Expansion of the plant-parasitic nematode RNA viruses: Unprecedented diversity, intron-bearing viruses, and cross-kingdom evolutionary links

Plant-parasitic nematodes (PPNs) pose a significant threat to global crop production, yet their associated viral diversity remains poorly characterized, limiting potential virus-mediated biocontrol strategies. In this study, we investigated PPN-associated viruses using both virome data obtained from ten field populations of potato rot nematode (Ditylenchus destructor) collected in Lulong County (Qinhuangdao city, China), a major sweet potato-producing region, along with 536 publicly available transcriptome datasets from the Sequence Read Archive (SRA) database, collectively encompassing twenty-five PPN species. We identified 94 PPN-associated viruses, representing a 7.9-fold increase over prior records. These viruses span eighteen established families and six unclassified viral groups, including the first discovery of orthomyxo-like viruses, Jingmen viruses, and ormycoviruses in PPNs or nematodes, expanding the possible host ranges of these viral groups. Notably, a clade of yue-like viruses harbored up to 10 introns, surpassing 2-3 introns that were only observed in orthomyxoviruses and certain members of the Mononegavirales. Furthermore, we identified two larger nematode-associated bunyaviruses with the L segments exceeding 12,000 bp, which appear to have acquired a putative cysteine proteinase gene potentially originating from their nematode hosts (possibly Pristionchus spp.). Our findings reveal that natural PPN populations could host an unexpectedly high diversity of RNA viruses, higher than previously recognized. Exploring these viruses provides novel insights into viral evolution and establishes a foundation for utilizing viruses as a potential method for controlling PPN diseases.