The expanding field of plant virus ecology: Historical foundations, knowledge gaps, and research directions

Virus Research 159 (2011) 84–94

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The expanding field of plant virus ecology: Historical foundations, knowledge gaps, and research directions Carolyn M. Malmstrom a,∗ , Ulrich Melcher b , Nilsa A. Bosque-Pérez c a

Department of Plant Biology, Michigan State University, East Lansing, MI, 48824-1312, USA Department of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK, 74078-3035, USA c Department of Plant, Soil and Entomological Sciences, University of Idaho, Moscow, ID, 83844-2339, USA b

a r t i c l e

i n f o

Article history: Available online 19 May 2011 Keywords: Virus Ecology Ecosystem Vector Nature Diversity

a b s t r a c t Plant viruses are widespread in nature, where they operate in intimate association with their hosts and often with vectors. Most research on plant viruses to the present has focused on agricultural systems (agronomic and horticultural) and viruses that are pathogenic. Consequently, there is a dearth of fundamental information about plant virus dynamics in natural ecosystems and how they might differ from or be influenced by virus interactions in managed systems. Key questions include under what conditions the influence of virus on host fitness is negative, neutral, or positive and the extent to which this relationship is influenced by ecosystem properties. To address these critical knowledge gaps, the expanding field of plant virus ecology seeks to examine (i) the ecological roles of plant-associated viruses and their vectors in managed and unmanaged ecosystems and (ii) the reciprocal influence of ecosystem properties on the distribution and evolution of plant viruses and their vectors. In this work, plant virus ecology draws on the achievements of epidemiology and extends the research focus to new ecological arenas. Here we provide an historical perspective and highlight key issues and emerging research directions. We suggest that there is broad need to (i) integrate consideration of plant viruses into ecological research and theory, in which viruses have generally been overlooked, and (ii) to expand ecological perspectives in virology to include new methods and disciplines in ecology, such as ecosystem ecology. Studies of plant–virus–vector interactions in nature offer both opportunities and challenges that will ultimately produce multi-faceted understanding of the role of viruses in shaping ecological and evolutionary dynamics. © 2011 Elsevier B.V. All rights reserved.

1. Plant virus ecology: an expanding field Plant viruses are widespread in nature where they operate in intimate association with their hosts and have tremendous potential to cause unanticipated ecological effects (Anderson et al., 2004; Woolhouse et al., 2005). As transportable genetic units, viruses flow through plant communities and across landscapes, evolving as they interact with each other, with their hosts, and often with vectors. The capacity of plant viruses to cause disease and to recombine with each other and with host genomes has led to several urgent questions for society. These questions include how to (i) predict the nature of emerging pathogens and their response to environmental change (Committee on the National Ecological Observatory Network, 2003; Canto et al., 2009); (ii) prevent misuse of viruses in bioterrorism (Madden and Wheelis, 2003); and (iii) assess risk of

∗ Corresponding author. Tel.: +1 517 355 4690; fax: +1 517 353 1926. E-mail address: [email protected] (C.M. Malmstrom). 0168-1702/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.virusres.2011.05.010

recombination with endogenous viruses or with viral transgenes in resistant plants (Thompson and Tepfer, 2010).Our ability to answer these questions is hampered by a dearth of basic information about the extent and influence of plant viruses in natural ecosystems and the reciprocal influence of natural ecosystems on the dynamics and evolution of plant viruses. In terrestrial ecosystems, studies have increasingly found evidence of virus infection in a broad range of wild plant hosts (e.g., Duffus, 1971; Bosque-Pérez, 2000; Guy et al., 1987; MacClement and Richards, 1956; Marais et al., 2010; Melcher et al., 2008; Muthukumar et al., 2009; Polischuk et al., 2007; Raybould et al., 1999; Robertson, 2005; Roossinck et al., 2010; Saunders et al., 2003; Webster et al., 2007), yet the ecological and evolutionary influences of these viruses remain largely unexplored. To address this critical knowledge gap, the field of plant virus ecology is re-emerging from its historical roots as an expanding scientific frontier that seeks to examine (i) the ecological roles of plant-associated viruses and their vectors in managed or unmanaged ecosystems; and (ii) the reciprocal influence of ecosystem properties on the distribution and evolution of plant viruses and vectors.

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2. Historical foundations The history of plant virus ecology reflects the trajectory of much of modern biological science, which developed from roots in the 18th century Enlightenment, produced field-defining discoveries in the 19th–20th centuries, and then accelerated in the 21st century, spurred by technological innovation in genomics, computation, and geospatial analysis. As a field, modern plant virus ecology represents a confluence of ideas contributed by several biological disciplines, including virology, epidemiology, ecology, and entomology. During the last 150 years, exchange between these disciplines has been only intermittent, fluctuating as a function of intellectual currents and societal context. This history of intermittent exchange between disciplines that have otherwise developed separately has produced both major accomplishments and profound gaps that remain evident in plant virus ecology today. The ironic result is that until recently much of the driving energy for plant virus ecology came from work in virology and entomology, driven by pioneering scientists who saw the need for taking an ecological perspective even as their fields became increasingly reductionist with the rise of molecular approaches in the 1980s. In addition, the limited exchange between disciplines meant that the field of ecology – a field known for championing the importance of biodiversity – developed with little consideration of an entire sector of the web of life. Reconnection between virology and ecology (as between virology and evolution (Forterre, 2003)) thus promises to produce powerful advances in both basic and applied biology. 2.1. The beginnings of virology and ecology As true for many other biological phenomena, symptoms of virus infections in plants were observed for centuries before modern science began to study the agents and mechanisms involved. For example, as early as the 8th century, symptoms of what is now known to be a geminivirus infection were noted in Eupatorium in Japan (Saunders et al., 2003). Then, in the 19th and early 20th centuries, rising intellectual ferment produced ideas and techniques that spawned new scientific fields, including both virology and ecology. Virology as a field commonly is considered to have been born in the 1890s, when the Russian scientist Dimitri Ivanovsky and the Dutch microbiologist and botanist Martinus Willem Beijerinck independently used filtration experiments to demonstrate that the causal agent of tobacco mosaic disease was smaller than a bacterium (Scholthof et al., 1999). By 1935, Wendell Stanley had demonstrated the particulate nature of viruses through his crystallization of Tobacco mosaic virus (TMV) (family Virgaviridae: genus Tobamovirus) coat protein, and many putative viruses had been identified in plants, animals, and bacteria (e.g., Holmes, 1939). Thus began a lively period of debate about how to conceptualize viruses and their relation to life – were they alive or not? (Villarreal, 2004) – and an urgent need to understand virus dynamics and control disease in humans, livestock, and crops. During the same period in the late 19th century and early 20th centuries, the field of ecology – energized by Darwin’s 1859 publication of On the Origin of Species By Means of Natural Selection – began to coalesce from roots in earlier explorations of natural history and biogeography. “Oekologie” as a term was first used by the German zoologist Ernst Haeckel in the 1860s to describe the study of the “multifaceted struggle for existence” that Darwin had delineated in his seminal work (Kingsland, 1991). The young field built equally on work by scientists such as the German explorer Alexander von Humboldt, who examined environmental distributions of organisms (Von Humboldt, 1805), and by chemists such as Antoine Lavoisier whose studies of stochiometry (Lavoisier, 1789) laid the foundation for modern ecological studies of biogeochemical cycling. In a period when natural history was sometimes

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considered the “domain of women and children and weak-minded persons” (Cox (1893) as described in Kingsland (2005)), ecological studies aimed to progress from descriptive work to more rigorous experimental and mathematical analyses. With these aims in mind, the British Ecological Society (BES) was formed in 1913 and the Ecological Society of America (ESA) in 1915. As Kingsland (1991) describes it, these early ecologists promoted “a dynamic, experimental approach to the study of adaptation, community succession, and population interactions.” In 1935, as Stanley crystallized TMV, the British botanist Arthur George Tansley (1935) helped set the course of future ecological work by introducing the term “ecosystem.” 2.2. Connection and divergence in the first half of the 20th century As the 20th century advanced, virologists and entomologists sought to map the biological complexity of virus–vector–host relations – deemed the ‘inseparable ecological trinity’ (Carter, 1939) – by taking an ecological perspective in their search for sources of infection that was plaguing crop fields. One of the most dramatic cases was that of the sugar-beet leafhopper (Circulifer tenellus) found in the early 20th century to initiate epidemics of beet curly top disease in sugar beet fields in the southwestern United States (Carter, 1930), for which the casual agents were later identified as a complex of Curtoviruses (family Geminiviridae). Work by multiple researchers, including Carter, R. Piemeisal, and others, established that rangeland degradation promoted growth of annual weeds that amplified populations of leafhoppers, which then migrated over sometimes long distances to sugarbeet fields in spring as their desert hosts senesced (Piemeisel et al., 1951; see also summaries in Carter (1961) and Thresh (1981)). However, while virology was developing this ecological perspective, the field of ecology turned away from questions of agricultural application to focus more intently on natural ecosystems. Even though agricultural questions helped inspire quantitative ecological methods – the oldest ecological experiment in existence is the Park Grass Experiment at Rothamsted, England, begun in 1856 to investigate the effects of fertilizer on grass yield (Silvertown et al., 2006) – ecology as a field remained focused on wild systems. By 1938, when the combined effects of prolonged drought and poor agricultural practices had turned much of the American prairie lands into a “Dust Bowl” of eroded fields (Cook et al., 2009), the then-president of the Ecological Society of America, Herbert C. Hanson, was so troubled by the growing gap between ecology and agriculture that he used his annual ESA dinner address to exhort his fellow ecologists to address applied questions (Hanson, 1939). One of the main examples of relevance he offered was the case of beet curly top disease. However, despite the urgings of Hanson and others, the gulf between ecological studies of natural and managed systems persisted. As the fields of ecology and virology (and plant pathology as a whole) developed into the mid20th century, exchange between them was surprisingly limited, as evident from the paucity of references to viruses in the ecological journals of that period (for example, there are only four citations of “ecolo*” in journal and “virus*” in topic for 1940–1949 in the ISI database). 2.3. A widening separation Technological and intellectual advances that began in the second half of the 20th century then widened the separation between the fields of plant virology and ecology for some time, despite the continuing efforts of individuals to bridge the divisions (Harper, 1990; Thresh, 1981). The development of modern molecular methods ultimately directed much of virology towards a powerful but

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reductionist approach in which the ecological perspective of earlier studies was diminished and many plant virologists became molecular biologists (Sequeira, 2000). As several authors well outline (Zaitlin and Palukaitis, 2000; Hull, 2002; van der Want and Dijkstra, 2006), this trajectory began gradually, perhaps starting with the demonstration in Turnip yellow mosaic virus (family Tymoviridae: genus Tymovirus) that RNA was critical for viral infectivity (Markham and Smith, 1949). Brakke’s subsequent development of density gradient centrifugation for virus purification enabled the characterization of many new viruses (Brakke, 1951, 1953), which advanced with use of electron microscopy in the 1960s (e.g., Harrison and Nixon, 1960) and with serological methods and nucleic acid hybridization in the late 1970s–1980s (e.g., Clark and Adams, 1977; Hull, 2002). Kary Mullis’s invention of PCR in 1984 marked the advent of the recent molecular era in which understanding of viral mechanisms expanded greatly (Zaitlin and Palukaitis, 2000). While molecular discussion dominated the virology literature, the ecological perspective persisted within the smaller subdiscipline of plant virus epidemiology, marked by the 1978 initiation of the Plant Virus Epidemiology Committee of the International Society for Plant Pathology (ISPP) by Mike Thresh et al. and the first Plant Virus Epidemiology Symposium, held in 1981 in Oxford, UK. Variously defined as the study of disease in host populations (J.M. Thresh, personal communication) or the study of patterns of disease in space, time, and within populations (Waggoner and Aylor, 2000), plant epidemiology draws on ecological perspectives to understand and model complex pathosystems, typically those with deleterious effects in plants of economic importance (Plumb and Thresh, 1983; Jones et al., 2010). The power of plant virus epidemiology is demonstrated in numerous scientific achievements, from the 20th century studies of Beet curly top disease in the US to modern cases in Africa (Traoré et al., 2009). Its practitioners have undertaken some of the most detailed studies of exchange of viruses among managed and natural systems in seeking to understand factors that drive disease emergence and spread (e.g., Bosque-Pérez, 2000; Fargette et al., 2006). With the ecological methods and perspectives of epidemiologists, it is therefore not surprising that, to many, the fields and nature of ecology and epidemiology are nearly synonymous. In one of the most respected plant virology texts, for example, Hull (2002, p. 556) exhorts readers to “distinguish between the terms epidemiology and ecology, which in many papers have been used interchangeably.” After defining ecology to be “the factors influencing the behavior of a virus in a given situation” and epidemiology to be “the study of the determinants, dynamics, and distribution of viral diseases in host populations,” Hull thereafter considers the two together. However, part of the legacy of the 20th century is that the field of ecology developed new approaches and new sub-disciplines during this period of limited exchange with virology. Among these were ecosystem ecology, landscape ecology, and restoration ecology. Ecosystem ecology is the largest and most developed of these areas, representing a major subdivision of ecology on par with population and community ecology. Although its name may suggest that its practitioners describe ecosystem types, ecosystem ecology is in fact the quantitative study of the exchange of energy and matter between organic and inorganic compartments, and its heritage traces to Lavoisier’s 18th century work in chemistry. From these roots, early studies of plant ecophysiology led to more complex ecosystem analyses after the Second World War and to the 1953 publication of Eugene Odum’s landmark text, Fundamentals of Ecology, seen by many to mark the beginning of ecosystem ecology. Subsequent key accomplishments in ecosystem ecology included the initiation of watershed-scale experiments in biogeochemical cycling in the 1960s that stimulated later development of long-term ecological research sites in the US and elsewhere (Bormann and

Likens, 1967). More recently, ecosystem ecology has driven development of global ecology and models of Earth system function (e.g., Mooney, 1999) that inform global assessments of anthropogenic impact on climate and its consequences (IPCC, 2007). Like that of sub-disciplines in plant virology, the rise of ecosystem ecology was influenced by technological progress, which included advances in nuclear energy and chemistry, as well as by reactions to technology-induced environmental problems such as those documented in Rachel Carson’s seminal work, Silent Spring (1963). But because it matured as a field during a period of limited exchange with virology, ecosystem ecology had little call to consider the contributions of viruses in its analyses and much of virology has only a limited view of the approaches and contributions of this field. Other fields of ecology have also been both limited in, and potentially limited by, the dearth of exchange with plant virology. For example, landscape ecology, a field that emerged in the 1980s propelled in part by advances in geospatial technology, has had little interchange with virology and virus epidemiology until recently (Turner, 2005; Moslonka-Lefebvre et al., 2011). Likewise, landmark studies of biodiversity (e.g., Myers et al., 2000) that have guided efforts to conserve and restore degraded ecosystems have been conducted in the virtual absence of information about plant virus diversity, distribution, and influence in nature. 2.4. Reconnection As the 21st century begins, further developments in science and changes in societal context provide new opportunities for plant virology and ecology to reconnect and to address knowledge gaps that are a legacy of disciplinary separation in the previous century. Advances in molecular biology are generating renewed interest in questions of complex systems – now termed “systems biology” (Kitano, 2002). Likewise, genomic tools and molecular approaches are now common in population and community ecology (e.g., Snoeren et al., 2007). Ecosystem ecology, which once seemed far removed from virology, has been stimulated by recent studies of viruses in marine systems to consider the influence of these tiny microorganisms on carbon cycling and other key processes (Suttle, 2007). In parallel, virology and plant pathology now rely on ecosystem models to provide potential climate change scenarios (Anderson et al., 2004). Within the field of ecology as a whole, disease ecology is of increasing interest (e.g., Gilbert, 2002; Parker and Gilbert, 2004; Smith et al., 2006; Plowright et al., 2008; Archie et al., 2009; Alexander, 2010; Hawley and Altizer, 2011), and there is greater acceptance of the view that viruses are important taxa that are likely to provide critical insights in ecology and evolution (Villarreal, 2005; Zimmer, 2011). 3. Knowledge gaps and opportunities for reintegration of plant virology and ecology To help accelerate the reintegration of plant virology and ecology, the international Plant Virus Ecology Network (PVEN) was founded in 2007 by U. Melcher, C. Malmstrom, and colleagues, with initial funding from the US National Science Foundation. The PVEN has sponsored four conferences, including one jointly arranged with the Plant Virus Epidemiology Committee of the International Society for Plant Pathology (ICPVE). The two groups and others are now collaborating to foster and accelerate research on the ecology of plant viruses across both managed and natural ecosystems. Key aims are to (i) uncover the basic principles that mediate interactions among plants, viruses, vectors, and ecological factors across varied ecosystems; (ii) assess the distributions and genetic and ecological characteristics of established and emerging plant viruses globally;

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and (iii) evaluate the ecosystem consequences of plant virus activity and the reciprocal influence of ecosystem properties on plant virus dynamics. In this work, plant virus ecology builds on the achievements of plant virus epidemiology and extends the research focus to new ecological arenas. It seeks necessarily to foster interdisciplinary collaboration and integration of molecular, ecological, and quantitative approaches. Major accomplishments in plant virus ecology and the call for increased attention to this area have been well described by virologists (e.g., Thresh, 1991; Cooper and Jones, 2006) and some ecologists (e.g., Harper, 1990), over recent decades. Here we highlight persistent gaps in knowledge that have developed as a consequence of the limited exchange between the fields of virology and ecology during the last century. We believe there are three broad knowledge gaps that require attention:

(1) Despite their prevalence in nature, plant viruses have been considered in only a few ecology studies and have not been integrated into most ecological theory, as demonstrated by their near total absence in most current ecology textbooks. This gap developed partly because ecology as a field had reduced its interest in descriptive studies of natural history and taxa substantially before viruses were recognized as a key sector of the web of life and their rich diversity had begun to be catalogued. Incorporation of viruses into ecological understanding will require intellectual investment but is likely to bring substantial rewards. (2) The conceptualization of the field of ecology by many plant virologists and epidemiologists has been narrowed both by an historical focus on factors driving the emergence of viral diseases in plants of economic importance and by reduced opportunity to interact with central modern subdisciplines, such as ecosystem ecology. These gaps are the predictable outcome of limitations in exchange between virology and ecology over the last century. As Cooper and Jones (2006) note, “[u]ntil about 20 years ago, ecologists and plant virologists rarely if ever worked together.” Expanding inter-disciplinary collaborations will speed reintegration of plant virus ecology and promote consideration of virus influence in all ecological arenas. (3) Understanding of virus diversity and influence is much more limited in natural ecosystems than in agricultural ones, in large part due to the 20th century separation of basic and applied life sciences. In this era, wild plants were considered in virology largely as reservoirs of infection for crops, not as the primary subject of study (Cooper and Jones, 2006; Elena, 2011), whereas ecological disciplines examining natural communities rarely considered plant viruses (Harper, 1990). Moreover, many researchers across disciplines assumed that viruses infected natural vegetation inconsequentially, in part based on the view that viruses in nature usually co-evolve with hosts to a state of reduced virulence or aggressiveness. As data have accumulated, however, such assumptions have been questioned. It has become increasingly evident, for example, (i) that viruses are widespread in wild plants (MacClement and Richards, 1956; Hammond, 1981; Fargette, 1982; Guy et al., 1987; Nienhaus and Castello, 1989; Power and Remold, 1996; Raybould et al., 1999; Bosque-Pérez, 2000; Garrett et al., 2004; Cooper and Jones, 2006; Jones, 2009; Muthukumar et al., 2009; Pagan et al., 2010a,b) and phytoplankton (Clasen and Suttle, 2009); (ii) that virus influence on such hosts spans a range from fitnessreducing (e.g., Kelley, 1994; Remold, 2002; Malmstrom et al., 2005a, 2006) to fitness-enhancing (Márquez et al., 2007; Xu et al., 2008); and (iii) that selective forces drive moderation of virulence only under some circumstances (Ewald, 1995; Levin, 1996).

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4. Perspectives and emerging research directions As a result of new insights, there is growing agreement that to understand and predict the dynamics of plant viruses and their evolution, research must consider virus influence not only in agriculture,1 but also in nature. To do otherwise would be to consign a large part of virus biology to a “black box” from whence epidemics on occasion arise, an approach that is clearly unacceptable to a society that needs to conduct virus-related risk assessments. It is likely that the extent of virus influence in nature has been substantially underestimated. Findings in wild plant communities (Pagan et al., 2010a; Raybould et al., 1999), such as those in the Guanacaste conservation area of Costa Rica (ACG) (Roossinck et al., 2010) and the Tallgrass Prairie Preserve in Oklahoma, USA (TPP) (Melcher and Grover, 2011), indicate that while almost half of such wild plant specimens probably contain viruses, virus infection may not be readily associated with the display of distinctive symptoms of the type seen in crops (e.g., obvious foliar discoloration), and thus may have been overlooked. Indeed, these areas have yielded evidence of hundreds of viruses of which only 5% were already known. These results suggest that there are many plant viruses as yet undiscovered in nature and that determining their influence on host fitness likely will require techniques more rigorous than simple visual inspection. 4.1. Increasing interdisciplinary collaboration To assess virus effects in natural settings, virologists increasingly collaborate with plant ecologists, who bring complementary skills and expertise. Trained to work at scales ranging from whole plants to ecosystems, plant ecologists can help identify the emergent properties of, and resolve mechanisms within, complex systems. Collaboration with virologists also benefits plant ecologists. Although a growing area of ecological research, disease ecology has emphasized readily identifiable plant pathogens, such as fungi (Alexander, 2010); virus detection and identification usually requires ELISA, quantitative PCR, or other molecular methods that initially may seem daunting (e.g., Remold, 2002). In this arena and with questions of molecular and biochemical mechanisms, virologists can contribute much valuable expertise. 4.2. Differences in characteristics along the range of ecosystems from agricultural to wild Globally, ecosystems range from highly mechanized agricultural landscapes to near-pristine wild communities, with many intermediates. As plant virus ecology seeks to integrate understanding from agricultural and natural science, it is useful to consider how ecological characteristics differ along this spectrum of ecosystems, and how such differences both provide research opportunities and necessitate methodological adjustment. Central differences reflect the increased complexity evident in most natural ecosystems and include differences in host and virus species, the age structure of host populations, diversity patterns, and environmental stresses. Because of these differences, researchers moving from studies of virus dynamics in agricultural systems to those in more natural communities are likely to find new classes of questions to pursue, as well as a need to adapt research strategies to the new settings. The next sections highlight some key issues and emerging research directions at several scales: molecular to population-level, community and ecosystem, and regional to global. The impact of human activity on plant–virus interactions is then considered.

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Defined here in the broad sense to include agronomy, horticulture, and forestry.

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4.3. Molecular to population-level interactions Reflecting the historical focus of plant virology, current understanding of plant–virus dynamics is greatest for molecular to population-level interactions and much greater for cultivated host plants than for non-cultivated, wild or weedy species. In the future, understanding of key issues such as the mechanisms determining host plant resistance are likely to be extended to wild plants and links between molecular mechanisms and ecological consequences will be explored. As the research focus extends from managed to natural systems, it is useful to consider differences along this gradient in species identities and population structures, and the need for studies of virus influence on plant demography. 4.3.1. Novel hosts and viruses Most information about plant viruses comes from studies of those that infect economically important hosts or a few other ‘model’ species, such as Arabidopsis thaliana. However important to humanity, this list of species is relatively short and encompasses only a small fraction of plant life on Earth. In agriculture, for example, species of just three genera – Triticum, Zea, and Oryza – provide 43% of human daily calorie consumption (FAO, 2007). Lists of crop species are dominated by annual plants from a few key families including Asteraceae, Cucurbitaceae, Fabaceae, Poaceae, and Solanaceae. In nature, in contrast, there are more than 257,000 angiosperm species from 451 families, 600 coniferous species, and some 18,000 non-vascular terrestrial species (Judd et al., 2008; Angiosperm Phylogeny Group, 2009), for almost all of which nothing is known about their interactions with viruses. At present, novel viruses are being discovered rapidly in wild hosts in diverse natural ecosystems (Polischuk et al., 2007; Robertson, 2005; Marais et al., 2010), and such discovery has been accelerated by metagenomics techniques that permit sequencing of presumptive viral nucleic acid without prior knowledge of what viruses were present or with which organism they are associated (Breitbart et al., 2004; Suttle, 2005; Thurber et al., 2009). Using deep sequencing, several laboratories discovered that small RNAs of infected plants are rich in viral sequences (Donaire et al., 2009; Kreuze et al., 2009; Pallett et al., 2010; Qi et al., 2009). Two complementary approaches have been used for sequencing viral genomes from numerous samples of specific wild plants. In one, double-stranded RNA (dsRNA) was converted to dsDNA for random sequencing (Roossinck et al., 2010). In a second, nucleic acids extracted from virus-like particle fractions of plant homogenates were converted to dsDNA for sequencing (Melcher et al., 2008; Muthukumar et al., 2009). As exploration continues, the suite of viruses that infect cultivated plants, representing the vast majority of known plant viruses (Wren et al., 2006), is beginning to seem distinct from that found in natural communities. For example, in studies in the ACG in Costa Rica and the TPP in Oklahoma, the proportions of virus families identified differed significantly from those represented by recognized crop pathogens. For example, few viruses of the Potyviridae or the Begomoviridae were detected in the prairie samples, despite being abundant crop pathogens in that region (U. Melcher et al., unpublished). Differences between viruses of cultivated and noncultivated plants are also indicated by the suggestion that the diversity of currently known plant viruses arose thousands of years ago near the dawn of agriculture (Duffy and Holmes, 2008; Gibbs et al., 2008). Such rapid evolution is supported by estimates of the accumulation rate of mutations in laboratory experiments (Ge et al., 2007). In contrast, phylogenetic studies suggest that virus divergences coincide with those of their plant hosts (Lartey et al., 1996; Wu et al., 2009) or their arthropod vectors (Karasev, 2000). Future studies of novel viruses in wild hosts are likely to yield unexpected insights into virus–host interactions at multi-

ple scales. Of particular interest are the nature of the interactions between viruses and long-lived perennial plants, which are underrepresented in agricultural systems and yet dominant in nature. However, greater resource investment may be required to help research programs overcome costs associated with the development of new wild model systems. 4.3.2. Structure of host populations In nature, host populations typically have greater genetic diversity and more complex age structures than populations in agroecosystems, particularly in regions where crops are grown as monocultures of genetically similar or identical plants maintained by human selection. In wild communities, in contrast, plant genomes are under natural selection that may favor persistence of multiple alleles and emergence of new ones. Understanding the role of genetic diversity in controlling patterns of pathogen emergence and impact in nature has the potential to provide new insights for crop management. For instance, analogous work with fungal pathogens showed that introducing within-field genetic diversity to rice crops allowed growers to discontinue the use of fungicidal sprays within two years (Zhu et al., 2000). The greater complexity of age structures in natural communities offers opportunities to explore new questions – e.g., how does the movement of viruses between young and mature plants in the same population influence virus selection and host population dynamics? It also can make it more difficult to assess the influence of viruses on host fitness. In plantings of an annual crop, assessing fitness effects may be more straightforward because all individuals are the same age. Against this uniform background, individuals negatively impacted by a pathogenic virus may be notably smaller and thus easily identified. In a natural community where seedlings, young plants, and mature adults coexist, the effects of virus infection can be confounded with those of age and other possible negative impacts as determinants of plant size; thus, small plants may be small because they are infected with a virus, or simply because they are younger or have experienced another negative influence. Consequently, estimates of virus impact on plant fitness in nature based on field observations alone provide only very limited information. Best tests of fitness effects rely instead on results of direct inoculations of plants in the field or on manipulations of virus pressure under field conditions. 4.3.3. Need for studies of demographic impact Studies of virus influence on the demography of wild plant populations are a high priority in plant virus ecology research. Recent work with wild genotypes of A. thaliana found, for example, that the effects of infection with Cucumber mosaic virus (CMV) (family Bromoviridae: genus Cucumovirus) were strongly influenced by interactions with host density and genotype (Pagan et al., 2009). The extent to which virus infection has population-level consequences for hosts depends upon which host processes are affected (e.g., germination, growth, resource allocation, survival, and fecundity), the magnitude of change in those processes, and the sensitivity of host population growth to this change (Alexander and Mihail, 2000; Caswell, 2001). A key consideration with perennial plants is that estimates of virus impacts on life-time fitness should include effects on individual longevity as well as on reproductive output per year. Consequently, virus infections that reduce annual seed production but promote long-term survivorship have potential to enhance an individual’s life-time fitness. 4.4. Community and ecosystem interactions

Studies at the level of communities and ecosystems require consideration of multiple ecological factors. Research in com-

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munity ecology emphasizes interactions among populations and among taxa from different trophic levels (biotic interactions), which include consumers and mutualists as well as pathogens. Ecosystem studies emphasize interactions between communities and their physical environments, with a particular focus on ecological processes such as biogeochemical cycling, and exchange of water and energy. At this level of consideration, the characteristics of agricultural and natural systems differ substantially, and the complexity of natural systems becomes even more apparent. Central differences include species diversity and the influence of environmental constraints such as resource limitations and climatic extremes. Species diversity generally increases along gradients from the industrialized agroecosystems to wild communities. Modern agriculture has created large swathes of low diversity landscapes around the globe. For example, 39% (543 million ha) of the estimated 1.4 billion ha of global arable land or about 4% of all global land area is harvested solely for wheat, rice or maize (FAO, 2008). In ecology, the term species richness (S) describes the number of species in a given area, and species diversity generally refers to a combined measure of both species richness and species evenness or the relative abundance of each species. One commonly applied measure of species diversity is the ln-based Shannon–Wiener index (H ) (Gurevitch et al., 2006). In a crop monoculture with no weeds, Splants = 1 and H plants = 0; in a simple polyculture with equal numbers of only three species, Splants = 3 and H plants = 1.099. For comparison, abundance of woody species in forested ecosystems has been measured in 0.1 ha plots as S = 15–26 and H = 2.19–3.74 in North American and European temperate forests and as S = 53–265 and H = 4.52–7.59 in lowland neotropical areas (Gentry, 1988). Agroecosystems and natural communities typically also differ in the extent and nature of the environmental stress experienced by individuals within them. In wild communities, for example, plants compete with each other for space, water, nutrients, and light, and for access to mutualists such as pollinators. In most agroecosystems, human managers employ cultivation strategies to ameliorate these stresses through practices such as adjusting plant density, applying fertilizer and irrigation, and supplementing pollinator populations. In parallel, managers use cultivation techniques, physical deterrents, and insecticides to limit the extent of herbivory by insects, birds, and mammals that crops experience, while wild plant communities have no such external protection. Thus, studies focused on agroecosystems have explored only a small proportion of the environmental conditions under which plants, viruses, and their vectors interact and influence each other’s fitness. A central question in plant virus ecology therefore is, under what conditions are virus influences on host fitness negative, neutral, or positive? Historically, plant viruses in agriculture have been conceptualized as pathogens because those studied usually exert negative effects on the fitness of individual hosts and on crop yield; such effects of virus infection are also observed in wild plants (e.g., Kelley, 1994; Maskell et al., 1999; Remold, 2002; Malmstrom et al., 2005a). However, sometimes viruses may be merely commensal and cause little or no disease, and at other times viruses may even benefit their hosts (Roossinck, 2005). Within the increased complexity of natural ecosystems, virus interactions that appear neutral to negative in simpler settings may have greater potential to affect community dynamics in ways that unexpectedly promote host fitness. 4.4.1. Biotic interactions The complexity that diversity introduces to communities increases the potential number of biotic interactions that may influence host fitness, virus evolution, and other key factors. Developing means to predict the net outcome of multiple diversity-dependent

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mechanisms is therefore a key goal of plant virus ecology. It is interesting to consider, for example, under what conditions diversity is most likely to decrease or increase virus inoculum pressure. In some situations, diversity might reduce such inoculum pressure, for example by increasing the abundance of natural enemies that control vector populations. In other situations, host diversity might increase inoculum pressure, for example by favoring the evolution of ‘generalist’ viruses that infect multiple host species rather than ‘specialists’ that infect few species. Such a possibility is of further interest because it has been established that generalist viruses, when present, can alter community dynamics through processes such as apparent competition, in which one host population limits another by indirectly increasing the pathogen pressure experienced by the second population (e.g., Holt, 1977; Malmstrom et al., 2005a,b; Power and Mitchell, 2004; Power et al., in this issue). In complex natural communities, multi-trophic interactions have an enhanced potential to affect how viruses and plants influence each other and to determine their fitness. Vector ecology is a key example and area for consideration. Since most plant viruses are partially or completely dependent for transmission upon arthropod (Brault et al., 2010; Nault, 1997; Fereres and Moreno, 2009), nematode (Neilson et al., 2008), or fungal (Varrelmann, 2007) vectors, vector interactions are central determinants of virus dispersal, prevalence, and fitness (Power, 1991; Sisterson, 2008). For example, interactions between vector and host genotypes can influence the distribution of pathogens among hosts (Hall et al., 2010). Concurrently, virus infection of plants can enhance vector fitness by altering vector population growth, reproduction and/or behavior (Kennedy, 1951; Fereres et al., 1989; Blua and Perring, 1992; Jiménez-Martínez et al., 2004a,b). For example, vectors may prefer to colonize infected plants because of infection-induced changes in host plant morphology, nutrition, or physiology (Macias and Mink, 1969; Markkula and Laurema, 1964; Fereres et al., 1990, 1999). A particularly intriguing issue is the influence of virus infection on the production of volatile organic compounds by the host plant (Bosque-Pérez and Eigenbrode, in this issue). When produced by virus-infected plants, such compounds can induce behavioral changes in vectors that enhance their preference for these hosts (Eigenbrode et al., 2002; Jiménez-Martínez et al., 2004b; Ngumbi et al., 2007; Medina-Ortega et al., 2009; Werner et al., 2009). However, the complexity of such effects is only now being resolved (Bosque-Pérez and Eigenbrode, in this issue). For example, studies with nonpersistently transmitted CMV infecting squash plants have demonstrated that aphids are initially attracted to volatiles emitted by CMV-infected plants but subsequently disperse to colonize virus-free plants preferentially (Mauck et al., 2010). Understanding the evolution and ecological implications of virus-induced volatiles requires comparative studies using laboratory, greenhouse and field experiments to elucidate vector preferences for infected plants among viruses with different types of vector dependency (Castle et al., 1998; Eigenbrode et al., 2002). While previous research in this area focused mostly on cultivated plants, recent studies have begun to include wild crop relatives (Srinivasan and Alvarez, 2007; Srinivasan et al., 2006, 2008). Investigations of virus–plant–vector chemical ecology need to be expanded to include other wild host plants, virus–vector combinations, and the extended herbivore communities associated with plant populations in both cultivated and non-cultivated settings. Interactions between plant viruses and mammalian herbivores have been much less explored and deserve attention. For example, Gibbs (1980) suggested that virus-induced production of secondary metabolites could help protect infected plants from herbivory by small mammals, such as rabbits, but this idea has not yet been pursued. Plant–virus interactions with domestic livestock have received slightly more attention, but remain understudied. In some cases, livestock may have the capacity to serve as vectors and dis-

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perse viruses within grazed lands (e.g., McKirdy et al., 1998). In other cases, grazing may increase the survival of infected plants disproportionately (Malmstrom et al., 2006) or favor proliferation of more virus-competent hosts (Borer et al., 2009). Increased prevalence of virus-infected plants in turn can negatively affect livestock health. Jones and Ferris (2001) found, for example, that Alfalfa mosaic virus (family Bromoviridae; genus Alfamovirus) infection in medic pasture increased levels of coumestral in plant tissue, which could contribute to fertility disorders in livestock (see also Jones, 2004). Ecological interactions among viruses and between viruses and other microbes have also received little attention. Plants often are infected by more than one virus (Melcher et al., 2008; Pagan et al., 2010a,b), as well as by fungi and bacteria, but little is known about the ecological consequences of interactions among these organisms. Studies integrating molecular and ecological mechanisms are needed in these areas. 4.4.2. Interactions with the physical environment Because virus infection can alter plant traits – biochemical, physiological, structural – infection has the potential to increase the phenotypic diversity of plant populations. Consequently, infected plants may respond differently to resource constraints or release, or to other abiotic stresses. Where infection inflicts a growth penalty on the host, relaxation of resource constraints, either through direct resource addition (e.g., elevated CO2 : Malmstrom and Field, 1997) or through indirect release by activities such as grazing (Malmstrom et al., 2006), may stimulate infected hosts preferentially. In other cases, virus infection has been reported to increase plant tolerance to temperature extremes or to drought (Márquez et al., 2007; Xu et al., 2008). Such host responses may be more likely to manifest in stressful, low-resource conditions in natural communities than in managed agroecosystems, and their consequences for plant virus ecology and evolution merit investigation. For example, virus infection that inhibits plant capacity for photosynthetic acclimation may limit infected individuals to shady environments (Osmond et al., 1990). This phenomenon might not be evident in crop fields in which most individuals are exposed to full sunlight. Self-thinning that occurs naturally from resource competition in dense stands of wild plants, and which agronomists seek to minimize in crops, may be one mechanism whereby plant populations can shed virus infection by accelerating the death of infected individuals (Malmstrom et al., 2005a,b). The dynamics and outcomes of plant–virus interactions may be further shaped by ecosystem-level availability of elements that are critical for plant and virus replication, including nitrogen and phosphorus. The availability of such nutrient elements shapes dynamics in bacterial pathogen systems and others (e.g., Frost et al., 2008; Smith, 2007; Smith et al., 2005), but the intricacies of such interactions are only beginning to be studied in plant virus ecology. It is known, for example, that successful viruses that accumulate to high titer can sequester large amounts of phosphate in their genomes, but empirical evidence of the influence of phosphorus levels on virus dynamics in natural ecosystems is only now being accumulated. Borer et al. (2010), for example, found that infection rates in experimental grass plots increased with the amount of phosphorus but not with that of nitrogen. Since nitrogen availability can alter plant tissue quality and influence vector dynamics in some systems (Garratt et al., 2010), interactions with nitrogen remain an important area of ongoing study. Further experiments are in progress to evaluate the effect of free air carbon dioxide enrichment on viral infection of plants and virus–vector interactions (P. Trebicki, personal communication). Can viruses in turn influence ecosystem processes and biogeochemical cycling? In oceans, the answer is emphatically ‘yes.’ Virus effects on plankton dynamics have been shown to influence marine

carbon cycling and the release of dimethyl sulfide from the ocean surface (Suttle, 2007). In terrestrial ecosystems, this question has been little explored and merits attention. It is not known, for example, if viral-induced sequestration of phosphorus influences rates of its depletion from soils, or whether virus infections influence ecosystem-wide values of net primary production or respiration. 4.5. Regional and global distributions Plant–virus interactions at molecular to community and ecosystem level scales are ultimately ‘nested’ within regional contexts that have the potential to exert considerable influence as well. Key questions center on patterns of host and virus diversity across landscapes and at regional to global scales. In ecology, diversity, as previously discussed, describes ␣-diversity or local or community species abundance (see Section 4.4). At broader scales, ␥-diversity measures landscape or regional species abundance values and ␧-diversity may be used to describe diversity of even larger geographic areas (Whittaker, 1960; Whittaker, 1972; Gurevitch et al., 2006). ␤-diversity is an intermediate measure that describes either change in diversity along a transect or non-directional heterogeneity in a patchy environment (Anderson et al., 2011). Within landscapes, heterogeneous distributions of susceptible hosts may result in a patch network distribution of individual virus strains or species (Margosian et al., 2009). Transmission of virus from one patch of susceptible hosts to another requires mobile vectors or dispersal events, such as strong winds or human intervention. The effect of host density on connectivity of infection zones can be examined using graph theory, which allows estimates of landscape resistance to transmission (Margosian et al., 2009). Field studies suggest that in some cases virus pressure may decrease with increasing diversity of land cover types, perhaps due to increased abundance of biocontrol agents (A.C. Schrotenboer, unpublished data). At the global scale, plant species richness and diversity vary by biome, as a function of factors such as resource availability, latitudinal gradients, and evolutionary history (Kier et al., 2005, 2009; Mutke and Barthlott, 2005). The global species richness of pathogens causing human disease has been linked to climate factors and negatively correlated with latitude (Guernier et al., 2004), as for other taxa, but the extent of such patterns among wild plant viruses is only now being explored. For example, the distribution of strains of Kennedya yellow mosaic virus (family Tymoviridae; genus Tymovirus) along the Australian eastern coast was found to depend on latitude (Skotnicki et al., 1996) and the ␤-diversity of four Barley and cereal yellow dwarf viruses (B/CYDVs) (family Luteoviridae) was found to decline with increasing latitude in Pacific coast grasslands of the USA (Seabloom et al., 2010). In comparison, multiple examples of emergence of viral diseases in crops suggest that most pathogenic viruses of cultivated crops are not naturally distributed globally (Bosque-Pérez, 2000; Gildow et al., 2004) and have required human intervention to achieve their current continental or global scale distribution. 4.6. Response to anthropogenic change With essential research in the areas described above, the field of plant virus ecology seeks to build fundamental understanding of plant virus dynamics to address pressing questions of societal importance. These include the potential consequences for regional and global virus dynamics of global land use change, species introductions, and atmospheric and climate change, as well as questions about means of monitoring the potential for and preventing acts of bioterrorism. Evidence already indicates that human-induced changes in vegetation patterns can alter the dynamics and distribution of plant

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viruses. In broad terms, “domestication of nature” describes the increasingly widespread influence of human activities on wild communities that is driving shifts in population structures and genetic characteristics of many organisms worldwide (Kareiva et al., 2007). Increasing concern focuses on the observation that a reduction in biodiversity tends to increase disease incidence (Keesing et al., 2010). Wide-scale changes in land use and agricultural practices already have created conditions that promote virus diversification and spread into new environments (Bos, 1981; Harrison, 1981; Thresh, 1982; Cooper and Jones, 2006; Fargette et al., 2006; Webster et al., 2007; Gibbs et al., 2008). Devastating “new encounter” crop diseases have resulted when native viruses infected introduced crop plants that proved to be excellent hosts (Buddenhagen, 1977; Bosque-Pérez, 2000). Similarly, invasion of new hosts into natural communities have the potential to alter virus and vector dynamics, increase virus pressures on native species (Borer et al., 2007; Malmstrom, 1998; Malmstrom et al., 2005a,b, 2006, 2007; Power et al., in this issue) and other naturalized residents (Power and Mitchell, 2004), and thereby alter species distributions and ecosystem properties. Weedy plants with fast growth and high nutrient value may be particularly likely to serve as effective virus reservoirs (Cronin et al., 2010). Accidental introductions of viruses and vectors to new geographic regions are also a major cause of emerging plant diseases (Anderson et al., 2004; Woolhouse et al., 2005); escape from natural enemies may promote exotic plant invasions in other cases (Mitchell and Power, 2003; Torchin and Mitchell, 2004). Concurrently, human modification of native plants for new uses in restoration ecology and bioenergy production has increased selection for traits such as fast growth and digestibility that can increase plant susceptibility to viruses (Schrotenboer et al., 2011). Changes in atmospheric composition and climate have already impacted agro-ecosystems (U.S. Climate Change Science Program, 2008), particularly by influencing insect vectors (Canto et al., 2009), and may increase the extent of virus epidemics. Impacts that influence vector ecology include reduced plant defenses, increased feeding rates, enhanced over-wintering ability, earlier spring arrivals, and geographic range expansions (Canto et al., 2009). Anthropogenic increases in nitrogen deposition (Vitousek et al., 1997; Galloway and Cowling, 2002; Matson et al., 2002) may also influence virus dynamics, in part through nitrogen’s documented effects on vector biology (Garratt et al., 2010). Moreover, climate change is likely to alter the distribution of arthropod vector-borne pathogens and may expand the geographical limits of the diseases they cause (Sutherst, 2004). Increased temperatures affect distribution, reproduction and survival of herbivorous arthropods (Bale et al., 2002), but understanding of the effects of temperature change on vector-borne plant viruses remains limited. Of all the challenges in global environmental science, the question of how to predict and manage “low probability/high-impact events”, such as damaging outbreaks of pathogenic viruses, remains among the most difficult (Intergovernmental Panel on Climate Change, 2007). Risk assessments are needed for scenarios that include adoption of novel crops, changes in cropping systems, habitat restoration efforts, and climate changes. For bioterrorism control efforts, understanding environmental factors that facilitate or slow regional dispersal of viruses is essential, as is development of improved virus detection tools (Fletcher et al., 2008).

5. Conclusions Plant virus ecology is an expanding discipline that has grown from roots in diverse fields. Advancing understanding of plant–virus interactions and exchange among diverse ecosys-

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tems requires multi-disciplinary integration of perspectives, from molecular to ecological. Specific knowledge gaps that require attention include the need to (i) integrate consideration of plant viruses broadly into ecological research and theory, in which viruses have generally been overlooked; (ii) broaden ecological perspectives in virology to include new methods and disciplines, such as ecosystem ecology; and (iii) expand knowledge of virus influence in wild plants and communities. Studies of plant–virus–vector interactions in nature provide both opportunities and challenges that will ultimately give rise to multifaceted understanding of the role of viruses in shaping ecological and evolutionary dynamics.

Acknowledgements We are grateful to our PVEN and ICPVE colleagues for insightful discussions, and for suggestions on this manuscript provided by J.M. Thresh and two anonymous reviewers. This work was supported by the National Science Foundation grant no. IOS-0639139, the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494 (CMM), and the Michigan (CMM), Oklahoma (UM), and Idaho (NBP) Agricultural Experimental Stations. E. Cole provided technical assistance.

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