Diversity and pathobiology of an ilarvirus unexpectedly detected in diverse plants and global sequencing data

Sequencing technologies, and the massive data generated from it, revolutionized virus detection and discovery in recent years. We coupled modern high-throughput sequencing and data-driven virus discovery or detection approaches with classical plant virology techniques to accelerate the characterization of Solanum nigrum ilarvirus 1 (SnIV1). SnIV1 was recently reported in various Solanaceae plants from France, Slovenia, Greece, and South Africa. Interestingly, it was also detected in several plants under Vitaceae, Fabaceae, and Rosaceae. This warranted further investigation, because a very diverse host association are atypical for ilarviruses. Through in silico searches of sequencing datasets, we further detected SnIV1 in new diverse plants and non-plant sources globally. We observed relatively low variability and distinct phylogenetic clustering among SnIV1 isolates. We demonstrated systemic SnIV1 infection in Solanum villosum and its mechanical and graft transmissibility to several Solanaceae species, thus supporting its infectivity in plants. We sequenced SnIV1 genome from the inoculum (S. villosum) and artificially-inoculated Nicotiana benthamiana, thus fulfilling Koch's postulates. We demonstrated that SnIV1 is potentially seed-transmitted and pollen-borne, has typical quasi-spherical virions, and possibly induces histopathological changes in inoculated N. benthamiana leaves. Whether SnIV1 could emerge as a destructive crop pathogen is unpredictable, but our study gave us a head start to better understand its epidemiology. Finally, we emphasize the importance of minimum standards for virus genome detections in sequencing experiments and when conducting in silico searches of public sequencing data. We encourage additional diagnostic and inoculation tests, if possible, to verify virus presence in the original sample and its infectivity.