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

Abstract

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 plant-associated 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.

New Ca. Liberibacter psyllaurous haplotype resurrected from a 49-year-old specimen of Solanum umbelliferum: a native host of the psyllid vector

“…This knowledge gap can only be addressed by increasing efforts to perform diagnostic and genetic characterization studies using historical specimens and sampling in unmanaged habitats 5,11 . Such approaches are yielding a wealth of information on the diversity and epidemiology of other plant pathogen taxa across different landscape types 5,7,[12][13][14][15][16] . However, to date there have been no efforts to discover and characterize Ca.…”

Host Range Evolution of Potyviruses: A Global Phylogenetic Analysis

“…Consequently, potyvirus evolution and speciation in the future could be strongly affected by future agricultural changes, such as the choice of new crop species or of growing crop species in new geographical areas. Indeed, agricultural environments are favorable for virus adaptation, specialization, and speciation, given the large number and genetic homogeneity of hosts in crops [27,28,36].…”

Endemicity and prevalence of multipartite viruses under heterogeneous between-host transmission

“…Though our knowledge of existing viral forms is still incomplete and likely biased [16,55], our results indicate that endemic states mixing monopartite and multipartite cognate forms (hj, all) need values of transmissibility difficult to sustain: endemicity could be achieved with lower values of transmissibility if the virus propagated only as a wild-type, while high values entail a cost that is usually compensated by decreasing infectivity [56]. Albeit rare, however, these endemic states might 13/27 act also as a stepping stone towards multipartitism even if they are only transiently present, as in the following example.…”

“…It is known that changes in land cover offer multiple opportunities for novel interactions between plants and pathogens [12][13][14][15]. Studies on the impact of agriculture in viral ecology have uncovered a surprisingly negative association between plant diversity and family-level diversity of plant-associated viruses, and a higher prevalence of viruses in cultivated areas [16].…”