A novel partitivirus conferring hypovirulence by affecting vesicle transport in the fungus Colletotrichum

Abstract

Colletotrichum spp. are economically important phytopathogenic fungi that cause anthracnose in a variety of plant species worldwide. Hypovirulence-associated mycoviruses provide new options for the biological control of plant fungal diseases. Here, we found a novel partitivirus from Colletotrichum alienum and named it Colletotrichum alienum partitivirus 1 (CaPV1). CaPV1 contained two dsRNA segments encoding an RNA-dependent RNA polymerase and a capsid protein and was classified under the genus Gammapartitivirus of the family Partitiviridae . CaPV1 significantly decreased host virulence, mycelial growth, appressorial development, and appressorium turgor but increased conidial production with abnormal morphology. In addition, CaPV1 could be successfully transfected into other Colletotrichum species, including C. fructicola , C. spaethianum , and C. gloeosporioides, and caused hypovirulence, indicating the broad application potential of this virus. CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum . Notably, some genes related to vesicle transport in the CaPV1-infected strain were downregulated, consistent with the impaired endocytosis pathway in this fungus. When the Rab gene CaRab7, which is associated with endocytosis in vesicle transport, was knocked out, the virulence of the mutants was reduced. Overall, our findings demonstrated that CaPV1 has the potential to control anthracnose caused by Colletotrichum , and the mechanism by which Colletotrichum induces hypovirulence is caused by affecting vesicle transport. IMPORTANCE Colletotrichum is a kind of economically important phytopathogenic fungi that cause anthracnose disease in a variety of plant species worldwide. We found a novel mycovirus of the Gammapartitiviru s genus and Partitiviridae family from the phytopathogenic fungus Colletotrichum alienum and named it CaPV1. This study revealed that CaPV1 infection significantly decreased host virulence and fitness by affecting mycelial growth, appressorial development, and appressorium turgor. In addition, CaPV1 could also infect other Colletotrichum species, including C. fructicola , C. spaethianum , and C. gloeosporioides , by viral particle transfection and resulting in hypovirulence of these Colletotrichum species. Transcriptomic analysis showed that CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum , especially the genes involved in vesicle transport. Moreover, endocytosis and gene knockout assays demonstrated that the mechanism underlying CaPV1-induced hypovirulence is, at least in part, caused by affecting the vesicle transport of the host fungus. This study provided insights into the mechanisms underlying the pathogenesis of Colletotrichum species and mycovirus-fungus interactions, linking the role of mycovirus and fungus vesicle transport systems in shaping fungal pathogenicity.

Molecular Characterization of the First Partitivirus from a Causal Agent of Salvia miltiorrhiza Dry Rot

“…A mass of partitiviruses have been found from a wide variety of phytopathogenic fungi, oomycetes, biological control fungi, and even human pathogenic fungi [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 ]. Partitiviruses generally have a typical genome composed of two major dsRNA segments and each one contains a single ORF encoding RdRP or CP, respectively [ 18 , 47 ].…”

“…A mass of partitiviruses have been found from a wide variety of phytopathogenic fungi, oomycetes, biological control fungi, and even human pathogenic fungi [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 ]. Partitiviruses generally have a typical genome composed of two major dsRNA segments and each one contains a single ORF encoding RdRP or CP, respectively [ 18 , 47 ]. Currently, viruses in the Partitiviridae family are divided into five recognized genera: Alphapartitivirus , Betapartitivirus , Cryspovirus , Deltapartitivirus , Gammapartitivirus , and two proposed genera: Epsilonpartitivirus , Zetapartitivirus [ 6 , 18 ].…”

“…For the fungi host, the members of the family Partitiviridae have been reported from phytopathogenic fungi ( Aspergillus fumigatus , Botrytis cinerea , Cytospora sacchari , Rhizoctonia solani , Ustilaginoidea virens , etc. ), oomycete ( Pythium nunn ), biological control fungi ( Trichoderma harzianum ), and even human pathogenic fungi ( Talaromyces marneffei ) [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 ]. In general, the mycoviruses in this family contain two dsRNA segments which have a 1.4 to 2.4 kb genome.…”

“…Each of the dsRNA segments consists of one open reading frame (ORF), encoding the RNA-dependent RNA polymerase (RdRp) and the capsid protein (CP), respectively [ 6 , 7 ]. According to evolutionary analysis, viruses in the Partitiviridae family are divided into five recognized and two proposed genera: Alphapartitivirus , Betapartitivirus , Cryspovirus , Deltapartitivirus , Gammapartitivirus , Epsilonpartitivirus, and Zetapartitivirus [ 6 , 18 , 22 ].…”

“…[ 16 , 24 , 25 , 26 ]. The members of the partitivirus also have some hypovirulence-associated mycoviruses, like Sclerotinia sclerotiorum partitivirus 1 (SsPV1/WF-1), Colletotrichum liriopes partitivirus 1 (ClPV1), Botrytis cinerea partitivirus 2 (BcPV2), and Colletotrichum alienum partitivirus 1 (CaPV1) [ 16 , 17 , 18 , 27 ]. Some partitiviruses induced host hypovirulence by co-infecting with other mycoviruses, like Rosellinia necatrix partitivirus 1 (RnPV1) and Rosellinia necatrix partitivirus 10 (RnPV10) [ 20 , 28 ].…”