No abstract

Because viruses have been mostly studied in cultivated plants, little is known about virus diversity and ecology in less-managed vegetation or about the influence of human management and agriculture on virome composition. Poaceae (grass family)-dominated communities provide invaluable opportunities to examine these ecological issues, as they are distributed worldwide across agro-ecological gradients, are essential for food security and conservation, and can be infected by numerous viruses. Here, we used multiple levels of analysis that considered plant communities, individual plants, virus species, and haplotypes to broaden understanding of the Poaceae virome and to evaluate host-parasite richness relationships within agro-ecological landscapes in our study area.

Modern agriculture has influenced plant virus emergence through ecosystem simplification, introduction of new host species, and reduction in crop genetic diversity. Therefore, it is crucial to better understand virus distributions across cultivated and uncultivated communities in agro-ecological interfaces, as well as virus exchange among them. Here we advance fundamental understanding in this area by characterizing the virome of three co-occurring replicated Poaceae community types that represent a gradient of grass species richness and management intensity, from highly managed crop monocultures to little-managed, species-rich grasslands. We performed a large-scale study on 950 Poaceae over two years combining untargeted virome analysis down to virus species level with targeted detection of three plant viruses. Deep sequencing revealed i) a diversified and largely unknown Poaceae virome (at least 51 virus species/taxa), with an abundance of so-called persistent viruses; ii) an increase of virome richness with grass species richness within the community; iii) a stable virome richness over time but a large viral intraspecific variability; and iv) contrasted patterns of virus prevalence, co-infections and geographical distribution among plant communities and species. Our findings highlight the complex structure of phytoviral communities in nature and suggest the influence of anthropic management on viral distribution and prevalence.