Core virome shapes adaptation of a phytopathogenic fungus to climate and cropping patterns

Despite extensive exploration of fungal viromes (mycoviromes), the ecological roles of mycoviruses remain poorly understood. Hence, we investigated the virome of Leptosphaeria biglobosa (an important fungal pathogen of rapeseed) from different geographic origins to determine the impacts of external factors on virome composition and their role in fungal ecological adaptation. The viromes of different L. biglobosa groups were investigated, and viral diversity correlated positively with field disease incidence and host diversity, but negatively with the altitude of the strain collection sites. A positive single-stranded RNA virus, namely, Leptosphaeria biglobosa letobirnavirus 1 (LbLV1), one of the core virome members (predominant viruses that constitute the majority of the viral community), has a significantly high incidence in L. biglobosa populations in winter rapeseed in southern China but a low incidence in L. biglobosa populations in spring rapeseed in northern China. Further laboratory and field tests revealed that LbLV1 could increase the ability of L. biglobosa to oversummer at average temperatures ranging from 23°C to 34°C in the winter rapeseed region of China. Therefore, the variation in LbLV1 incidence between winter and spring rapeseed should be a consequence of LbLV1-mediated adaptation to climate and cropping patterns. Furthermore, one gene, namely Lbhsp12, significantly induced by the hypothetical protein of LbLV1, is responsible for LbLV1-mediated thermal tolerance. Our findings indicate that mycovirome composition reflects environmental constraints, and core viruses can drive ecological adaptation by modulating host stress responses.