Despite increasing effort to sequence and characterize the ubiquitous wild viruses that inhabit wild plant communities, we have very little understanding of the impacts of wild plant–virus interactions. Given the demonstrable effects of crop-infecting viruses on both crops and wild plants, there has been much conjecture about the impacts of wild viruses on wild plants, as well as increasing realization that such interactions likely have significant ecological and evolutionary implications that are currently unrecognized. Investigation of wild plant – wild virus interactions has lagged in part because they can be more challenging to study than virus dynamics in crops. This challenge stems from several factors: wild plants are generally longer lived and more architecturally complex than crop species, and they typically exhibit greater phenotypic, genetic, and age-structure variation within populations. In this dissertation, I conduct a series of investigations to characterize interactions between a wild plant and a wild virus at organismal, genomic, and population scales. For a model system, I use switchgrass (Panicum virgatum L.)—a candidate species for biofuel development—and switchgrass mosaic virus (SwMV), a wild virus that circulates within perennial grasslands in Midwestern North America. The main research aims of this work were (i) to characterize disease dynamics and fitness effects of SwMV infection within individual switchgrass plants over time; (ii) to characterize within-population variation in SwMV disease expression; and (iii) to identify genes potentially associated with SwMV disease expression.In the first research chapter, I present the results of several related field studies of naturally-infected established switchgrass plants, most notably a three-year longitudinal study of individual plants representing a range of SwMV disease extent (proportion of tillers with symptoms). These results demonstrate that while SwMV infection can cause significant disease and loss of tiller performance, it may persist for years within individual plants that continue to grow and reproduce, particularly when infection is localized to only a portion of the plant. The second research chapter describes an additional field study in which I experimentally inoculated young switchgrass plants to further explore multi-year fitness effects of SwMV. The results suggest that SwMV infection confers tolerance to hosts in the context of moderate to high foliar fungal disease (anthracnose) extents (proportion of plant with necrotic lesions). The third research chapter reports work I conducted with collaborators to examine SwMV disease dynamics within a diversity panel of 500+ switchgrass accessions that originated from a broad swath of switchgrass’ natural range in the USA. In a common garden in Michigan, this panel naturally accumulated SwMV infection and many accessions developed disease. There was striking variation in the extent and severity of disease among ecotypes and regional subgroups, underscoring the importance of developing better understanding of how virus pressures have shaped wild plant populations. Genome-wide association studies found associations between SwMV disease and a diverse set of genes widely distributed across the switchgrass genome. Overall, these results suggest that there are complex and nuanced mechanisms by which pathogenic wild viruses persist within the long-lived and architecturally complex plants that dominate natural landscapes, including potential benefits in certain environmental contexts. Additionally, this work suggests that the subpopulations of a wild plant species can have divergent responses to wild virus infection, and that viral disease expression may be associated with a broader and more diverse genetic network than is currently indicated from studies of crop plant–virus systems.
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