Hypovirulence induced by mycovirus colletotrichum gloeosporioides RNA virus 1 strain Ssa-44.1 in Colletotrichum gloeosporioides: Insights from a multi-omics analysis of host-virus interactions

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Muhammad Kabir Hassan, Liying Sun, Jiraporn Jirakkakul, Treenut Saithong, Saowalak Kalapanulak, Sucheewin Krobthong, Arnatchai Maiuthed, Yingchutrakul Yodying, Bayu Hadi Permana, Lakha Salaipeth

2025 Microbiological Research Vol. 301 Article Cited by 1 Quartile Top Tier

Abstract

Mycovirus infections significantly impact fungal virulence and physiology, inducing either hypovirulence or hypervirulence. This study investigated the hypovirulent effects of Colletotrichum gloeosporioides RNA virus 1 (CgRV1-Ssa-44.1) infection on Colletotrichum gloeosporioides using multi-omics approaches. Transcriptomic analysis identified 261 differentially expressed genes (141 up-regulated, 120 down-regulated), while LC-MS/MS-based proteomic analyses revealed 2222 proteins, including 19 unique to virus-infected samples and 649 unique to virus-free samples. These results highlighted extensive gene and protein expression alterations, emphasizing profound impacts on the host cellular process. Changes in membrane-associated terms and cell wall-related processes suggested that the virus may exploit host structures to facilitate horizontal transfer. The disruption of carbohydrate metabolism and pathways, such as the non-sense mediated mRNA decay (NMD) system, reflected sophisticated viral strategies for suppressing host defenses and redirecting resources for its benefit. Notably, Upregulated genes, such as sorbose reductase and COMPASS complex component SWD2, pointed to adaptive response to stress and survival mechanisms during viral infection. Conversely, downregulated genes like elongation factor 3, survival factor 1, and zuotin, indicated viral manipulation of host cellular machinery to subvert normal processes. Real-time PCR validated these transcriptional changes, confirming the robustness of the findings. The study demonstrates a complex host-virus interplay, where fungal metabolic and adaptive pathways are intricately targeted and exploited. These findings underscore the dual nature of viral subversion strategies, balancing host suppression with survival adaptation. Future functional analyses of key pathways will provide insights into the molecular mechanisms underlying fungal-virus interactions and coevolution. This knowledge could guide the development of novel antifungal strategies applicable to similar host-pathogen systems. © 2025 Elsevier GmbH

Affiliations

Natural Resource Management and Sustainability Program, School of Bioresources and Technology, King Mongkut's University of Technology Thonburi, Bangkuntien, Bangkok, 10150, Thailand; State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Xianyang, China; Pilot Plant Development and Training Institute, King Mongkut's University of Technology Thonburi, Bangkuntien, Bangkok, 10150, Thailand; Bioinformatics and Systems Biology Program, School of Bioresources and Technology, King Mongkut's University of Technology Thonburi, Bang Khun Thian, Bangkok, Thailand; Center for Agricultural Systems Biology (CASB), Systems Biology and Bioinformatics research laboratory, Pilot Plant Development and Training Institute, King Mongkut's University of Technology Thonburi, Bang Khun Thian, Bangkok, Thailand; Center of Excellence in Natural Products Chemistry (CENP), Department of Chemistry, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand; Center of Biopharmaceutical Science for Healthy Ageing, Faculty of Pharmacy, Mahidol University, Bangkok, 10400, Thailand; Department of Pharmacology, Faculty of Pharmacy, Mahidol University, Bangkok, 10400, Thailand; National Center for Genetic Engineering and Biotechnology, NSTDA, Pathum Thani, 12120, Thailand; Department of Biotechnology, Faculty of Food Security, Universitas Negeri Surabaya, Surabaya, 60286, Indonesia; LigniTech-Lignin Technology Research Group, School of Bioresources and Technology, King Mongkut's University of Technology Thonburi, Bangkuntien, Bangkok, 10150, Thailand