A Beneficial Endornavirus Enhances the Fitness of Phytopathogenic Fungus Rhizotonia solani

Abstract

Although viruses are primarily characterized as pathogenic agents, certain viruses confer advantages to their hosts. The extent to which a virus can improve host biological performance, however, remains a fascinating topic in virology. An endornavirus, Rhizoctonia solani endornavirus IM (RsEV-IM), was identified as prevalent in Rhizoctonia solani isolates obtained from potato plants. Comparative analysis with a virus-free isogenic strain demonstrated that RsEV-IM infection enhances mycelial growth, sclerotium formation, stress tolerance, and fungal virulence across multiple plant species. Inoculation tests involving numerous R. solani strains confirmed that only RsEV-IM-infected strains exhibited high pathogenicity, independent of other mycovirus infections. Additionally, its secreted protein fraction of RsEV-IM-infected fungus contained elevated levels of various proteins, including those involved in cell wall degradation. This fraction not only facilitated R. solani infection but also suppressed the growth of other fungi and bacteria. These findings position RsEV-IM as a beneficial virus that widely enhances its hosts biological fitness. From both pathological and ecological perspectives, these observations are significant, as they reveal that a mycovirus can serve as a key virulence determinant in fungal populations and potentially shape microbial community dynamics in natural environments. ImportanceFungal pathogenicity and ecological traits have long been thought to be primarily governed by endogenous genetic factors. However, this study reveals a mutualistic relationship between an endornavirus (RsEV-IM) and Rhizoctonia solani, demonstrating that viral infection enhances fungal virulence and ecological fitness. RsEV-IM stimulates fungal growth and the secretion of cell wall-degrading enzymes, resulting in a severe disease phenotype. Ecologically, RsEV-IM-infected fungi potentially gain a competitive advantage over soil microbiota. These findings present a key example of a virus acting as an essential extrachromosomal determinant of fungal pathogenicity and ecosystem interactions. Our results advance the understanding of fungal virulence mechanisms and underscore the broader significance of beneficial virus-fungus associations in agriculture and microbial ecology.