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.