Addressing Research Needs in the Field of Plant Virus Ecology by Defining Knowledge Gaps and Developing Wild Dicot Study Systems

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

Substrate limitations for heterotrophs: Implications for models that estimate the seasonal cycle of atmospheric CO_2

We examine the sensitivity of the seasonal cycle of heterotrophic respiration to model estimates of litterfall seasonality, herbivory, plant allocation, tissue chemistry, and land use. As a part of this analysis, we compare heterotrophic respiration models based solely on temperature and soil moisture controls (zero‐order models) with models that depend on available substrate as well (first‐order models). As indicators of regional and global CO_2 exchange, we use maps of monthly global net ecosystem production, growing season net flux (GSNF), and simulated atmospheric CO_2 concentrations from an atmospheric tracer transport model. In one first‐order model, CASA, variations on the representation of the seasonal flow of organic matter from plants to heterotrophs can increase global GSNF as much as 60% (5.7 Pg C yr^(−1)) above estimates obtained from a zero‐order model. Under a new first‐order scheme that includes separate seasonal dynamics for leaf litterfall, fine root mortality, coarse woody debris, and herbivory, we observe an increase in GSNF of 8% (0.7 Pg C yr^(−1)) over that predicted by the zero‐order model. The increase in seasonality of CO2 exchange in first‐order models reflects the dynamics of labile litter fractions; specifically, the rapid decomposition of a pulse of labile leaf and fine root litter that enters the heterotrophic community primarily from the middle to the end of the growing season shifts respiration outside the growing season. From the perspective of a first‐order model, we then explore the consequences of land use change and winter temperature anomalies on the amplitude of the seasonal cycle of atmospheric CO_2. Agricultural practices that accelerate decomposition may drive a long‐term increase in the amplitude, independent of human impacts on plant production. Consideration of first‐order litter decomposition dynamics may also help explain year‐to‐year variation in the amplitude

Mixed viral infection constrains the genome formula of multipartite cucumber mosaic virus

Many plant viruses have a multipartite organization, with multiple genome segments packaged into separate virus particles. The genome formula describes the relative frequencies of all viral genome segments, and previous work suggests rapid changes in these frequencies facilitate virus adaptation. Many studies have reported mixed viral infections in plants, often resulting in strong virus–virus interactions. Here, we tested whether mixed infections with tripartite alfalfa mosaic virus (AMV) and monopartite potato virus Y (PVY) affected the genome formula of the tripartite cucumber mosaic virus (CMV), our experimental model. We found that the CMV titer was reduced in mixed infections with its tripartite Bromoviridae relative AMV and in triple infections with both AMV and PVY, indicating notable virus–virus interactions. The variability of the CMV genome formula was significantly lower in mixed infections (CMV and AMV, CMV and PVY, and CMV and AMV and PVY) than in single infections (CMV only). These observations led to the surprising conclusion that mixed infections with two distinct viruses constrain the CMV genome formula. It remains unclear how common these effects are for different combinations of virus species and strains and what the underlying mechanisms are. We, therefore, extended a simulation model to consider three putative scenarios in which a second virus affected the genome formula. The simulation results also suggested that shifts in the genome formula occur, but may not be widespread due to the required conditions. One scenario modeled—co-infection exclusion through niche differentiation—was congruent with the experimental data, as this scenario led to reductions in genome formula variability and titer of the multipartite virus. Whereas previous studies highlighted host–species effects, our results indicate that the genome formula is also affected by mixed infections, suggesting that there is a broader set of environmental cues that affect the genome formula

Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale

Disease emergence events regularly result from human activities such as agriculture, which frequently brings large populations of genetically uniform hosts into contact with potential pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic information about virus distribution across agro-ecological interfaces and large gaps in understanding of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics approach to examine relationships between agricultural land use and distributions of plantassociated viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant samples collected over two years from 4.5 × 4.5 km2 grids spanning farmlands and adjacent uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but prevalence and identified family-level virus diversity were greatest in cultivated areas, with some virus families displaying strong agricultural associations. Our survey revealed 94 previously unknown virus species, primarily from uncultivated plants. This is the first effort to systematically evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that agriculture substantially influences plant virus distributions and highlight the extent of current ignorance about the diversity and roles of viruses in nature

Experimental Use of Remote Sensing by Private Range Managers and Its Influence on Management Decisions

Although remote sensing has many potential applications for range management, its use by range managers thus far has been limited. To investigate the factors that encourage use of remote sensing and to examine its influence on decision making by individuals who manage privately owned rangeland, we evaluated the decision-making processes of 3 ranch owners and 1 professional ranch manager who were introduced to remote sensing while collaborating with us in a rangeland stewardship program in California. Two of the participants had extensive ranching experience (11 to > 20 years) and managed large cattle ranches (1 000 to > 2 000 ha), and 2 had less experience and managed smaller sheep ranches (< 200 ha). During the 5-year program, the participants implemented a series of new management practices, including prescribed burning, rotational grazing, and seeding of native grasses, with the aim of reducing noxious weeds and increasing productivity. We used remote sensing to quantify the effect of these practices and provided ranch-wide remote sensing analyses to each manager on a password-protected Web site. Using case study methodologies, we found that managers of larger, commercially active ranches found the experimental use of remote sensing to be a highly positive experience that convinced them that this technology could help address difficult management situations and increase ranch profitability. This suggests that the broad use of remote sensing by managers of privately held, commercial rangelands may be limited in part by the simple lack of opportunity to test these technologies. Programs that assist ranchers in obtaining appropriate remote sensing products thus may be a cost-effective way to enhance conservation on private rangelands. Our findings suggest that voluntary self-analysis by ranchers of the landscape dynamics of their own properties is likely to lead to more engaged conservation efforts than will top- down prescriptions. The Rangeland Ecology & Management archives are made available by the Society for Range Management and the University of Arizona Libraries. Contact [email protected] for further information.Migrated from OJS platform August 2020Legacy DOIs that must be preserved: 10.2458/azu_jrm_v59i5_betterfiel

Data from: Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection

To understand the eco-evolutionary significance of plant viruses in nature, we must (i) quantify the effects of infection on plant fitness and (ii) recognize that native plants are increasingly exposed to crop-associated viruses. Studies of perennials are particularly needed: most of our knowledge of plant-virus interactions is from annuals, yet long-lived species dominate landscapes. Here we used aster models for life-history analysis and longitudinal measures of plant virus status to evaluate multi-year consequences of crop virus infection in a native perennial. We used Barley yellow dwarf virus acquired from wheat to inoculate seedlings of Panicum virgatum L. (switchgrass), a North American prairie grass. We grew inoculated and mock-inoculated individuals of two ecotypes for 3 years in the field. We measured plant size, infection status and fitness components. Aster modelling provided integrated multi-year measures of fitness. Crop virus inoculation reduced multi-year native plant fitness by 30% over 2 years despite generally asymptomatic infection and evidence of resistance. This reduction was greater than predicted from individual fitness components or most size measures. Ecotypes differed in response, with the lowland ecotype experiencing higher apparent recovery from infection. Virus treatment in the upland ecotype delayed flowering phenology and reduced seed filling. Synthesis. Our use of field experimentation, surveys of plant infection status and aster modelling demonstrates a rigorous and broadly applicable approach for quantifying the effects of viruses and other microbes on multi-year plant fitness. We found that a crop virus had negative multi-year effects on native plant fitness even after infection was no longer detected. Viruses may have substantial effects on native vegetation with domestication of landscapes and agricultural expansion