Transcriptome Mining Expands Knowledge of RNA Viruses across the Plant Kingdom

Our current understanding of plant viruses stems largely from those affecting economically important plants. Yet plant species in cultivation represent a small and biased subset of the plant kingdom. Here, we describe virus diversity and abundance in 1,079 transcriptomes from species across the breadth of the plant kingdom (Archaeplastida) by analyzing open-source data from the 1000 Plant Transcriptomes Initiative (1KP). We identified 104 potentially novel viruses, of which 40% were single-stranded positive-sense RNA viruses across eight orders, including members of the Hepelivirales, Tymovirales, Cryppavirales, Martellivirales, and Picornavirales. One-third of the newly described viruses were double-stranded RNA viruses from the orders Durnavirales and Ghabrivirales. The remaining were negative-sense RNA viruses from the Rhabdoviridae, Aspiviridae, Yueviridae, and Phenuiviridae and the newly proposed Viridisbunyaviridae. Our analysis considerably expands the known host range of 13 virus families to include lower plants (e.g., Benyviridae and Secoviridae) and 4 virus families to include alga hosts (e.g., Tymoviridae and Chrysoviridae). More broadly, however, a cophylogeny analysis revealed that the evolutionary history of these families is largely driven by cross-species transmission events. The discovery of the first 30-kDa movement protein in a nonvascular plant suggests that the acquisition of plant virus movement proteins occurred prior to the emergence of the plant vascular system. Together, these data highlight that numerous RNA virus families are associated with older evolutionary plant lineages than previously thought and that the apparent scarcity of RNA viruses found in lower plants likely reflects a lack of investigation rather than their absence. IMPORTANCE Our knowledge of plant viruses is mainly limited to those infecting economically important host species. In particular, we know little about those viruses infecting basal plant lineages such as the ferns, lycophytes, bryophytes, and charophytes. To expand this understanding, we conducted a broad-scale viral survey of species across the breadth of the plant kingdom. We found that basal plants harbor a wide diversity of RNA viruses, including some that are sufficiently divergent to likely compose a new virus family. The basal plant virome revealed offers key insights into the evolutionary history of core plant virus gene modules and genome segments. More broadly, this work emphasizes that the scarcity of viruses found in these species to date most likely reflects the limited research in this area.