Discovery of novel viruses related to the Potyviridae family reveals expanded diversity, a broad host range, and evidence of fungal and oomycete infections

ABSTRACT The family Potyviridae represents the largest and most economically important group of plant-infecting RNA viruses. Despite extensive study of crop-associated members, the full diversity, host range, and evolutionary history of potyvirids remain poorly understood. Here, we conducted a large-scale mining of publicly available RNA-seq datasets to systematically search for novel potyvirid sequences. This approach enabled the identification and assembly of 47 previously undescribed members of the family, distributed across eight recognized genera and, importantly, putative new groups. Beyond expanding the known genetic diversity of Potyviridae, our analyses revealed a distinct and deeply divergent lineage of potyvirid-like viruses associated with fungi and oomycetes. These viruses possess compact genomes and atypical genomic organizations, including the absence of canonical plant cell-to-cell movement factors and the presence of HCPro-like proteins arranged in tandem. Comparative structural and phylogenetic analyses indicate that these leader proteases are more closely related to fungal hypoviral counterparts than to canonical potyvirid HCPro factors. Together, our findings substantially expand the host range of Potyviridae, provide compelling evidence that potyvirid-like viruses likely infect fungi and oomycetes in nature, and offer new insights into the evolutionary pathways that have shaped this major virus family.