Abstract
Viruses are ubiquitous within all habitats that support cellular life and represent the most important emerging infectious diseases of plants. Despite this, it is only recently that we have begun to describe the ecological roles of plant viruses in unmanaged systems and the influence of ecosystem properties on virus evolution. We now know that wild plants frequently harbor infections by diverse virus species, but much remains to be learned about how viruses influence host traits and how hosts influence virus evolution and vector interactions. To identify knowledge gaps and suggest avenues for alleviating research deficits, we performed a quantitative synthesis of a representative sample of virus ecology literature, developed criteria for expanding the suite of pathosystems serving as models, and applied these criteria through a case study. We found significant gaps in the types of ecological systems studied, which merit more attention. In particular, there is a strong need for a greater diversity of logistically tractable, wild dicot perennial study systems suitable for experimental manipulations of infection status. Based on criteria developed from our quantitative synthesis, we evaluated three California native dicot perennials typically found in Mediterranean-climate plant communities as candidate models: Cucurbita foetidissima (buffalo gourd), Cucurbita palmata (coyote gourd), and Datura wrightii (sacred thorn-apple). We used Illumina sequencing and network analyses to characterize viromes and viral links among species, using samples taken from multiple individuals at two different reserves. We also compared our Illumina workflow with targeted RT-PCR detection assays of varying costs. To make this process accessible to ecologists looking to incorporate virology into existing studies, we describe our approach in detail and discuss advantages and challenges of different protocols. We also provide a bioinformatics workflow based on open-access tools with graphical user interfaces. Our study provides evidence that dicot perennials in xeric habitats support multiple, asymptomatic infections by viruses known to be pathogenic in related crop hosts. Quantifying the impacts of these interactions on plant performance and virus epidemiology in our logistically tractable host systems will provide fundamental information about plant virus ecology outside of crop environments.
Highlights
The integration of plant virology and ecology is recent, stimulated by the discovery that viruses are important but largely undescribed and understudied components of the ecology of wild plants
Among precursor papers (Figure 2A), studies focusing exclusively or partially on wild plant hosts have equal or greater representation relative to studies focusing exclusively on crop hosts within the areas of Environmental virology, Epidemiology, Virus effects on host traits, Virus evolution, and Virus discovery, while studies focusing exclusively or partially on wild hosts are somewhat underrepresented within the area of Virus–vector interactions (5/11 studies) (Figure 2B)
Among product papers falling into one or more of the six core virus ecology research areas (Figure 3A), there is a clear shift toward greater proportional representation of crop and model host plants relative to wild hosts (Figure 3B)
Summary
The integration of plant virology and ecology is recent, stimulated by the discovery that viruses are important but largely undescribed and understudied components of the ecology of wild plants. Since the inception of this field, ecologists and plant virologists have worked to illuminate two issues: (i) the ecological roles of plant viruses and vectors in unmanaged ecosystems, and (ii) the influence of ecosystem properties on the distribution and evolution of plant viruses and their vectors (Malmstrom et al, 2011). Thanks to these efforts, we know that wild plants frequently harbor infections by a wide diversity of plant viruses, which almost certainly influence host traits in ways not previously quantified or considered by the field of plant ecology (Malmstrom and Alexander, 2016). It is critical to ask to what degree these interactions will influence microbial evolution and the probability that some microbes will emerge as novel pathogens (Alexander et al, 2013; Roossinck and García-Arenal, 2015)
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