virus diseases at the Centenary Meeting of the AAB will be able to talk much more confidently, and paint a rosier picture, than I can today’.

In addition to other issues, Harrison (1980) emphasised progress in understanding vectors and virus transmission mechanisms, ecological systems and epidemiology, and advances in control methods. During the period 1954–1979, important additions to knowledge of how viruses spread from plant-to-plant included finding they can spread via pollen to the plant pollinated, and by two very different kinds of soil-inhabiting organisms, nematodes and fungi. Different types of virus transmission were described involving superficial attachment of virus particles to vectors or their presence inside them, such as, at one extreme, potyvirus attachment to aphid stylets and Tobacco necrosis virus (TNV; genus Necrovirus) to the surface of Olpidium vector zoospores, versus, at the other extreme, virus replication of plant reoviruses and rhabdoviruses within their aphid or leafhopper vectors. New ecological systems described included ones for viruses with soil-inhabiting vectors in which their fungal or nematode vectors have little mobility but have effective ways of persisting at sites. For viruses with aerial vectors, a growing realisation had developed of the importance of perennial hosts, seed transmission and long-term persistence within vectors in ensuring virus survival during periods unfavourable to plant growth. Moreover, a much improved understanding had developed of (a) the critical role of climate in influencing aerial vector activity and the rate of virus spread, and (b) how virus epidemics develop in space and time. The data derived from such work had direct application when assessing the prospects of control by killing vectors or when formulating requirements for healthy stock schemes with minimal virus content. To categorise virus ecological systems, the concepts of virus reproduction rate (rmax) and carrying capacity of habitat (k) were introduced from plant ecology. The concept of integrated control was also introduced, and, although few novel methods of virus control were developed during the 25 year period, application of previously established principles had resulted in major improvements in crop health.

Harrison & Robinson (2005) emphasised that a massive application of new molecular and cell biological, and molecular genetical, techniques had occurred during the period 1979–2004. Progress had been made in wide range of areas, but those most relevant to virus ecology and epidemiology included: mechanisms of virus transmission by invertebrate and plasmodiophorid vectors were unravelled; discovery of gene silencing and viral silencing-suppressor proteins had explained the phenomena of recovery from virus disease, cross-protection between virus strains and synergy between unrelated viruses; transgenic, virus-resistant plants were created, tested successfully in field conditions and a few commercialised; and genetic recombination was found to make an important contribution to generating virus variation. Although many epidemics had continued to be held in check by well-established control measures, several new kinds of serious virus epidemics had appeared. Important progress included identification of factors underlying their appearance. They were partly a result of mankind's activities, including those that led to pesticide-resistant forms of vectors and their intercontinental dissemination, and the increase in year-round culture of crops under plastic-covered structures. Examples included: (a) an upsurge in outbreaks of soil-borne Polymyxa-transmitted barley mosaic viruses in Western Europe following a substantial switch from spring-sown to autumn-sown barley, earlier planting of autumn-sown crops and greater susceptibility of autumn-sown cultivars; (b) greatly increased spread and losses caused by TSWV (Fig. 1A–D) and other tospoviruses resulting from increased global distribution of efficient thrips vector, Frankliniella occidentalis; and (c) appearance of crinivirus outbreaks in cucurbit and tomato crops grown in plastic-covered structures in which vector Bemisia tabaci whiteflies were able to survive in large numbers at times of year when carry over in the field would be problematic. However, the dramatic increase in begomovirus epidemics provided the most significant examples:

  1. In west Asia, and subsequently in Central America, southern North America and the Mediterranean region, epidemics of tomato-infecting begomoviruses, for example Tomato yellow leaf curl virus (TYLCV), caused major crop losses following inadvertent importation from other countries of a particularly fecund, insecticide-resistant biotype of B. tabaci, known as the ‘B’ biotype. For example, in the southern USA a range of begomoviruses reached epidemic levels in several botanically diverse crops causing considerable economic losses (Fig. 1E–F) (Harrison & Robinson, 2005).
  2. In much of sub-Saharan Africa, epidemics of a devastating mosaic disease of cassava, a staple food plant since the late 1980s, advanced through Uganda at about 20 km per year, and then spread into neighbouring countries, such as Kenya and Tanzania. This was associated with a recombinant begomovirus derived from East African cassava mosaic virus and African cassava mosaic virus (ACMV) both of which had wide, partially overlapping distributions in Africa. The most severely affected cassava plants contained both the recombinant virus and ACMV. Infection with the recombinant virus made cassava plants better hosts for B. tabaci, helping explain the enlarged vector populations found at the advancing front of the pandemic (Harrison & Robinson, 2005).
  3. In Pakistan, cotton leaf curl disease epidemics appeared at about the same time, and spread during a few years to affect about one million hectares of cotton, causing major crop losses in what was then the main source of foreign income for the country. These epidemics were associated with at least three begomovirus recombinants, each of which shared some of its genome with Okra yellow vein mosaic virus. Their spread was favoured by widespread cultivation of susceptible cotton cultivars and presence of large populations of insecticide-resistant B. tabaci (Harrison & Robinson, 2005).
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Figure 1. Whole crops, individual plants or fruits of three major vegetable species showing symptoms caused by infection with tospoviruses or begomoviruses. (A) Tomato crop in south-west Australia showing all plants severely stunted by infection with the tospovirus Tomato spotted wilt virus (TSWV). (B) Tomato fruit showing concentric chlorotic ring symptoms caused by infection with TSWV. (C) Pepper plant in a south-west Australian crop showing severe chlorotic mottle and leaf deformation symptoms in young leaves caused by infection with TSWV. (D) Pepper fruit showing deformation and concentric dark green ring symptoms caused by infection with TSWV. (E) Tomato crop in Florida showing plants severely stunted by infection with the begomovirus Tomato yellow leaf curl virus – inset (top left) shows foliar symptoms consisting of interveinal chlorosis and deformation of young leaves and death of older leaves. (F) Row of common bean plants in a Florida crop showing bright yellow leaf marking symptoms caused by infection with the begomovirus Bean golden mosaic virus.

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Additional examples of significant milestones in the development of diverse components of plant virus ecology and epidemiology include: (a) recognition of the importance of the ‘ecological trinity’ between virus, vector and host in determining how epidemics develop (Carter, 1939); (b) recognition that aphid vectors can transmit some viruses after very brief acquisition access (1 min) and inoculation access (2 min) periods (Kassanis, 1941); (c) the concept of vector intensity (Irwin & Ruesink, 1986), the product of vector propensity (ability of a given vector to transmit a virus under field conditions) and vector activity (number of vectors landing on a given crop); (d) discovery of the widespread occurrence of plant viruses in fresh waters (Tomlinson & Faithfull, 1984; Koenig, 1986), (e) major advances in the spatiotemporal analysis of virus epidemic data, such as the SADIE (Spatial Analysis by Distance IndicEs) methodology (Perry, 1995; Perry et al., 1996; Perry & Dixon, 2002); and (f) greatly increased sophistication and effectiveness of predictive models for virus epidemics (recently reviewed by Jones et al., 2010). Review articles in books or other journals that provide historical accounts of critical achievements and milestones in plant virus ecology and epidemiology research include: Thresh (1974, 1980a,b, 1981a, 2006a,b,c) and Malmstrom et al. (2011).

Influential reviews

Harrison (1981) published his AAB presidential address from 1980 entitled ‘Plant virus ecology: ingredients, interactions and environmental influences’. He outlined some important stages of progress: discovery of vectors, recognition of vector specificity and development of quantitative analysis of virus spread, and then discussed virus survival systems, virus behaviour in plant communities, effects of climate, evolutionary influences of virus and host upon one another, and the influence of agricultural practices. Among the many principles addressed, he pointed out that two different survival systems where a virus (a) spreads readily to other sites or (b) persists efficiently at a site suggest analogies to r-selected and K-selected species of higher organisms. The r-selected types are opportunists that multiply rapidly and colonise new areas, whereas K-selected types have well-developed competitive abilities and become predominant as the population reaches the carrying capacity of the habitat. However, the important factor here is the mechanism of virus transmission and whether its vectors are r-strategists or K-strategists, which dictates the method of virus perennation. He also made the distinction between CULPAD viruses and WILPAD viruses. CULPAD viruses are cultivated plant-adapted viruses and WILPAD viruses are wild plant-adapted viruses. The former are characterised by having narrow natural host ranges and being specialised to survive and spread within their cultivated plant hosts (Table 1). The latter generally have wide natural host ranges, persist for long periods in their vectors, are unspecialised and are adapted to survive within communities of wild plants. An example of the influence agricultural practices that he provided concerned competitive ability of virus-infected plants within defoliated vs un-defoliated pasture swards. Perennial ryegrass (Lolium perenne) plants infected with Barley yellow dwarf virus (BYDV, genus Luteovirus) have a greater competitive ability in grazed swards than in swards allowed to grow up for hay production whereas the reverse applied to cocksfoot (Dactylis glomerata) plants infected with Cocksfoot streak virus (CSV; genus Potyvirus). This is because BYDV infection increases tillering but decreases height of perennial ryegrass plants whereas CSV does the opposite to cocksfoot plants, decreasing tillering but increasing their height. He concluded by emphasising that with epidemiological studies there is (a) a need for collaboration between virologists and other specialists in studies of virus vector transmission systems (including entomologists, nematologists, mycologists, plant physiologists, weed experts, ecologists), and (b) a similar need for collaboration between virologists and other disciplines over application of the latest techniques for sensitive and large virus detection and diagnosis (including immunologists and molecular biologists). The breadth of disciplines within the AAB made it ideally suited to such collaborations.

Table 1. Examples of virus groups adapted to cultivated (CULPAD viruses) or wild (WILPAD viruses) plantsa
Virus GroupGenomeNatural Host RangeTransmissionPersistence in Vectors
  1. a

    Modified from Harrison (1981).

(A) CULPAD
IlarvirusssRNANarrowPollenNot applicable
PotexvirusssRNANarrowContactNot applicable
TobamovirusssRNANarrowContactNot applicable
(B) WILPAD
GeminivirusssDNAVariousWhitefliesWeeks
LuteovirusssRNAModerateAphidsWeeks
NepovirusssRNAWideNematodesWeeks or months
TobravirusssRNAWideNematodesMonths

Thresh (1976) published an influential review entitled ‘Gradients of plant virus diseases’. Gradients refer to alterations in virus incidence over distance from a virus infection source. Firstly, he discussed the pros and cons of using different plot sizes and shapes (e.g. circular, cruciform, square, rectangular or hexagonal) to collect data on virus gradients. He concluded that circular plots are ideal when following virus spread from a point source but are difficult to plant and maintain. Planting staggered rows to form concentric hexagons provided a convenient alternative. Rectangular or cruciform plots were suited to following spread from external virus sources or from a centrally planted group or strip of virus infector plants. Secondly, he addressed the importance of plot orientation in relation to prevailing wind direction and virus infection source disposition and arrangement, and covered mathematical treatment of gradient data using transformations to produce linear regressions and equations to summarise results. The approaches he suggested for plot orientation and statistical analysis of gradient data were widely adopted and are still being used today. He then went on to describe (a) different types of gradients (e.g. linear, curvilinear, steep, shallow and ‘false’) and the reasons why each of them form, and (b) the implications of having primary and secondary infection foci, spread within and across rows, and spread from internal and external infection sources (Fig. 2). He also discussed how gradients can be used to evaluate the effectiveness of control measures. Finally, he emphasised that quite different factors influence the spread of virus and fungal plant pathogens. The latter seldom result in the chronic systemic infection caused by viruses and are generally independent of spread by vectors. Also, the way environmental factors influence the interaction between a fungal pathogen and its host differ greatly from those involving host, virus and vector. The numerous factors determining take-off, flight, landing and infectivity of insect vectors are much more difficult to quantify and assess than those influencing inert air-borne spores. This further complicates attempts to relate gradients of virus disease with the distribution of virus vectors.

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Figure 2. Examples of virus infection gradients illustrating different scenarios when virus spread occurred in lupin or wheat plantings. (A) Gradient of plants symptomatic for infection with Bean yellow mosaic virus necrotic strain (BYMV-N) in a commercial lupin crop starting from the crop edge adjacent to the BYMV-N infected pasture source (with fitted exponential line 7.76 + 43.7 (0.8406x)). (B) Gradients of plants symptomatic for infection with BYMV-N in a commercial lupin crop, starting from the crop edge bordering either a perimeter oat barrier 20 m-wide that separated adjacent BYMV-N infected pasture from the crop (with fitted linear line 6.561 − 0.1511x; image, solid red spots and red line), or internal tracks containing BYMV-N infected clovers (with fitted exponential line 7.308 + 37.7 (0.27x ); image, solid black spots and black line). (C) Gradients within a lupin stand of plants symptomatic for infection with BYMV-N (with fitted linear line 20.503 − 0.367x; image, solid black spots and black line) or symptomatic for Cucumber mosaic virus (CMV; with fitted exponential line 12.74 + 4.87 (1.088x); image, solid red squares and red line) – the BYMV-N gradient started at the edge bordering a 25 cm wide oat barrier that separated the lupins from a BYMV-N source 11 m to the north, and the CMV gradient started on the opposite edge close to a CMV source 11 m to the south. (D) Gradients of Wheat streak mosaic virus (WSMV) infection in relation to westerly frontal winds in neighbouring wheat fields upwind (west) and downwind (east) of a 100% WSMV-infected wheat cv. Machete crop – note rapid decline in WSMV incidence upwind but very slow decline downwind. (E) Gradient of infection from a fence line adjacent to a WSMV-infected pasture into a crop of wheat cv. Machete – westerly frontal winds blew along the fence line which ran west to east. Graphs were from previous studies in south-west Australia: (A)–(C) are from Jones (2005) and (D)–(E) from Coutts et al. (2008).

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Tomlinson (1987) published a review entitled ‘The epidemiology and control of virus diseases of vegetables’. His approach was to take a wide ranging focus and summarise key aspects of the diverse ecological and epidemiological factors that determine virus spread and virus disease development within vegetable crops in parts of the world with temperate, Mediterranean-type and subtropical climates. The aspects he covered included virus infection reservoirs for spread such as virus-infected weeds, wild plants, volunteer crop plants and nearby crop plants; means of persistence outside the growing season such as dormant infected seeds or roots and tubers, plant debris, volunteers, etc. carried over from the previous growing season; introduction of virus inoculum through sowing infected seed stocks; spread of virus infection to healthy plants by vector transmission and other means; and agricultural and horticultural practices that influence epidemic development. He also described different types of control measures and how they operate, including application of pesticides and oil sprays, measures that alter vector behaviour or repel them, and deployment of virus resistant cultivars. A detailed Appendix listed vegetable diseases known to occur in 28 countries representing the three climatic zones mentioned above. His review provided an excellent general introduction for those wishing to develop an understanding of the scope and importance of vegetable viruses, and learn of the options available for their management.

Mumford et al. (1996) published a review entitled ‘The biology of the tospoviruses’. Interest in the tospoviruses had been rekindled with the resurgence and expansion of TSWV epidemics (Fig. 1A–D) and the appearance of damaging new tospoviruses in different parts of the world, including ones caused by Impatiens necrotic spot virus, Peanut (=Groundnut) bud necrosis virus and Watermelon silver mottle virus. This renewed interest, accompanied by advances in molecular biology techniques, had resulted in a rapid growth in understanding of tospoviruses, especially about their diversity and economic significance. The review encompassed all the major aspects of tospovirus biology, including changes in classification of the genus and knowledge of their molecular biology, vector relations, control and diagnosis. Eight different thrips species were known to transmit tospoviruses, with Frankliniella occidentalis being the most important of these. Its expansion from its original range in Western North America to other parts of the world had led to many tospovirus epidemics and a general increase in tospovirus occurrence. Some of the worst damage in temperate climates occurred amongst protected crops. Thrips transmitted tospoviruses in a persistent, circulative manner, but although adults were able to retain and transmit them for the rest of their lives, they were unable to acquire them. Acquisition only occurred at the first larval stage. This unique virus–vector relationship had major implications over how virus spread occurs in the field. Control of tospoviruses in the field was possible through host resistance to viruses or vectors, insecticide application, phytosanitary measures and cultural control. Biological control using predator mites or insects was also possible under glasshouse conditions.

Varma & Malathi (2003) published a much cited review entitled ‘Emerging geminivirus problems: a serious threat to crop production”. During the two decades before their publication, Geminiviruses had emerged as devastating pathogens, particularly in the tropics and subtropics, their epidemics causing huge economic losses and seriously threatening crop production. Geminiviruses included the genera Begomovirus, Curtovirus, Mastrevirus and Topocuvirus, but begomoviruses caused the most serious problems, including in cassava, cotton, grain legumes and vegetables (Fig. 1E–F). Economic losses due to geminiviruses were estimated to be: US$1300–2300 million in cassava in Africa, US$5 billion in cotton in Pakistan, US$300 million for grain legumes in India and US$140 million in tomato in Florida. Major contributory factors responsible for the emergence and spread of new geminiviruses were the evolution of new virus variants, appearance of the ‘B’ biotype of the vector B. tabaci, and the increase in its population. Genomic recombination in geminiviruses, not only between variants of the same virus, but also between species and even genera, resulted in rapid virus diversification. Some of the most virulent geminiviruses arising from recombination of viral genomes included those associated with cotton leaf curl, tomato leaf curl and cassava mosaic diseases. Heterologous recombinants containing parts of the host genome and/or sequences from satellite-like molecules provided unlimited evolutionary opportunities. Human activity also played a key role in the emergence of serious geminivirus diseases worldwide including changes in cropping systems, introduction of new crops, movement of infected planting materials, and introduction of susceptible germplasm.

Other influential reviews relevant to plant virus ecology and epidemiology published in the journal include ones on controlling virus spread in crop plants by vector resistance (Jones, 1987) and transmission of plant viruses by fungi (Adams, 1991).

Annals of Applied Biology research papers

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

Many valuable additions to the plant virus literature were published in the journal over the last 100 years, including many published in the last 10 years. A large proportion of these contributed significantly to worldwide understanding of plant virus ecology and epidemiology. Some examples are provided below.

Analysis of epidemics

Gradients of infection (see above and Fig. 2) and pathogen or disease progress curves (Fig. 3) are traditional ways to investigate the dynamics of plant virus epidemic development and determine the effectiveness of virus control measures. Recent Annals papers that used the latter include studies involving spread of Bean yellow mosaic virus (BYMV, genus Potyvirus) in lupin (Cheng et al., 2002), TSWV in lettuce (Coutts & Jones, 2005), Carrot virus Y (CarVY; genus Potyvirus) in carrot (Jones et al., 2005) and Lettuce mosaic virus (LMV; genus Potyvirus) in lettuce (Moreno et al., 2007). Such studies of gradients and progress curves are critical ingredients in epidemiology studies designed to measure diverse virus epidemic parameters, including the importance of magnitude and proximity to virus sources, the importance of different types of virus sources, the effect of wind direction on virus spread, the rate and extent of virus spread, the relationships between vector arrival and abundance and amount of virus spread, the likelihood that major yield and quality losses may arise, and whether suggested control measures are likely to be effective.

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Figure 3. Examples of virus disease or pathogen progress curves illustrating different scenarios when virus spread occurred in lettuce or carrot plantings. (A) Disease progress curves for Tomato spotted wilt virus incidence in a field experiment with plots of lettuce in which tomato ‘infector’ or lettuce plants, or both, were treated with neonicotinoid insecticide drench. Treatments applied: (image) thiamethoxam to ‘infector’ and lettuce plants; (image) thiamethoxam to ‘infector’ plants only; (image) thiamethoxam to lettuce plants only; (image) no insecticide to ‘infector’ or lettuce plants; (image) no ‘infector’ plants present or insecticide used; and (image) imidacloprid to ‘infector’ and lettuce plants (Coutts & Jones, 2005). (B) Pathogen progress curves for carrot plants infected with Carrot virus Y in plots at 1 m and 15 m distances from a 100%-infected virus source plot; image, solid spot = 1 m upwind; image, solid square = 1 m downwind; image, solid triangle = 15 m upwind; image, =15 m downwind (from Jones et al. 2005).

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Development of SADIE methodology provided a major advance in the spatiotemporal analysis of virus epidemic data that complements the types of information obtained from gradients and progress curves. Several research papers in the journal employed it to analyse spatiotemporal patterns of virus spread. Thackray et al. (2002) used it to compare patterns resulting from spread of BYMV variants that cause necrotic (systemic hypersensitive) or non-necrotic symptoms in lupin stands by vector aphids. The combination of data from clustering and association analysis showed that spread of non-necrotic BYMV was less diffuse with much more localised infection surrounding infection sources. Jones (2005) used it to examine scenarios where aphid vectors spread Cucumber mosaic virus (CMV; genus Cucumovirus) and necrotic BYMV in lupin stands when the primary virus sources were internal or external. CMV spread was more comprehensive while spread of necrotic BYMV was more diffuse with smaller clusters and more isolated diseased plants, the pattern for non-necrotic BYMV resembling that for CMV. These differences reflected polycylic (CMV, and non-necrotic BYMV) or near monocyclic (necrotic BYMV) patterns of spread. Coutts et al. (2004a) used SADIE to examine spread of lettuce big-vein disease (LBVD) and Lettuce necrotic yellows virus (LNYV; genus Cytorhabdovirus) in lettuce stands. The primary LBVD infection sources were within the stand consisting of soil infested with resting spores of its Olpidium virulentus vector. Clustering of LBVD-infected plants developed where soil was heavily infested with viruliferous resting spores with only sporadic occurrence elsewhere. Aphid vectors spread LNYV from external sources consisting LNYV-infected weeds. Clustering of LNYV-diseased plants was greatest at the crop edge closest to the weed infection source. Moreno et al. (2007) used SADIE to examine the patterns of spread of aphid-borne LMV in a stand in which LMV spread started along one edge. Clusters of LMV-infected plants that enlarged and coalesced reflected its polycyclic spread pattern. SADIE was also used to study patterns of spread of aphid-borne CarVY in carrot plantings (Jones et al., 2005), and of thrips-borne TSWV in lettuce and pepper stands (Coutts et al., 2004b). With CarVY, clusters of diseased plants that enlarged and coalesced were concentrated near to infection sources but expanding clusters also developed further away, reflecting a polycyclic spread pattern (Fig. 4). With TSWV, clustering was greatest near to infection sources but only slow-growing, isolated clusters developed further away. This was consistent with only limited polycyclic spread occurring despite (a) TSWV being a persistently vector transmitted virus, and (b) representing a situation where viruliferous vectors do not lose a virus after probing healthy plants, as occurs with non-persistently vector-borne viruses such as BYMV, CarVY, CMV and LMV. The spatial analysis data for CarVY and TSWV were used to validate inclusion of control measures within Integrated Disease Management strategies for each pathosystem. Measures validated were: planting upwind of infection sources (CarVY, TSWV); deploying intervening non-host barrier crops (TSWV); isolation and safe planting distances (CarVY, TSWV); avoidance of side-by-side plantings (CarVY, TSWV); intervening fallow (CarVY); prompt removal of virus sources (CarVY, TSWV); and manipulation of planting date (CarVY) (Coutts et al., 2004b; Jones et al., 2005).

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Figure 4. Maps of clustering indices for cumulative numbers of Carrot virus Y-infected carrot plants on four different days after sowing (das). Axes show distances in metres. Spots represent units denoting infection patches with v > 0 (red) and infection gaps with v < 0 (blue). Small spots represent clustering indices of 0 to ±0.99 (clustering below expectation), intermediate sized spots ±1 to ±1.49 (clustering exceeds expectation) and large spots >1.5 or <−1.5 (half as much again as expectation). Red lines enclosing patch clusters are contours of v = 1.5 and blue lines enclosing gap clusters are of v = −1.5. Black lines are zero-value contours, representing boundaries between patch and gap regions where the count is close to the overall sample mean (from Jones et al., 2005).

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Roles of alternative hosts

Several recent Annals papers included study of potential alternative hosts to establish their importance as virus reservoirs for spread to susceptible crops. For example, Trebicki et al. (2010) assessed factors likely to be important in the epidemiology of Tobacco yellow dwarf virus (genus Mastrevirus) in tobacco crops in south-east Australia. Orosius orientalis proved to be its predominant leafhopper vector. The virus was detected in four of 40 plant species sampled, tobacco and common bean (Phaseolus vulgaris), and the alternative weed host species Amaranthus retroflexus and Raphanus raphanistrum. The two weed hosts were apparently acting as virus reservoirs from which O. orientalis spread the virus to the two cultivated species. Moreno et al. (2004) examined wild vegetation in Spain to establish whether it was acting as a source of viruses for spread to cultivated brassica and lettuce. All the viruses commonly found infecting these cultivated species were also present in the wild vegetation associated with them, for example Sonchus spp. were frequently infected with CMV, LMV and Beet western yellows virus (BWYV, genus Polerovirus), and Chenopodium album was commonly infected with TSWV and BWYV, suggesting that they both played a significant role as virus reservoirs. In another example, when Prassada Rao et al. (2003) studied an epidemic of Tobacco streak virus in peanut (=groundnut) in India, the weed Parthenium hysterophorus played a major role as an alternative host for virus spread by its thrips vectors to peanut crops. Two other crop hosts for the virus, sunflower and marigold, were also potential alternative hosts for thrips vectored spread to peanut. A comprehensive study of sweetpotato viruses infection in wild species in Uganda, East Africa found a large number of species of Convolvulaceae not previously known to be hosts of Sweet potato feathery mottle virus (SPFMV, genus Potyvirus), Sweet potato mild mottle virus (SPMMV, genus Ipomovirus) and Sweet potato chlorotic stunt virus (SPCSV, genus Crinivirus). All these wild hosts were infected in their natural habitats and were potential virus reservoirs for spread to sweetpotato crops. Although SPFMV and SPCSV originated in other parts of the world, SPMMV spread from native Convolvulaceae species to sweetpotato about 300 years ago after it was introduced to East Africa (Karyeija et al., 1998; Tugume et al., 2008, 2010a,b, 2013).

Emerging viruses

Varma & Malathi (2003) attributed the rapid emergence of geminiviruses as devastating crop pathogens in the tropics and subtropics to increased human activity, appearance and rapid population increase of the ‘B’ biotype B. tabaci vector, and rapid evolution and diversification of new virus variants (see above). Boulton (2003) referred to unlimited evolutionary possibilities for emergence of disease problems arising from widespread dissemination of begomovirus-infected planting material, their abilities to infect many crops and wide occurrence of their ‘B’ biotype vector, coupled with presence of non-specific satellite molecules that alter their virulence and their propensity for genetic recombination. This emergence of geminivuses as crop pathogens in the tropics and subtropics is reflected by the large numbers of Annals papers published recently on new members of this virus group. Examples include begomoviruses infecting: tomato and pepper in North Africa (Tahiri et al., 2006), the Andean region of South America (Martínez-Ayala et al., 2014) and south-east Asia (Tsai et al., 2011); crop legumes in the Andean region and southern cone of South America (Rodríguez-Pardina et al., 2011; Martínez-Ayala et al., 2014), and in south-east Asia (Tsai et al., 2011, 2013); and cassava crops in sub-Saharan Africa (Ssweruwagi et al., 2004). Begomoviruses have also emerged as important crop pathogens in protected cropping situations in cooler climates, for example epidemics of B. tabaci transmitted TYLCV and Tomato yellow leaf curl Sardinia virus in south-east Spain (Velasco et al., 2008).

In a much cited Annals paper, Bedford et al. (1994) studied the transmission and biological characterisation of B. tabaci biotypes from North and Central America, the Caribbean, Africa, the Middle East, Asia and Europe. Most morphological parameters studied could not be used to distinguish different biotypes, but there were clear differences in body lengths and ability to induce phytotoxic disorders in some plant species. The ‘B’ biotype had a diagnostic esterase banding pattern and was the only biotype to induce phytotoxic disorders. Non ‘B’ biotypes did not interbreed, but ‘B’ biotypes interbred with each other. All ‘B’ biotypes and most non ‘B’ biotypes transmitted at least 12 of the 15 different geminiviruses tested. Wang et al. (2010) studied transmission of TYLCV and Tomato yellow leaf curl China virus by the B and Q biotypes of B. tabaci in China. They examined transmission between males and females and transovarially to their progeny. Both viruses were transmitted in both ways but the frequency of transmission was low. Also, adults that developed from the eggs of viruliferous B. tabaci were not infective to plants. They concluded that neither method of transmission were likely to have much epidemiological relevance in the field. Mallowa et al. (2006) examined the characteristics of cassava mosaic virus disease (CMD) in post epidemic areas of Kenya. East African cassava mosaic virus was the predominant geminivirus present while the abundance of B. tabaci vectors varied. Cassava cultivation was being re-established but local land races predominated over bred cultivars. Limited CMD spread provided a suitable environment for use of phytosanitation as a control measure.

Mumford et al. (1996) discussed the emergence of damaging new tospoviruses in different parts of the world (see above). A recent Annals paper provides an example of an emerging tospovirus from sweet pepper. Cheng et al. (2014) found this virus in Taiwan in 2009 causing fruit and leaf mottle and deformation and gave it the provisional name Pepper chlorotic spot virus. No vector or epidemiological studies were reported.

Influence of world trade

An example of the inadvertent movement of damaging viruses around the world through trade in plants and plant products was provided by Pepino mosaic virus (PepMV, genus Potexvirus), a virus first described in an Annals paper (Jones et al., 1980). In 1974, PepMV was isolated from a pepino (Solanum muricatum) crop growing in coastal Peru in the Andean region of South America. It caused a yellow mosaic in young leaves of pepino (Fig. 5A), had stable particles and was readily contact transmissible. It was able to infect a range of species in the Solanaceae on sap inoculation, including potato and tomato. There were no further reports until 1999 when it appeared infecting tomato in the Netherlands (van der Vlugt et al., 2000). It then spread rapidly to several other European countries, North America and China. It is economically important because it compromises the appearance of tomato fruits (Fig. 5B) and contaminates the surface of its seed. Its appearance in other continents was attributed to activities of international seed companies using South America to propagate tomato seed crops for sale elsewhere, and the increased speed and volume of international trade in tomato seeds and fruits (Mumford & Jones, 2005). It was thought only to spread from plant-to-plant by contact and seed transmission, but a recent Annals paper demonstrated that it is also spread by bumble-bees (Bombus impatiens) which are widely used to pollinate tomato and other crops in commercial greenhouses (Shipp et al., 2008). This transmission might occur through direct injury to flowers (biting the anthers and shaking the flowers to collect pollen) or through fertilisation with infected pollen, but which infection pathway was important was not determined. Since the risk of PepMV spread is greater when hand pollination is used, pollination by bumble-bees is still required necessitating strict sanitation and roguing of infected plants within affected greenhouses. Gómez et al. (2010) suggested that in mixed infections in tomato plants, accumulation of Tomato torrado virus (genus, Torradovirus) and PepMV may modulate the epidemiology of both viruses.

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Figure 5. Symptoms in virus-infected plants, aphid vector studies and an example of a recent interface between managed and natural vegetation. (A) Pepino leaves showing a yellow mosaic caused by natural infection in Peru (in 1974) with the original strain of Pepino mosaic virus (PepMV). (B) Tomato fruit symptoms showing uneven ripening and surface 'marbling' caused by the tomato strain of PepMV (bottom), healthy with normal appearance (top). (C) Collection of individual, live winged aphids caught on an aerial net downwind of virus-infected plants to determine which species are viruliferous and the numbers of each flying. (D) Winged and wingless individuals of Acyrthosiphon kondoi, an important aphid vector of legume viruses. (E) Agro-ecological interfaces between disturbed or undisturbed ancient unmanaged and recent managed vegetation in the ORD River Irrigation area of north-west Australia where agriculture only commenced <70 years ago. (F) Obvious yellow mottle and leaf deformation symptoms caused by natural infection with Bean yellow mosaic virus in the south-west Australian native plant Kennedia prostrata. Photographs from previous publications: (A) from Jones et al. (1980), (B) from Mumford and Jones (2005), (C) from Berlandier et al. (1997), and (E) from Jones (2013). [(B) was supplied by R. Mumford, and (E) by B.A. Coutts].

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Epidemics in plant species mixtures

When viruses infect their hosts within a population of mixed plant species, a dynamic balance exists for each virus between decreasing virus incidence resulting from poor competitive ability of infected plants and increasing virus incidence due to infection of further healthy host plants. In an Annals paper, Coutts & Jones (2002) found that in the white clover components of mixed grass and white clover pastures, there were often wide temporal fluctuations in incidences of Alfalfa mosaic virus (AMV; genus Alfamovirus) and White clover mosaic virus (WClMV; genus Potexvirus). Factors that favoured spread to healthy host plants by aphid vectors (AMV) or contact (WClMV) increased virus occurrence. These included ones that favoured growth and survival of infected host plants, or virus multiplication within them, so ensuring presence of a considerable virus source, and ones that favoured increased plant wounding by stock and mowing or aphid numbers. Declining virus incidences resulted from factors that (a) increased invasiveness and competitive ability of healthy plants of host species, or of non-host plant species, at the expense of growth and survival of infected host plants, (b) diminished virus concentration within virus-infected host plants, or (c) decreased aphid vector numbers or plant wounding by stock or mowing. Both (a) and (b) were important as, when the proportion of infected host plants or virus concentration within them decreased, the source of virus inoculum for further spread also declined; and (c) was important as less virus transmission to healthy host plants occurred.

Virus ecology in wild plant communities

Fitness is a critical concept when considering the ecology of viruses in wild plants. When virus-infected wild plants grow in species mixtures in undisturbed natural plant communities, relative fitness of infected plants refers to survivorship arising from their abilities to compete with healthy plants of other species, reproduce sufficiently and produce the next generation of seedlings. In an Annals paper, Maskell et al. (1999) investigated viruses infecting plants of wild cabbage (Brassica oleracea) in the UK. Such plants are commonly infected with Turnip mosaic potyvirus (TuMV, genus Potyvirus), TYMV and several other viruses. A field experiment in which plants were inoculated either with TuMV or TYMV showed that virus infection significantly reduced survival, growth and reproduction. They concluded that both viruses significantly diminish vegetative and reproductive performance of wild cabbage. This research showed that virus infection has the potential to seriously damage natural plant communities.

Soil-borne virus ecology

An example of the ecology of a fungus-transmitted virus was provided in a series of Annals papers on Potato mop-top virus (PMTV, genus Pomovirus) in potato. PMTV is transmitted to roots and tubers of healthy potato plants by zoospores and spore balls of Spongospora subterranea (the powdery scab fungus). The virus was carried internally within the spore balls. It was transmitted to potato plants and tubers reproducing typical leaf and tuber symptoms of PMTV. PMTV became established in virus-free soil when PMTV-infected potato tubers carrying S. subterranea were planted. Infection resulted from propagation of seed potatoes on infested land and from unwitting selection of infected plants to start new clones. The virus was able to survive in soil inside S. subterranea resting spores for 12 years after potatoes were grown. S. subterranea had a wide host range infecting the roots of many crop and wild plant species (Jones & Harrison, 1969, 1972). Subsequently, the demonstration of PMTV acquisition and transmission by an S. subterranea culture derived from a single resting spore confirmed its status as its vector unequivocally (Arif et al., 1995). The virus was only passed from an infected plant to a proportion of progeny tubers, so it was gradually self eliminating in the absence of new infections. Decreasing soil pH and adding zinc or calomel to soil diminished PMTV spread, and treating tubers with formaldehyde or organo-mercurial fungicide decreased its establishment in soils (Cooper et al., 1976). These findings explained how the virus spreads within potato crops growing in parts of the world with cool moist climates, and the difficulty of controlling it. Santala et al. (2010) reviewed current knowledge on detection, distribution and control of PMTV, focussing mainly on the Nordic region. The possibility of PMTV spreading when viruliferous zoospores are blown in the wind was discussed, along with the demonstration of its dispersal in soil adhering to tubers. Roots of the common weed Solanum nigrum collected from infested fields were often infected with PMTV so this species could help maintain field infestations through crop rotation when potato is absent. Potato growing areas in Nordic countries were widely contaminated with PMTV, but it was found only once in Poland and Latvia, and remained undetected in Estonia, Lithuania and north-west Russia. Importation of seed potatoes into the five latter countries only started recently while it has occurred into the Nordic countries for decades, which might explain why it was so rarely found in them.

Vector transmission efficiencies

Many past Annals papers reported studies to compare the virus transmission efficiencies of different insect vector species. This was necessary to establish their relative importance as vectors when virus spread was occurring in the field. In a recent example, Verbeek et al. (2010) determined the transmission efficiencies of 16 aphid vector species using Potato virus Y (PVY; genus Potyvirus) strains N, NTN and Wi. For each aphid species and PVY strain, the relative transmission efficiency (REF), in relation to that of Myzus persicae, was compared with the REF reported in the 1980s in this same species. REFs are used to calculate cumulative vector pressure data and contribute to PVY forecasting systems for potato crops in the Netherlands. Re-evaluation of REFs was necessary in the Netherlands because the PVY strain spectrum had changed and the newer recombinant PVY strains were likely to be more efficiently transmitted by aphid vectors. When comparing the calculated REFs for PVY-N with the REFs reported in the last century for PVY-N, they were comparable for half the aphid species, but lower for five (Aphis fabae, Aphis spp., Hyperomyzus lactucae, Macrosiphum euphorbiae and Rhopalosiphum padi) and higher for two (Aphis frangulae and Phorodon humuli) of them. When comparing the new REFs found for PVY-NTN with the new REFs for PVY-N, they were mostly comparable, except with A. frangulae (lower) and Schizaphis graminum (higher). When comparing the REFs calculated for PVYN-Wi with those calculated for PVY-N, six aphid species had higher REFs (Acyrthosiphon pisum, Aphis fabae, Aphis nasturtii, Aphis spp., P. humuli and R. padi) and one a lower REF (A. frangulae). Three aphid species (Aulacorthum solani, Myzus ascalonicus and S. graminum) with no REF value previously were found to be vectors of PVY and their REFs were determined. These newer REFs were substituted for the REFs used formerly when calculating cumulative vector pressure data in PVY forecasting for potato crops in the Netherlands. The methodology Verbeek et al. (2010) used to determine REFs involved conducting transmission experiments with reared biotypes of each aphid species. Kirchner et al. (2011) used a modelling approach to determine which aphid species were most significant PVY vectors in Finland's high grade seed potato production area. The main vector was Aphis fabae which occurred in seed potato fields soon after plant emergence. Straw mulch present then consistently diminished PVY incidence. The model's predictions held up well in practice so it and straw mulch now provide the basis for controlling PVY spread.

An alternative approach to determining the relative importance of different aphid species as vectors was reported earlier in the Annals by Halbert et al. (1981) and Raccah et al. (1985). These two papers proposed a methodology to determine the relative contributions in the field of each aphid vector species, their vector propensities and their roles in epidemics of non-persistently aphid transmitted viruses. They also stressed the importance of non-colonising aphid species as vectors of non-persistently transmitted viruses. Their approach was followed by many researchers. For example, Berlandier et al. (1997) studied the transmission of CMV and BYMV to lupin in south-west Australia. In addition to establishing the efficiencies of nine aphid species to transmit these two viruses in glasshouse conditions, they trapped live flying aphids belonging to 13 different aphid species on vertical nets placed downwind of virus-infected lupins and placed each individual aphid onto a lupin plant in the field (Fig. 5C). The objective was to determine which species were viruliferous and the relative proportions of each species flying. Fig. 5D illustrates an important legume virus vector, Acyrthosiphon kondoi, caught in that study. Averaged over 4 years at one site, A. kondoi accounted for 50% of CMV transmissions, M. persicae for 16% and R. padi for 22%, and these three species were caught in the greatest numbers, comprising 28%, 13% and 32% of the total catch respectively. At another site, R. padi accounted for half of the CMV transmissions, while R. padi and A. kondoi together accounted for most of the BYMV transmissions: R. padi, A. kondoi, M. persicae and Toxoptera citricus were the most common aphid species. When combined with the glasshouse transmission efficiency studies, these findings suggested that R. padi, A. kondoi and M. persicae were the most important vectors of CMV and BYMV in lupin crops south-west Australia. This was critical information when developing forecasting models for spread of both viruses in lupins (Jones et al., 2010).

Seed and pollen transmission

The importance of seed and pollen transmission in the epidemiology of plant viruses was illustrated by two early Annals papers. A ‘tomato strain’ of TMV was carried externally on the surfaces of tomato seeds, and sometimes within their testa and endosperm, but never inside their embryo (Broadbent, 1965). Various treatments removed external seed contamination, but only heating at 70°C for 3 days was effective at removing TMV carried internally. Plants growing from TMV-contaminated seeds never became infected if left undisturbed after they were sown, but did become infected when they were transplanted and their testas, or remaining endosperm, were rubbed against the seedlings. TMV then spread to the rest of the crop. Raspberry bushy dwarf virus (RBDV; genus, Idaeovirus) was transmitted to raspberry seed both through the pollen and the embryo, but also from infected pollen to plants (Murant et al., 1974). There was no RBDV infection in plants prevented from flowering, and transmission through infected pollen was the only method of spread to healthy plants in the field. Plants infected with RBDV had symptomless infection, but flowers pollinated with infected pollen produced ‘crumbly’ fruit with a high proportion of aborted drupelets. Raspberry cultivars that still remained uninfected after graft inoculation had extreme RBDV resistance and were suitable for use as parents in crosses to breed virus-resistant cultivars. Milne & Walter (2003) studied thrips-mediated pollen transmission of Prunus necrotic ringspot virus (PNSV; genus Ilarvirus) in stonefruit orchards in north-east Australia. They concluded that (a) there is mounting circumstantial evidence that stonefruit flowers can be inoculated with PNRSV via an interaction with virus-bearing pollen and (b) this transmission mechanism might be an important cause of new tree infections in the field.

Other original contributions

A few examples of other original contributions from the many published in the journal over the last 100 years relevant to the theme of plant virus ecology and epidemiology include:-

  1. Virus spread by aphid (Broadbent, 1950; Watson et al., 1951, 1975; Elnagar & Murant, 1978; Tatchell et al., 1988); whitefly (Fargette et al., 1985), leafhopper (Soleimani et al., 2013), mite (Thresh, 1966), nematode (Harrison, 1964) and fungus (Rosner et al., 2006) vectors;
  2. Virus spread by contact (McKirdy et al., 1998);
  3. Seed transmission of nematode-borne (Lister & Murant, 1967; Murant & Lister, 1967; Hanada & Harrison, 1977), aphid-borne (Jones, 1988b; Jones & Proudlove, 1991), and contact-transmitted viruses (Wroth & Jones, 1992);
  4. Weeds as virus reservoirs (Tomlinson et al., 1970; Ramappa et al., 1998; Pallett et al., 2002);
  5. Virus or vector resistance deployment (Jones, 1979; Ferris et al., 1996);
  6. Virus resistance breakdown (Pelham et al., 1970; Thomas-Carroll & Jones, 2003);
  7. Effects of cultural practices on spread of aphid-borne viruses (Kendall et al., 1991; Jones, 1993, 1994; Difonzo et al., 1996; Sauke & Doring, 2004);
  8. Control of aphid-borne viruses by insecticides (Jones & Ferris, 2000) or mineral oil (Vidal et al., 2013);
  9. Control of nematode-borne viruses by nematicides (Harrison et al., 1963);
  10. Control of fungus-transmitted viruses by fungicides (Tomlinson & Faithfull, 1979);
  11. Forecasting virus epidemics (Harrington et al., 1989).

Molecular epidemiology and ecology

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

The simplicity of plant virus genomes makes them ideal subjects for molecular epidemiology and ecology studies. These provide detailed information of many kinds that were unavailable when biological assays or serological techniques were the only options. Molecular epidemiology and ecology studies assume that the genome sequences of virus isolates retain signatures that reflect their histories, give information on epidemic patterns, and provide an enhanced understanding of the ecological and evolutionary processes concerned. It brings new information, such as understanding of distant and rare events not discernible by traditional field approaches. However, the patterns it finds can only be interpreted if factors such as natural host range and method of transmission in the field are known (e.g. Traore et al., 2009). Moreover, sequencing and bioinformatics technologies are improving rapidly, facilitating the ability to collect high quality molecular data. Advantages, insights and applications that molecular epidemiology and ecology can provide when studying virus–plant pathosystems were discussed in several previous reviews (e.g. Thresh & Fargette, 2003; Fargette et al., 2006; Gibbs et al., 2008; Acosta-Leal et al., 2011; Malmstrom et al., 2011; Jones, 2014). They include improving the traceability of virus populations, producing information about epidemic patterns that cannot be revealed by traditional field investigations, establishing the risk of resistance breakdown, and testing the durability of virus or vector selective control measures. Examples of what has been achieved include papers by Garcia-Arenal et al. (2000), Desbiez et al. (2009), Lecoq et al. (2009, 2011), Traore et al. (2009), Olarte-Castillo et al. (2011), Thapa et al. (2012), Roossinck (2012) and Rodelo-Urego et al. (2013). Study of the way genetic diversity among plant populations affects virus epidemics showed how information from field studies employing molecular diagnostic tools can complement molecular studies on how diversity among virus populations influences virus epidemics (Pagan et al., 2012). An exciting time lies ahead for plant virus ecology and epidemiology as (a) the formerly sometimes disconnected traditional and molecular approaches to the discipline are increasingly brought together, and (b) the increasingly powerful molecular tools now appearing are deployed to provide fine details of virus genetic variation present within epidemics that were impossible to obtain previously (Jones, 2014).

Advances in understanding of virus–vector interactions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

The former assumption that as virus epidemics progress, arthropod vectors visit plants at random regardless of whether they are virus-infected or healthy has proven incorrect. Vectors are now known to respond differently to cues derived from healthy or virus-infected plants, natural enemies or environmental influences. These changes alter temporal and spatial virus spread patterns and need to be taken into consideration when predictive virus epidemic models are developed (Fig. 6).

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Figure 6. Disease triangles for non vector and vector-borne pathosystem scenarios. Arrows represent interactions occurring between the different triangle components. (From Jones & Barbetti, 2012).

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Presence of natural enemies of insect vectors can alter virus spread patterns in different ways. The aphid parasitoid Aphidius colemani of the vector Aphis gossypii enhanced spread of non-persistently transmitted CMV in cucumber plants, but limited spread of persistently transmitted Cucurbit aphid-borne yellows virus (genus Polerovirus) (Dáder et al., 2012). Jeger et al. (2011a) modelled effects of natural enemies on virus vector transmission. By increasing levels of virus transmission, presence of natural enemies can increase the rate of virus spread despite reducing vector population size. This suggested that biological control of arthropod vectors using parasitoid wasps in protected cropping situations might have unanticipated and negative effects in terms of increased virus spread. Jeger et al. (2011b) used a mathematical model linking the population dynamics of a vector–parasitoid system with virus transmission to investigate the effects of virus inoculation and acquisition rates, parasitoid attack rate and vector aggregation on disease dynamics across a wide range of parameter value combinations. Virus spread was found to increase with enhanced inoculation, acquisition and parasitoid attack rate, but decrease with high levels of vector aggregation.

Viruses can cause direct and plant-mediated indirect effects on their insect vectors by modifying their life cycles, fitness and behaviour. Direct virus–vector interactions that alter insect vector transmission occur when viruses circulate through their vectors' bodies remaining there throughout their lifespans. Moreno-Delafuente et al. (2013) studied persistent virus transmission in the tomato – B. tabaci – TYLCV pathosystem. Virus presence within its body directly influenced vector settling, probing and feeding behaviour in a way that enhanced transmission efficiency and spread. The interaction was mutually beneficial because B. tabaci fed more efficiently after TYLCV acquisition. However, this mutualistic relationship between B. tabaci and TYLCV only applied to biotype Q, biotype B and TYLCV having no mutualistic interaction (Pan et al., 2013). For this reason, the former biotype is displacing the latter biotype in different parts of the world. Similarly, with thrips transmission, the feeding behaviour of TSWV-infected male F. occidentalis was modified in a way that seems likely to influence virus transmission (Stafford et al., 2011).

One of the most intriguing current plant virus vector research fields concerns how virus infection is able to manipulate plant hosts to change insect vector behaviour thereby increasing virus spread. New information about this comes from studies showing that virus infection induces changes in plant hosts that alter the frequency and nature of host–arthropod vector interactions resulting in enhanced virus transmission. Mauck et al. (2012) analysed existing literature on insect vector transmission to test the hypothesis that non-persistently and persistently transmitted viruses both enhance vector attraction to infected host plants, but have contrasting effects on vector settling and feeding preference, and on vector performance. Non-persistently transmitted viruses tend to diminish host quality and therefore promote rapid dispersal, whereas persistently transmitted viruses tend to improve host quality for vectors and promote long-term feeding. Patterns consistent with these suggestions were found showing transmission mechanisms influence virus manipulative strategies.

Evidence that viruses induce changes in host plants that cause the insect vectors that transmit them to settle preferentially on infected plants was provided by several studies (e.g. Alvarez et al., 2007; Mauck et al., 2010), and was especially well documented for two pathosystems involving persistent aphid transmission: the wheat – Rhopalosiphum padi – BYDV pathosystem, and the potato – Myzus persicae – Potato leafroll virus (PLRV; genus Polerovirus) pathosystem (Bosque-Pérez & Eigenbrode, 2011). More recently, feeding preferences or behaviour of insect vectors were found to change after exposure to infected plants and virus acquisition (Stafford et al., 2011; Ingwell et al., 2012; Shestra et al.., 2012; Moreno-Delafuente et al., 2013; Rajabascar et al., 2014; Carmo-Sousa et al., 2014). Ingwell et al. (2012) studied BYDV transmission by R. padi in wheat. After acquiring virus from BYDV-infected plants, the aphids preferred to feed on healthy wheat plants. By contrast, non-viruliferous aphids preferred to feed on infected plants. Rajabascar et al. (2014) demonstrated that the same thing occurs with PLRV transmission by M. persicae in potato. Thus, aphid attraction to infected plants promotes virus acquisition from them while their attraction to healthy plants promotes virus transmission to them. This virus manipulation of aphid feeding preferences promotes virus spread. The explanation was that virus infection alters the concentration and relative composition of volatile organic compounds in host plants, such that virus-infected plants attract winged non-viruliferous aphids, but winged viruliferous aphids are attracted to healthy plants (Rajabascar et al., 2014). Plant-mediated indirect modifications that stimulate alterations in the behaviour or performance of their vectors when landing or feeding on virus-infected plants have also been reported for whitefly vectors (Jiu et al., 2007; Wang et al., 2012; Zhang et al., 2012).

Exciting new research is delivering knowledge of how viruses induce changes in infected plants that influence interactions between viruses and their vectors, and virus transmission from infected to new hosts (e.g. Cilia et al., 2012; Westwood et al., 2013; Zhou, 2013). For example, Westwood et al. (2013) studied the effects of CMV on aphid–plant interactions in Arabidopsis thaliana. Induction of feeding deterrence to M. persicae in CMV-infected A. thaliana resulted from direct or indirect interactions involving three of its gene products (the 1a, 2a and 2b proteins) with the host, or with each other. Interplay of these three viral proteins balanced the need of the virus to inhibit antiviral silencing. The 2a protein triggered defensive signalling leading to increased biosynthesis of a feeding deterrent chemical (4M13M) that inhibited aphid phloem ingestion and consequently discouraged its settling. Discouraging settling would increase CMV transmission to healthy plants.

New research is also providing novel information about how viruses can increase virus acquisition by sharing their host plants perception system. Martinière et al. (2013) studied non-persistent aphid transmission of Cauliflower mosaic virus (CaMV; genus Caulimovirus). Specialised transmission bodies formed within infected plant host cells take up CaMV. These transmission bodies respond instantly to vector presence on the host by rapid redistribution of their key components into micro-tubules throughout the cell. The transmission bodies are required for efficient virus acquisition. This research shows that by sharing their hosts' perception system CaMV can perceive aphid vectors either directly or indirectly.

Plant–virus interactions at the managed-natural vegetation interface

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

Rapidly expanding world trade moves cultivated plants away from their centres of domestication to other parts of the world, thereby dispersing previously localised viruses and virus vectors widely. In so doing, it exposes introduced cultivated plants and weeds to new encounter situations as they come into contact for the first time with indigenous viruses spreading from native plants growing at the managed and natural vegetation interface (Fig. 5E). Since such viruses have not co-evolved with their wild ancestors, damaging epidemics are likely to arise in the introduced plants. The same process exposes native plants to new encounters as they make contact with newly introduced viruses they never encountered before that spread to them from introduced cultivated plants or weeds (Fig. 5F). Moreover, new encounters involving viruses and plant species are becoming increasingly common because of rapidly increasing human activity, such as agricultural practices involving extensification, intensification and diversification, resulting from the need to maintain food security and feed the rapidly increasing human population (Thresh, 1980b, 1981a; Boss, 1992; Anderson et al., 2004; Fargette et al., 2006; Jones, 2006, 2009; Alexander et al., 2014).

New encounters provide new opportunities for rapid, adaptive virus evolution and host species jumps, thereby increasing the rate of invasion of introduced plants by indigenous viruses emerging from native plants, and of indigenous flora by introduced viruses (e.g. Fargette et al., 2006; Seal et al., 2006a,b; Varsani et al., 2008; Jones, 2009; Vincent et al., 2014). The process of virus emergence from natural vegetation to infect introduced cultivated plants is well documented, especially in the tropics and subtropics (e.g. Thresh, 1980b, 1981a; Bosque-Pérez, 2000; Morales & Anderson, 2001; Morales & Jones, 2004; Fargette et al., 2006; Morales, 2006; Varsani et al., 2008; Jones, 2009). Anderson et al. (2004) calculated that just under half (47%) of all emerging pathogens are viruses. This is because the simplicity of plant virus genomes allows viruses to adapt quickly to new hosts (Sacristan & Garcia-Arenal, 2008; Varsani et al., 2008; Tatineni et al., 2011; Bedhomme et al., 2012; Rodelo-Urego et al., 2013). As mentioned above, Begomoviruses in particular evolve rapidly making hosts jumps to species they have not met previously (e.g. Morales, 2006; Seal et al., 2006a,b; Legg et al., 2011; Navas-Castillo et al., 2011). Tospoviruses (see above) and potyviruses are other examples of plant virus groups that contain many economically important recently emerged viruses (e.g. Desbiez et al., 2009; Jones, 2009; Lecoq et al., 2009; Pappu et al., 2009). By contrast, the process of invasion of native plants by introduced viruses (e.g. McKirdy et al., 1994; Webster et al., 2007; Vincent et al., 2014) is much less well documented in most parts of the world (Fig. 5F). Further, although indigenous viruses are often considered benign when they infect plants growing in undisturbed natural vegetation, they do sometimes induce obvious symptoms and damage in infected plants growing in such situations (e.g. Jones & Fribourg, 1979; Cooper & Jones, 2006; Vincent et al., 2014). Also, abundance of virus resistance genes in wild ancestors of modern cultivated plants provides evidence of past battles between them and viruses that co-evolved with them (Cooper & Jones, 2006).

There is an increasing need to study viruses in natural ecosystems in areas of the world with rich but endangered floras to provide critical information on virus evolution and facilitate the development of effective strategies to conserve endangered populations of indigenous plants (Cooper & Jones, 2006; Jones, 2009; Vincent et al., 2014). Such studies also help to identify potential threats posed by indigenous viruses likely to cross the interface between natural and managed vegetation to infect introduced cultivated plants that subsequently might be distributed worldwide through the rapidly expanding world trade in plants and plant products. Alexander et al. (2014) suggested three priorities for future research at the managed and natural vegetation interface: (a) an increased effort to identify and describe plant virus diversity and distribution across agricultural and ecological boundaries; (b) multi-scale studies of virus transmission to develop predictive power in estimating virus propagation across landscapes; and (c) quantitative evaluation of the influence of viruses on plant fitness and populations in environmental contexts beyond crop fields.

Effects of climate change

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

During the 21st century, our planet's surface temperature is likely to rise by 2.1–2.9°C to 2.4–6.4°C for lowest and highest greenhouse gas emissions scenarios, respectively. Warming is expected to vary between regions with most occurring at high latitudes. Increasing global temperature is expected to cause sea levels to rise further, change the amount and pattern of rainfall precipitation, and cause expansion of subtropical deserts. Increases in the amount of precipitation are projected for high latitudes, but decreases in precipitation in most subtropical land regions. More frequent extreme weather events, including strong winds, heat waves, droughts and torrential rain, are predicted. Future tropical cyclones are expected to become more intense. Extra-tropical storm tracks are projected to move poleward, with consequent changes in wind, precipitation and temperature patterns (Lu et al., 2007; Metz et al., 2007; Pachauri & Reisinger, 2007; Parry et al., 2007; Solomon et al., 2007).

Knowledge of what alterations climate change is likely to cause to the prevalence of virus diseases in cultivated and wild plants, and the magnitude of the losses likely to result in different parts of the world, is of crucial importance. This importance arises from the need for food security as the world's population expands at a time when its capacity to increase production in many populous middle and lower latitude regions is projected to decline and climate insecurity challenges man's ability to control plant virus diseases effectively (Canto et al., 2009; Jones, 2009; Jones & Barbetti, 2012). Jones & Barbetti (2012) developed comprehensive climatic and biological frameworks and used them to determine the likely influences of direct and indirect climate change parameters on the many host, vector and viral pathogen parameters that represent the diversity of plant viral pathosystems. This analysis suggested that climate change is likely to alter diverse virus epidemic components in different ways, including altering host morphology, physiology and resistance to vectors or viruses, and vector and pathogen life cycles, abundance, diversity, reservoirs and inoculum. Their approach identified the international research data available worldwide and the many information gaps where research is needed in the future. With new encounter scenarios and vector-borne virus pathosystems, the complication of having to take into account effects of climate change parameters on emergence of previously unknown viruses and diverse types of vectors added significant extra variables. As climate change-induced temporal and spatial shifts in their distributions causes more newly introduced crops and weeds to meet indigenous vegetation for the first time, new encounters between cultivated and wild plants are projected to increase. This would accelerate the appearance of epidemics caused by (a) new or little understood viral pathogens that emerge from indigenous vegetation to threaten newly introduced cultivated plants, and (b) newly introduced viruses and vectors that arrive with newly introduced cultivated plants and invade natural plant communities. Furthermore, climate change was likely to diminish the effectiveness of control measures, such as some cultural control measures and temperature sensitive single gene resistance, and viral epidemics were projected to become less predictable, causing increasing difficulties in suppressing them successfully using current management technologies. In many instances, losses in cultivated plants and damage to natural vegetation resulting from virus diseases was likely to increase considerably with potentially serious consequence for world food security and plant biodiversity. Examples of the many types of research needed included to (a) identify the kinds of locations where climate change-induced temporal and spatial shifts in crop, virus reservoir and weed host distributions are likely to foster new encounter scenarios that result in damaging epidemics caused by emerging viral pathogens; (b) understand which climate change parameters accelerate evolution of generalist virus pathogens, including their ability to make host species jumps, become more virulent and overcome host resistances; (c) devise models to help identify where new encounters that result in virus emergence are likely to occur in a given locality, and the probability that damaging virus epidemics of emerging viruses would occur as a consequence of climate change; (d) understand the likely influences of different climate change scenarios on epidemics in wild plant communities arising from new encounters with introduced viruses or vectors; and (e) investigate the influence of climate change parameters, particularly enhanced temperature, where viral epidemics are occurring within only one individual component species within plant species mixtures.

Opportunities from technological innovation

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

The current epoch of rapidly advancing technological innovation provides many opportunities to future research on plant virus ecology and epidemiology. For example, recent innovations in remote sensing and precision agriculture provide valuable information about (a) virus epidemics occurring at continental, regional or district scales (via satellites) and within individual crops (mostly via lightweight unmanned aerial vehicles), and (b) exactly where to target control measures. Improvements in information systems and innovations in modelling improve (a) understanding of virus epidemics and ability to predict them, and (b) delivery to end-users of advice on control measure deployment. Advances in analysis of spatiotemporal virus spread patterns increase understanding of how virus spread occurs. Also, the ever increasing sophistication, diversity and availability of molecular tools suitable for virus detection, quantification and analysis is providing many opportunities to collect and analyse new types, and ever increasing amounts, of data about the genetic variability of virus populations, and how this variation influences what then occurs in virus-infected plant populations subject to diverse climatic and other environmental variables. The discipline is entering an exciting era in which such advances provide the means to (a) greatly streamline the collection and processing of standard ecological and epidemiological data sets; (b) collect and process entirely new types of ecological and epidemiological data; (c) enhance knowledge by making available many new insights into why and how virus spread occurs differently when circumstances change; and (d) provide much more effective prediction and decision support over when to deploy carefully targeted interventions that suppress damaging epidemics effectively on continental, regional, district or within-field scales (Jones, 2014).

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References

Since its early beginnings, plant virus ecology and epidemiology has come a very long way as a research discipline. Over the last 100 years, the many publications in the Annals of Applied Biology on different aspects of the subject have played a crucial role in its development. A revealing picture of the way understanding advanced from nothing to what it is today is provided by four reviews written to celebrate the 50th (Bawden, 1955; Smith, 1955), 75th (Harrison, 1980) and 100th (Harrison & Robinson, 2005) anniversaries of the AAB. These summarise progress in plant virus research over three different eras, including emphasising major milestones in the development of plant virus ecology and epidemiology as a discipline. Moreover, a wealth of information on the subject can be found in the journal in other reviews and its many original research articles. Additional reviews and research papers in the journal are likely to continue to provide such information well into the future.

Since 1980, the International Committee on Plant Virus Epidemiology (ICPVE), and in 2008–2012 the Plant Virus Ecology Network (PVEN), contributed considerably to the discipline's development through the International Symposia (ICPVE) and Conferences (PVEN) they sponsored, and the ICPVE through its a books and special journal editions. That plant virus ecology and epidemiology continues to thrive as a discipline today owes much to the inspiration provided over many years by ICPVE foundation chairman Mike Thresh, a former Programme Secretary of the AAB.

Since 1979, application of new molecular techniques has greatly accelerated the rate of progress in understanding factors underlying the discipline. The many benefits that molecular epidemiology and ecology provides include improving the traceability of virus populations, producing information about virus epidemic patterns not revealed by traditional field investigations, establishing the risk of virus resistance breakdown, and testing the durability of virus or vector selective control measures. An intriguing future lies ahead for the discipline's researchers, and the implications of their findings are likely to be far reaching, as (a) traditional and molecular approaches to plant virus ecology and epidemiology are combined to increasing extents, and (b) increasingly sophisticated molecular tools are employed to provide fine details of genetic variation present within virus populations.

Insect vectors respond differently to cues derived from natural enemies, healthy or virus-infected plants or environmental influences. These changes alter temporal and spatial virus spread patterns and all need to be taken into consideration when predictive virus epidemic models are developed. Viruses cause direct and plant-mediated indirect effects on insect vectors by modifying their life cycles, fitness and behaviour. Virus presence inside their bodies can directly influence vector settling, probing and feeding behaviour in a way that enhances virus transmission efficiency and spread. However, one of the most intriguing current research fields concerns plant-mediated indirect manipulation of insect vector behaviour that encourages virus spread. Such manipulation stimulates changes in behaviour of vectors when landing or feeding on virus-infected plants. Vector attraction to infected plants promotes virus acquisition while their attraction to healthy plants promotes virus transmission. Furthermore, new research is delivering an understanding of how viruses induce biochemical changes in infected plants that influence interactions between viruses and their vectors, and virus transmission from infected to new hosts. New research is also providing information about how viruses can increase virus acquisition by sharing their host plants insect perception system. Specialised transmission bodies that form within virus-infected cells and respond instantly to vector presence were required for efficient virus acquisition.

In the future, a continued increase in new encounters between viruses and both cultivated and wild plants, and alteration in the distribution of virus vectors, is inevitable. This is because of (a) rapidly increasing international trade in plants and plant products, and the need to expand the area of land growing food crops to feed the rapidly growing human population, and (b) the anticipated temporal and spatial shifts in world regions producing cultivated plant species due to global warming. Such acceleration in the rates of new encounters and redistribution of efficient virus vectors on a global scale would result in acceleration in the rate of emergence of indigenous viruses that damage cultivated plants and the rate of invasion of native plants by introduced viruses. This process is a very serious issue not only for effective production of mankind's food, fibre and medicinal plants, but also for maintenance of global plant biodiversity. Forewarned is forearmed so instead of merely reacting after damaging epidemics of plant viruses appear in cultivated and endangered native plants, there is an urgent need to understand how they do this and be able to anticipate their occurrence. To obtain an understanding of, and ability to foresee, these kinds of events will require a major research effort into the future.

The rapid pace at which the climate is currently changing on planet earth poses a serious threat to mankind and many of its other species. This is exacerbated by the rapid increase in the human population and the consequent need to clear ever increasing amounts of natural vegetation to satisfy its requirements. Understanding what alterations climate change is likely to cause to the occurrence and importance of virus disease epidemics in cultivated plants and the remaining natural vegetation in different world regions is therefore of great importance. Gaining such an understanding is made more difficult by the effects of climate alterations on behaviour of different kinds of invertebrate and fungal vectors, the ease by which previously unknown viruses can emerge and the increasing impact of mankind's activities. However, when compared with the magnitude of the worldwide research effort to assess the likely impacts of climate change on the severity of fungal disease epidemics and insect pest outbreaks, there has been lamentably little focus on research to determine the magnitude of the threat from diseases caused in diverse plant virus pathosystems under different climate change scenarios. It is high time for this situation to be rectified, especially for food insecure regions of the world.

Rapidly increasing technological innovation is providing an increasingly important means to help address the threat plant virus disease epidemics pose to future food security and the diversity of the planet's remaining vegetation. This innovation is making available new techniques that provide considerable opportunities to magnify and accelerate the achievements of worldwide research on plant virus ecology and epidemiology. If employed flexibly, innovatively and intelligently, new transformative technologies can ensure much more efficient and intelligent use of experience, skills and information when undertaking research to enhance understanding of the subject, and ensure correct decisions are made over which control measures to employ. Increasing technological innovation will ensure that the subject has a very exciting future!

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Past Annals of Applied Biology review articles
  5. Annals of Applied Biology research papers
  6. Molecular epidemiology and ecology
  7. Advances in understanding of virus–vector interactions
  8. Plant–virus interactions at the managed-natural vegetation interface
  9. Effects of climate change
  10. Opportunities from technological innovation
  11. Conclusions
  12. Acknowledgements
  13. References