Unlocking the hidden genetic diversity of varicosaviruses, the neglected plant rhabdoviruses

Abstract

The genus Varicosavirus is one of six genera of plant-infecting rhabdoviruses. Varicosaviruses have nonenveloped flexuous rod-shaped virions and a negative-sense, single-stranded RNA genome. A distinguishing feature of varicosaviruses, that is shared with dichorhaviruses, is a bi-segmented genome. Before 2017, a sole varicosavirus was known and characterized, then two more varicosaviruses were identified through high-throughput sequencing in 2017 and 2018. More recently, the number of known varicosaviruses has substantially increased in concert with the extensive use of high-throughput sequencing platforms and data mining approaches. The novel varicosaviruses revealed not only sequence diversity but also plasticity in terms of genome architecture, including a virus with a tentatively unsegmented genome. Here, we report the discovery of 45 novel varicosavirus genomes, which were identified in publicly available metatranscriptomic data. Identification, assembly, and curation of raw Sequence Read Archive reads resulted in 39 viral genome sequences with full-length coding regions and 6 with nearly complete coding regions. Highlights of the obtained sequences include eight varicosaviruses with unsegmented genomes, linked to a phylogenetic clade associated with gymnosperms. These findings resulted in the most complete phylogeny of varicosaviruses to date and shed new light on the phylogenetic relationships and evolutionary landscape of this group of plant rhabdoviruses. Thus, the extensive use of sequence data mining for virus discovery has allowed unlocking of the hidden genetic diversity of varicosaviruses, the largely neglected plant rhabdoviruses.