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Molecular Hydrogen Confers Resistance to Rice Stripe Virus

Although molecular hydrogen (H(2)) has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. Here, after rice stripe virus (RSV) infection, H(2) production was pronouncedly stimulated in Zhendao 88, a resistant rice varie...

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Autores principales: Shao, Yudong, Lin, Feng, Wang, Yueqiao, Cheng, Pengfei, Lou, Wang, Wang, Zhaoyun, Liu, Zhiyang, Chen, Dongyue, Guo, Wei, Lan, Ying, Du, Linlin, Zhou, Yijun, Zhou, Tong, Shen, Wenbiao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100981/
https://www.ncbi.nlm.nih.gov/pubmed/36840556
http://dx.doi.org/10.1128/spectrum.04417-22
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author Shao, Yudong
Lin, Feng
Wang, Yueqiao
Cheng, Pengfei
Lou, Wang
Wang, Zhaoyun
Liu, Zhiyang
Chen, Dongyue
Guo, Wei
Lan, Ying
Du, Linlin
Zhou, Yijun
Zhou, Tong
Shen, Wenbiao
author_facet Shao, Yudong
Lin, Feng
Wang, Yueqiao
Cheng, Pengfei
Lou, Wang
Wang, Zhaoyun
Liu, Zhiyang
Chen, Dongyue
Guo, Wei
Lan, Ying
Du, Linlin
Zhou, Yijun
Zhou, Tong
Shen, Wenbiao
author_sort Shao, Yudong
collection PubMed
description Although molecular hydrogen (H(2)) has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. Here, after rice stripe virus (RSV) infection, H(2) production was pronouncedly stimulated in Zhendao 88, a resistant rice variety, compared to that in a susceptible variety (Wuyujing No.3). External H(2) supply remarkably reduced the disease symptoms and RSV coat protein (CP) levels, especially in Wuyujing No.3. The above responses were abolished by the pharmacological inhibition of H(2) production. The transgenic Arabidopsis plants overexpressing a hydrogenase gene from Chlamydomonas reinhardtii also improved plant resistance. In the presence of H(2), the transcription levels of salicylic acid (SA) synthetic genes were stimulated, and the activity of SA glucosyltransferases was suppressed, thus facilitating SA accumulation. Genetic evidence revealed that two SA synthetic mutants of Arabidopsis (sid2-2 and pad4) were more susceptible to RSV than the wild type (WT). The treatments with H(2) failed to improve the resistance to RSV in two SA synthetic mutants. The above results indicated that H(2) enhances rice resistance to RSV infection possibly through the SA-dependent pathway. This study might open a new window for applying the H(2)-based approach to improve plant disease resistance. IMPORTANCE Although molecular hydrogen has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. RSV was considered the most devastating plant virus in rice, since it could cause severe losses in field production. This disease was thus selected as a classical model to explore the interrelationship between molecular hydrogen and plant pathogen resistance. In this study, we discovered that both exogenous and endogenous H(2) could enhance plant resistance against Rice stripe virus infection by regulating salicylic acid signaling. Compared with some frequently used agrochemicals, H(2) is almost nontoxic. We hope that the findings presented here will serve as an opportunity for the scientific community to push hydrogen-based agriculture forward.
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spelling pubmed-101009812023-04-14 Molecular Hydrogen Confers Resistance to Rice Stripe Virus Shao, Yudong Lin, Feng Wang, Yueqiao Cheng, Pengfei Lou, Wang Wang, Zhaoyun Liu, Zhiyang Chen, Dongyue Guo, Wei Lan, Ying Du, Linlin Zhou, Yijun Zhou, Tong Shen, Wenbiao Microbiol Spectr Research Article Although molecular hydrogen (H(2)) has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. Here, after rice stripe virus (RSV) infection, H(2) production was pronouncedly stimulated in Zhendao 88, a resistant rice variety, compared to that in a susceptible variety (Wuyujing No.3). External H(2) supply remarkably reduced the disease symptoms and RSV coat protein (CP) levels, especially in Wuyujing No.3. The above responses were abolished by the pharmacological inhibition of H(2) production. The transgenic Arabidopsis plants overexpressing a hydrogenase gene from Chlamydomonas reinhardtii also improved plant resistance. In the presence of H(2), the transcription levels of salicylic acid (SA) synthetic genes were stimulated, and the activity of SA glucosyltransferases was suppressed, thus facilitating SA accumulation. Genetic evidence revealed that two SA synthetic mutants of Arabidopsis (sid2-2 and pad4) were more susceptible to RSV than the wild type (WT). The treatments with H(2) failed to improve the resistance to RSV in two SA synthetic mutants. The above results indicated that H(2) enhances rice resistance to RSV infection possibly through the SA-dependent pathway. This study might open a new window for applying the H(2)-based approach to improve plant disease resistance. IMPORTANCE Although molecular hydrogen has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. RSV was considered the most devastating plant virus in rice, since it could cause severe losses in field production. This disease was thus selected as a classical model to explore the interrelationship between molecular hydrogen and plant pathogen resistance. In this study, we discovered that both exogenous and endogenous H(2) could enhance plant resistance against Rice stripe virus infection by regulating salicylic acid signaling. Compared with some frequently used agrochemicals, H(2) is almost nontoxic. We hope that the findings presented here will serve as an opportunity for the scientific community to push hydrogen-based agriculture forward. American Society for Microbiology 2023-02-22 /pmc/articles/PMC10100981/ /pubmed/36840556 http://dx.doi.org/10.1128/spectrum.04417-22 Text en Copyright © 2023 Shao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Shao, Yudong
Lin, Feng
Wang, Yueqiao
Cheng, Pengfei
Lou, Wang
Wang, Zhaoyun
Liu, Zhiyang
Chen, Dongyue
Guo, Wei
Lan, Ying
Du, Linlin
Zhou, Yijun
Zhou, Tong
Shen, Wenbiao
Molecular Hydrogen Confers Resistance to Rice Stripe Virus
title Molecular Hydrogen Confers Resistance to Rice Stripe Virus
title_full Molecular Hydrogen Confers Resistance to Rice Stripe Virus
title_fullStr Molecular Hydrogen Confers Resistance to Rice Stripe Virus
title_full_unstemmed Molecular Hydrogen Confers Resistance to Rice Stripe Virus
title_short Molecular Hydrogen Confers Resistance to Rice Stripe Virus
title_sort molecular hydrogen confers resistance to rice stripe virus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100981/
https://www.ncbi.nlm.nih.gov/pubmed/36840556
http://dx.doi.org/10.1128/spectrum.04417-22
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