Exploration of mycovirus composition in a hypovirulent strain of Sclerotinia sclerotiorum potentially uncovers mycovirus cross-taxa transmission

Sclerotinia sclerotiorum is a worldwide plant pathogenic fungus. Identifying novel mycoviruses in this fungus can aid in developing fungal disease control strategies and enhance our understanding of viral evolution. Here, we analyzed mycovirus composition in S. sclerotiorum strain XZ69, and identified six ssRNA mycoviruses, including five known mycoviruses and one unassigned mycovirus. The newly identified mycovirus, tentatively named Sclerotinia sclerotiorum narna-like virus 1 (SsNLV1/XZ69), possesses a full-length genome of 3534 nucleotides, containing a single ORF that encodes an RNA-dependent RNA polymerase (RdRp) of 1090 amino acids. The RdRp encoded by SsNLV1/XZ69 shares 60.4 % identity with that encoded by Monilinia narnavirus H. SsNLV1/XZ69 phylogenetically clusters with unclassified narna-like viruses potentially infecting fungi, plants, and animals, and they form an independent branch that is distant from established families, therefore supporting the establishment of a new family to accommodate these viruses. Sclerotinia sclerotiorum fusarivirus 3 (SsFV3/XZ69) share 97 % amino acid identities with preciously reported Botrytis cinerea fusarivirus 8 (BcFV8). This last mycovirus originated from Botrytis cinerea, and hence this reveals that cross-genus transmission of SsFV3 or BcFV8 between B. cinerea and S. sclerotiorum may have potentially occurred. Mycovirus elimination, horizontal transmission, and RNA transfection experiments revealed that Sclerotinia sclerotiorum negative-stranded RNA virus 1 (SsNSRV1/XZ69), SsNSRV2/XZ69, and SsFV3/XZ69 may be associated with hypovirulence in S. sclerotiorum, and strain XZ69 exhibits potential disease biocontrol on rapeseed seedlings. Our study expands our understanding of viral evolution, and may provide new potential biocontrol agents for S. sclerotiorum.