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A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants

Communication between interacting organisms via bioactive molecules is widespread in nature and plays key roles in diverse biological processes. Small RNAs (sRNAs) can travel between host plants and filamentous pathogens to trigger transkingdom RNA interference (RNAi) in recipient cells and modulate...

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Autores principales: Zhu, Chen, Liu, Jia-Hui, Zhao, Jian-Hua, Liu, Ting, Chen, Yun-Ya, Wang, Chun-Han, Zhang, Zhong-Hui, Guo, Hui-Shan, Duan, Cheng-Guo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8944911/
https://www.ncbi.nlm.nih.gov/pubmed/35290117
http://dx.doi.org/10.1073/pnas.2114583119
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author Zhu, Chen
Liu, Jia-Hui
Zhao, Jian-Hua
Liu, Ting
Chen, Yun-Ya
Wang, Chun-Han
Zhang, Zhong-Hui
Guo, Hui-Shan
Duan, Cheng-Guo
author_facet Zhu, Chen
Liu, Jia-Hui
Zhao, Jian-Hua
Liu, Ting
Chen, Yun-Ya
Wang, Chun-Han
Zhang, Zhong-Hui
Guo, Hui-Shan
Duan, Cheng-Guo
author_sort Zhu, Chen
collection PubMed
description Communication between interacting organisms via bioactive molecules is widespread in nature and plays key roles in diverse biological processes. Small RNAs (sRNAs) can travel between host plants and filamentous pathogens to trigger transkingdom RNA interference (RNAi) in recipient cells and modulate plant defense and pathogen virulence. However, how fungal pathogens counteract transkingdom antifungal RNAi has rarely been reported. Here we show that a secretory protein VdSSR1 (secretory silencing repressor 1) from Verticillium dahliae, a soil-borne phytopathogenic fungus that causes wilt diseases in a wide range of plant hosts, is required for fungal virulence in plants. VdSSR1 can translocate to plant nucleus and serve as a general suppressor of sRNA nucleocytoplasmic shuttling. We further reveal that VdSSR1 sequesters ALY family proteins, adaptors of the TREX complex, to interfere with nuclear export of the AGO1–microRNA (AGO1–miRNA) complex, leading to a great attenuation in cytoplasmic AGO1 protein and sRNA levels. With this mechanism, V. dahliae can suppress the accumulation of mobile plant miRNAs in fungal cells and succedent transkingdom silencing of virulence genes, thereby increasing its virulence in plants. Our findings reveal a mechanism by which phytopathogenic fungi antagonize antifungal RNAi-dependent plant immunity and expand the understanding on the complex interaction between host and filamentous pathogens.
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spelling pubmed-89449112022-09-15 A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants Zhu, Chen Liu, Jia-Hui Zhao, Jian-Hua Liu, Ting Chen, Yun-Ya Wang, Chun-Han Zhang, Zhong-Hui Guo, Hui-Shan Duan, Cheng-Guo Proc Natl Acad Sci U S A Biological Sciences Communication between interacting organisms via bioactive molecules is widespread in nature and plays key roles in diverse biological processes. Small RNAs (sRNAs) can travel between host plants and filamentous pathogens to trigger transkingdom RNA interference (RNAi) in recipient cells and modulate plant defense and pathogen virulence. However, how fungal pathogens counteract transkingdom antifungal RNAi has rarely been reported. Here we show that a secretory protein VdSSR1 (secretory silencing repressor 1) from Verticillium dahliae, a soil-borne phytopathogenic fungus that causes wilt diseases in a wide range of plant hosts, is required for fungal virulence in plants. VdSSR1 can translocate to plant nucleus and serve as a general suppressor of sRNA nucleocytoplasmic shuttling. We further reveal that VdSSR1 sequesters ALY family proteins, adaptors of the TREX complex, to interfere with nuclear export of the AGO1–microRNA (AGO1–miRNA) complex, leading to a great attenuation in cytoplasmic AGO1 protein and sRNA levels. With this mechanism, V. dahliae can suppress the accumulation of mobile plant miRNAs in fungal cells and succedent transkingdom silencing of virulence genes, thereby increasing its virulence in plants. Our findings reveal a mechanism by which phytopathogenic fungi antagonize antifungal RNAi-dependent plant immunity and expand the understanding on the complex interaction between host and filamentous pathogens. National Academy of Sciences 2022-03-15 2022-03-22 /pmc/articles/PMC8944911/ /pubmed/35290117 http://dx.doi.org/10.1073/pnas.2114583119 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
Zhu, Chen
Liu, Jia-Hui
Zhao, Jian-Hua
Liu, Ting
Chen, Yun-Ya
Wang, Chun-Han
Zhang, Zhong-Hui
Guo, Hui-Shan
Duan, Cheng-Guo
A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants
title A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants
title_full A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants
title_fullStr A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants
title_full_unstemmed A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants
title_short A fungal effector suppresses the nuclear export of AGO1–miRNA complex to promote infection in plants
title_sort fungal effector suppresses the nuclear export of ago1–mirna complex to promote infection in plants
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8944911/
https://www.ncbi.nlm.nih.gov/pubmed/35290117
http://dx.doi.org/10.1073/pnas.2114583119
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