A novel partitivirus confers dual contradictory effects to its host fungus: growth attenuation and virulence enhancement.

Mycoviruses possess a potential role for biological control due to their ability to reduce both virulence and vegetative growth in some phytopathogenic fungi. However, mycoviruses that enhance fungal pathogenicity have been poorly studied and characterized. In this study, a novel double-stranded RNA (dsRNA) fungal virus, tentatively named Sinodiscula camellicola partitivirus 1 (ScPV1), was identified in the phytopathogenic fungus Sinodiscula camellicola, isolated from tea leaves. ScPV1 possesses two genomic components of 1,835 bp and 1,697 bp in length, each containing an open reading frame (ORF) encoding a putative RNA-dependent RNA polymerase (RdRP) and coat protein (CP), respectively, as confirmed by mass spectrometry. Phylogenetic analysis of the amino acid sequences of the RdRPs from ScPV1 and related mycoviruses placed ScPV1 within a newly proposed genus, Epsilonpartitivirus, in the family Partitiviridae. The virus was purified using ultracentrifugation, and transmission electron microscopy revealed that ScPV1 dsRNA genomes are encapsidated in virus particles ca. 31 nm in size, ranging from 24.9 to 36.8 nm, together with the RdRP protein, which was of an unexpected size. Transfection with purified virions generated transfectants with significantly reduced growth rates but with increased virulence, indicating that ScPV1 confers unusual effects on its host fungus. This finding represents a significant advancement in understanding the complex interactions between mycoviruses and their host fungi. IMPORTANCE: Here, we identified a novel partitivirus, tentatively named Sinodiscula camellicola partitivirus 1 (ScPV1), marking the first report of a partitivirus from a phytopathogenic fungus infecting tea plants. ScPV1 is characterized by possession of two dsRNA genomic components encapsidated in particles of varying sizes, along with an RNA-dependent RNA polymerase protein of an expected size, which contained some unique amino acids, indicating its distinct molecular and morphological traits. Biological tests on transfectants generated following protoplast infection with purified virions demonstrated that ScPV1 impairs vegetative growth while enhancing virulence in its fungal host. This finding represents the first instance of a mycovirus responsible for hypervirulence on a phytopathogenic fungus through virion transfection, as well as the first case of a partitivirus conferring hypervirulence while reducing vegetative growth in a phytopathogenic fungus. We anticipate that these findings will significantly advance our understanding of the complex interactions between mycoviruses and their host fungi.