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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2026,4,14]]},"abstract":"<jats:p>Hypovirulence-associated mycoviruses can be frequently isolated in nature despite their likely compromised ecological fitness, but how their fungal hosts survive in natural environments remains largely unresolved. The discovery of more mycoviruses provides opportunities to understand these mycovirus\u2013host relationships. Here, we characterize a capsidless RNA virus, Sclerotinia sclerotiorum ascoshuvirus 1 (SsAShV1), with a 10.7-kb ssRNA genome encoding a polyprotein containing conserved protease domain and RNA-dependent RNA polymerase (RdRP) domain. SsAShV1 shares structural similarities with animal-infecting viruses. SsAShV1 and its phylogenetically related shuviruses form a distinct evolutionary lineage, prompting the proposal to establish the family Shuviridae. SsAShV1 transfection alone induces hypovirulence in two Sclerotiniaceae fungal pathogens, with its 3\u2019-UTR repeat-containing structural region (RCSR) enhancing replication efficiency. In the hypovirulent strain SCH767, which harbors SsAShV1 and five other mycoviruses, we observed a synergistic enhancement of antifungal volatile organic compound (VOC) production that was dependent on the host genetic background. A VOC, 2-ethyl-1-hexanol, exhibited broad-spectrum antimicrobial activity. Our findings reveal an evolutionary trade-off where viral infection shifts the fungal survival strategy from high virulence to enhanced chemical competition, ensuring the persistence of the hypovirulent partnership, and offering valuable insights into the development of a combination of mycovirus-based and VOC-mediated biocontrol strategies.<\/jats:p>","DOI":"10.1073\/pnas.2526822123","type":"journal-article","created":{"date-parts":[[2026,4,6]],"date-time":"2026-04-06T19:12:12Z","timestamp":1775502732000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":5,"title":["Mycoviruses confer hypovirulence but enhance antifungal volatile organic compound production in a phytopathogenic fungus"],"prefix":"10.1073","volume":"123","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-9857-0880","authenticated-orcid":false,"given":"Zhijun","family":"Liu","sequence":"first","affiliation":[{"name":"National Key Laboratory of Agricultural 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Agricultural University","place":["Wuhan, China"]},{"name":"Hubei Provincial Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University","place":["Wuhan, China"]},{"name":"Hubei Hongshan Laboratory","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dan","family":"Zheng","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University","place":["Wuhan, China"]},{"name":"Hubei Provincial Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural University","place":["Wuhan, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueqiong","family":"Xiao","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University","place":["Wuhan, China"]},{"name":"Hubei Provincial Key Laboratory of Plant Pathology, 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Liu . Sclerotinia sclerotiorum ascoshuvirus 1 strain SCH767 polyprotein gene complete cds. GenBank. https:\/\/www.ncbi.nlm.nih.gov\/nuccore\/PX260938. Deposited 13 September 2025."},{"key":"e_1_3_4_64_2","unstructured":"Z. Liu . Data from \u201cNucleotide sequences of viruses SsULV1 SsOLV14 SsMV48 SsMV49 and SsNSRV2 from strain SCH767.\u201d GenBank. https:\/\/www.ncbi.nlm.nih.gov\/nuccore\/?term=PX260946:PX260950[accn]. Deposited 13 September 2025."},{"key":"e_1_3_4_65_2","unstructured":"Z. Liu . Sclerotinia sclerotiorum ascoshuvirus 1 polyprotein gene partial cds. GenBank. https:\/\/www.ncbi.nlm.nih.gov\/nuccore\/PX260939. Deposited 13 September 2025."},{"key":"e_1_3_4_66_2","unstructured":"Z. Liu . Data from \u201cNucleotide sequences of of SsAShV1-related viruses in Sclerotinia sclerotiorum.\u201d GenBank. https:\/\/www.ncbi.nlm.nih.gov\/nuccore\/?term=PX260940:PX260945[accn]. Deposited 13 September 2025."},{"key":"e_1_3_4_67_2","unstructured":"Z. Liu . Data from \u201cViral genome sequences assembled from SRA data.\u201d GenBank. https:\/\/www.ncbi.nlm.nih.gov\/nuccore\/BK074850 BK074851 BK074852 BK074853 BK074854 BK074855 BK074856 BK074857 BK074858 BK074859 BK074860 BK074861 BK074862 BK074863 BK074864 BK074865 BK074866. Deposited 24 March 2026."},{"key":"e_1_3_4_68_2","unstructured":"Z. Liu . Data from \u201cMycoviruses confer hypovirulence but enhance antifungal volatile organic compound production in a phytopathogenic fungus.\u201d Figshare. https:\/\/doi.org\/10.6084\/m9.figshare.30024784.v2. Deposited 2 September 2025."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2526822123","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,6]],"date-time":"2026-04-06T19:13:22Z","timestamp":1775502802000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2526822123"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,6]]},"references-count":68,"journal-issue":{"issue":"15","published-print":{"date-parts":[[2026,4,14]]}},"alternative-id":["10.1073\/pnas.2526822123"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2526822123","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,6]]},"assertion":[{"value":"2025-09-22","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-02-24","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-04-06","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2526822123"}}