Exploring the interaction between endornavirus and
Sclerotinia sclerotiorum
: mechanisms of phytopathogenic fungal virulence and antivirus
Authors: Mu Fan , Xia Jinsheng , Jia Jichun , Jiang Daohong , Zhang Baojun , Fu Yanping , Cheng Jiaseng , Xie Jiatao 
Published: February 2025

Hypovirulence-associated mycoviruses have the potential as biocontrol agents for plant fungal disease management, and exploration of the interactions between these mycoviruses and phytopathogenic fungi can provide opportunities to elucidate the underlying mechanisms of hypovirulence and antiviruses. We previously found that Sclerotinia sclerotiorum endornavirus 3 (SsEV3), belonging to the genus
Betaendornavirus
within the family
Endornaviridae
, confers hypovirulence on the phytopathogenic fungus
Sclerotinia sclerotiorum
, but the underlying mechanisms remains unclear. In this study, we found that the SsEV3-infected strain produced fewer sclerotia, failed to form infection cushions on plant hosts, exhibited increased cell vacuolation, and was more sensitive to abiotic stresses. SsEV3 infection evoked transcriptional rewiring in
S. sclerotiorum
, affecting genes related to virulence factors for pathogenicity and RNAi pathway for antiviruses. An unknown biological function of gene
Sssnf1
was downregulated following SsEV3 infection. Deletion of
Sssnf1
impaired infection cushion formation and decreased virulence of
S. sclerotiorum
. Five key RNAi-related genes were significantly upregulated, and deletion of
Ssdcl2
contributed to SsEV3 accumulation. Additionally, we identified a hypothetical protein encoded by
Sshp1
that directly interacts with the RNA-dependent RNA polymerase (RdRp) domain encoded by SsEV3. Although the deletion mutants of
Sshp1
exhibited normal colony morphology, they showed higher SsEV3 accumulation and reduced resistance to reactive oxygen species, indicating that this gene
,
similar to RNAi-related genes, plays an antiviral role in response to SsEV3 infection and may represent a new antivirus factor. Therefore, examination of the interaction between endornavirus and
S. sclerotiorum
provides new insights into the mechanisms of antivirus and virulence in phytopathogenic fungi.

IMPORTANCE

Hypovirulence-associated mycoviruses have emerged as promising biocontrol agents, and studying their interactions with phytopathogenic fungi helps uncover mechanisms of fungal pathogenesis and antiviral defense. This study provides critical insights into the interaction between
Sclerotinia sclerotiorum
and its hypovirulence-associated endornavirus, SsEV3, elucidating the molecular mechanisms underlying mycovirus-induced changes in fungal virulence and antivirus defense. SsEV3 infection not only impairs fungal virulence traits, including infection cushion formation and sclerotial production but also triggers host antiviral responses involving typical RNA interference pathways. New virulence factors, such as
Sssnf1
, and antiviral factors, such as
Sshp1
, were identified based on the established interaction system between
S. sclerotiorum
and endornavirus. These findings deepen our understanding of fungus-mycovirus interactions, highlighting the role of SsEV3 in reducing the virulence of
S. sclerotiorum
, and facilitating the development of mycovirus-based biological control strategies.