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Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent

Mycovirus-infected fungi can suffer from poor growth, attenuated pigmentation, and virulence. However, the molecular mechanisms of how mycoviruses confer these symptoms remain poorly understood. Here, we report a mycovirus Stemphylium lycopersici alternavirus 1 (SlAV1) isolated from a necrotrophic p...

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Autores principales: Liu, Hong, Wang, Hui, Liao, Xiao Lan, Gao, Bida, Lu, Xun, Sun, Donghui, Gong, Weijie, Zhong, Jie, Zhu, Hongjian, Pan, Xianting, Guo, Li, Deng, Xing Wang, Zhou, Qian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9897477/
https://www.ncbi.nlm.nih.gov/pubmed/36469771
http://dx.doi.org/10.1073/pnas.2214096119
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author Liu, Hong
Wang, Hui
Liao, Xiao Lan
Gao, Bida
Lu, Xun
Sun, Donghui
Gong, Weijie
Zhong, Jie
Zhu, Hongjian
Pan, Xianting
Guo, Li
Deng, Xing Wang
Zhou, Qian
author_facet Liu, Hong
Wang, Hui
Liao, Xiao Lan
Gao, Bida
Lu, Xun
Sun, Donghui
Gong, Weijie
Zhong, Jie
Zhu, Hongjian
Pan, Xianting
Guo, Li
Deng, Xing Wang
Zhou, Qian
author_sort Liu, Hong
collection PubMed
description Mycovirus-infected fungi can suffer from poor growth, attenuated pigmentation, and virulence. However, the molecular mechanisms of how mycoviruses confer these symptoms remain poorly understood. Here, we report a mycovirus Stemphylium lycopersici alternavirus 1 (SlAV1) isolated from a necrotrophic plant pathogen Stemphylium lycopersici that causes altered colony pigmentation and hypovirulence by specifically interfering host biosynthesis of Altersolanol A, a polyketide phytotoxin. SlAV1 significantly down-regulates a fungal polyketide synthase (PKS1), the core enzyme of Altersolanol A biosynthesis. PKS1 deletion mutants do not accumulate Altersolanol A and lose pathogenicity to tomato and lettuce. Transgenic expression of SlAV1 open-reading frame 3 (ORF3) in S. lycopersici inhibits fungal PKS1 expression and Altersolanol A accumulation, leading to symptoms like SlAV1-infected fungal strains. Multiple plant species sprayed with mycelial suspension of S. lycopersici or S. vesicarium strains integrating and expressing ORF3 display enhanced resistance against virulent strains, converting the pathogenic fungi into biocontrol agents. Hence, our study not only proves inhibiting a key enzyme of host phytotoxin biosynthesis as a molecular mechanism underlying SlAV1-mediated hypovirulence of Stemphylium spp., but also demonstrates the potential of mycovirus-gene integrated fungi as a potential biocontrol agent to protect plants from fungal diseases.
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spelling pubmed-98974772023-06-05 Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent Liu, Hong Wang, Hui Liao, Xiao Lan Gao, Bida Lu, Xun Sun, Donghui Gong, Weijie Zhong, Jie Zhu, Hongjian Pan, Xianting Guo, Li Deng, Xing Wang Zhou, Qian Proc Natl Acad Sci U S A Biological Sciences Mycovirus-infected fungi can suffer from poor growth, attenuated pigmentation, and virulence. However, the molecular mechanisms of how mycoviruses confer these symptoms remain poorly understood. Here, we report a mycovirus Stemphylium lycopersici alternavirus 1 (SlAV1) isolated from a necrotrophic plant pathogen Stemphylium lycopersici that causes altered colony pigmentation and hypovirulence by specifically interfering host biosynthesis of Altersolanol A, a polyketide phytotoxin. SlAV1 significantly down-regulates a fungal polyketide synthase (PKS1), the core enzyme of Altersolanol A biosynthesis. PKS1 deletion mutants do not accumulate Altersolanol A and lose pathogenicity to tomato and lettuce. Transgenic expression of SlAV1 open-reading frame 3 (ORF3) in S. lycopersici inhibits fungal PKS1 expression and Altersolanol A accumulation, leading to symptoms like SlAV1-infected fungal strains. Multiple plant species sprayed with mycelial suspension of S. lycopersici or S. vesicarium strains integrating and expressing ORF3 display enhanced resistance against virulent strains, converting the pathogenic fungi into biocontrol agents. Hence, our study not only proves inhibiting a key enzyme of host phytotoxin biosynthesis as a molecular mechanism underlying SlAV1-mediated hypovirulence of Stemphylium spp., but also demonstrates the potential of mycovirus-gene integrated fungi as a potential biocontrol agent to protect plants from fungal diseases. National Academy of Sciences 2022-12-05 2022-12-13 /pmc/articles/PMC9897477/ /pubmed/36469771 http://dx.doi.org/10.1073/pnas.2214096119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Liu, Hong
Wang, Hui
Liao, Xiao Lan
Gao, Bida
Lu, Xun
Sun, Donghui
Gong, Weijie
Zhong, Jie
Zhu, Hongjian
Pan, Xianting
Guo, Li
Deng, Xing Wang
Zhou, Qian
Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
title Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
title_full Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
title_fullStr Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
title_full_unstemmed Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
title_short Mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
title_sort mycoviral gene integration converts a plant pathogenic fungus into a biocontrol agent
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9897477/
https://www.ncbi.nlm.nih.gov/pubmed/36469771
http://dx.doi.org/10.1073/pnas.2214096119
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