A Novel Partitivirus Confers Dual Contradictory Effect to Its Host Fungus: Growth Attenuation and Virulence Enhancement

Abstract

Mycoviruses represent potential role in the biocontrol approach due to their ability to reduce both virulence and vegetative growth in some phytopathogenic fungi. However, the mycoviruses enhancing the damage caused by these fungi remains poorly identified 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 1835 and 1697 bp, each containing an open reading frame (ORF) that encodes the 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, of the family Partitiviridae. Viral purification via ultracentrifugation and transmission electron microscopy observations revealed that ScPV1 dsRNA genomes are encapsidated within virus particles approximately 31 nm in size, ranging from 24.9 to 36.8 nm, along with the RdRp protein in an unexpected size. Transfection experiments with purified virions exhibited transfectants with significant reduced growth rates while increased virulence, indicating that ScPV1 has two-sided effect on its host fungus. This finding represents a significant advancement in understanding the complex interactions between mycoviruses and their host fungi. Author summaryTo characterize new molecular and biological traits of partitiviruses will provide substantial contributions for a better understanding of mycoviruses, as partitiviruses are prevalent across a wide range of hosts, including plants, protists, and fungi. Here, we identified a novel partitivirus, tentatively named Sinodiscula camellicola partitivirus 1 (ScPV1), from a fungus infecting tea plant, marking the first report of a partitivirus from a phytopathogenic fungus infecting tea plant. ScPV1 is characterized by two dsRNA genomic components encapsidated in particles of varying sizes, along with an RNA-dependent RNA polymerase protein of an expected size and containing some unique amino acids, indicating its distinct molecular and morphological traits. Our biological tests on transfectants generated via protoplast transfection with purified virions have rigorously 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 and exhibiting dual effects on a phytopathogenic fungus through virion-transfection, as well as the first case of a partitivirus conferring hypervirulence while promoting 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.