Explorations of the plant virosphere

Plant viruses are near-ubiquitous across natural and managed ecosystems and are known to cause significant economic damage, influence host phenotypes and modulate host-insect and microbial interactions. Metagenomic surveys of plants have recently revealed the enormous diversity of viruses they carry. Yet, this new knowledge has predominantly come from cultivated species - a small and biased subset of the plant kingdom. Next-generation sequencing technology has led to an explosion in open-source transcriptomic data which is an untapped resource for virus discovery. Here, I surveyed the transcriptomes of 960 plant species to quantify the diversity and abundance of plant viruses across 422 plant families and multiple functional groupings (i.e. dispersal syndromes, fruit types, growth forms, longevity classes, and woodiness types). In total, 3,673 plant virus transcripts were found in 415 plant species across the plant kingdom. Virome composition was associated with plant growth form and phylogenetic lineage. Notably, high virus abundance is associated with plants with a climbing habit while ancient plant lineages (algae, gymnosperms) had significantly lower virus diversity compared to more recently evolved groups, like the basal eudicots. I identified 29 potentially novel viruses including the discovery of several single-stranded RNA virus families (i.e. Benyviridae, Tymoviridae and Secoviridae) for the first time in lower plants or algae highlighting that non-cultivated plants likely harbour a multitude of viruses, of which the vast majority are undescribed. With the knowledge generated herein, we can begin to resolve long-held questions about the origins and diversification of plant viruses.