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An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP

Rice false smut, caused by the ascomycete fungus Ustilaginoidea virens, which infects rice florets before heading, severely threatens rice grain yield and quality worldwide. The U. virens genome encodes a number of glycoside hydrolase (GH) proteins. So far, the functions of these GHs in U. virens ar...

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Autores principales: Zou, Jiaying, Jiang, Chunquan, Qiu, Shanshan, Duan, Guohua, Wang, Guanqun, Li, Dayong, Yu, Siwen, Zhao, Dan, Sun, Wenxian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10576179/
https://www.ncbi.nlm.nih.gov/pubmed/37452482
http://dx.doi.org/10.1111/mpp.13377
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author Zou, Jiaying
Jiang, Chunquan
Qiu, Shanshan
Duan, Guohua
Wang, Guanqun
Li, Dayong
Yu, Siwen
Zhao, Dan
Sun, Wenxian
author_facet Zou, Jiaying
Jiang, Chunquan
Qiu, Shanshan
Duan, Guohua
Wang, Guanqun
Li, Dayong
Yu, Siwen
Zhao, Dan
Sun, Wenxian
author_sort Zou, Jiaying
collection PubMed
description Rice false smut, caused by the ascomycete fungus Ustilaginoidea virens, which infects rice florets before heading, severely threatens rice grain yield and quality worldwide. The U. virens genome encodes a number of glycoside hydrolase (GH) proteins. So far, the functions of these GHs in U. virens are largely unknown. In this study, we identified a GH42 protein secreted by U. virens, named UvGHF1, that exhibits β‐galactosidase activity. UvGHF1 not only functions as an essential virulence factor during U. virens infection, but also serves as a pathogen‐associated molecular pattern (PAMP) in Nicotiana benthamiana and rice. The PAMP activity of UvGHF1 is independent of its β‐galactosidase activity. Moreover, UvGHF1 triggers cell death in N. benthamiana in a BAK1‐dependent manner. Ectopic expression of UvGHF1 in rice induces pattern‐triggered immunity and enhances rice resistance to fungal and bacterial diseases. RNA‐seq analysis revealed that UvGHF1 expression in rice not only activates expression of many defence‐related genes encoding leucine‐rich repeat receptor‐like kinases and WRKY and ERF transcription factors, but also induces diterpenoid biosynthesis and phenylpropanoid biosynthesis pathways. Therefore, UvGHF1 contributes to U. virens virulence, but is also recognized by the rice surveillance system to trigger plant immunity.
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spelling pubmed-105761792023-10-15 An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP Zou, Jiaying Jiang, Chunquan Qiu, Shanshan Duan, Guohua Wang, Guanqun Li, Dayong Yu, Siwen Zhao, Dan Sun, Wenxian Mol Plant Pathol Original Articles Rice false smut, caused by the ascomycete fungus Ustilaginoidea virens, which infects rice florets before heading, severely threatens rice grain yield and quality worldwide. The U. virens genome encodes a number of glycoside hydrolase (GH) proteins. So far, the functions of these GHs in U. virens are largely unknown. In this study, we identified a GH42 protein secreted by U. virens, named UvGHF1, that exhibits β‐galactosidase activity. UvGHF1 not only functions as an essential virulence factor during U. virens infection, but also serves as a pathogen‐associated molecular pattern (PAMP) in Nicotiana benthamiana and rice. The PAMP activity of UvGHF1 is independent of its β‐galactosidase activity. Moreover, UvGHF1 triggers cell death in N. benthamiana in a BAK1‐dependent manner. Ectopic expression of UvGHF1 in rice induces pattern‐triggered immunity and enhances rice resistance to fungal and bacterial diseases. RNA‐seq analysis revealed that UvGHF1 expression in rice not only activates expression of many defence‐related genes encoding leucine‐rich repeat receptor‐like kinases and WRKY and ERF transcription factors, but also induces diterpenoid biosynthesis and phenylpropanoid biosynthesis pathways. Therefore, UvGHF1 contributes to U. virens virulence, but is also recognized by the rice surveillance system to trigger plant immunity. John Wiley and Sons Inc. 2023-07-14 /pmc/articles/PMC10576179/ /pubmed/37452482 http://dx.doi.org/10.1111/mpp.13377 Text en © 2023 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Original Articles
Zou, Jiaying
Jiang, Chunquan
Qiu, Shanshan
Duan, Guohua
Wang, Guanqun
Li, Dayong
Yu, Siwen
Zhao, Dan
Sun, Wenxian
An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP
title An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP
title_full An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP
title_fullStr An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP
title_full_unstemmed An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP
title_short An Ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a PAMP
title_sort ustilaginoidea virens glycoside hydrolase 42 protein is an essential virulence factor and elicits plant immunity as a pamp
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10576179/
https://www.ncbi.nlm.nih.gov/pubmed/37452482
http://dx.doi.org/10.1111/mpp.13377
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