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Persulfidation-based Modification of Cysteine Desulfhydrase and the NADPH Oxidase RBOHD Controls Guard Cell Abscisic Acid Signaling

Jie Shen, Jing Zhang, Mingjian Zhou, Heng Zhou, Beimi Cui, Cecilia Gotor, Luis C. Romero, Ling Fu, Jing Yang, Christine Helen Foyer, Qiaona Pan, Wenbiao Shen, Yanjie Xie
Jie Shen
aLaboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
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Jing Zhang
aLaboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
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Mingjian Zhou
aLaboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
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Heng Zhou
aLaboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
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Beimi Cui
bInstitute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3BF, United Kingdom
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Cecilia Gotor
cInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas y Universidad de Sevilla, 41092 Sevilla, Spain
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Luis C. Romero
cInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas y Universidad de Sevilla, 41092 Sevilla, Spain
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Ling Fu
dState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences/Beijing, Beijing Institute of Lifeomics, Beijing 102206, China
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Jing Yang
dState Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences/Beijing, Beijing Institute of Lifeomics, Beijing 102206, China
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Christine Helen Foyer
eCentre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, LS2 9JT, United Kingdom
fSchool of Biosciences, College of Life and Environmental Sciences, University of Birmingham, B15 2TT, United Kingdom
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Qiaona Pan
bInstitute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3BF, United Kingdom
gThe Key Laboratory of Biotechnology for Medicinal Plant of Jiangsu Province, School of Life Science, Jiangsu Normal University, Xuzhou 221116
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Wenbiao Shen
aLaboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
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Yanjie Xie
aLaboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, PR China
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Published April 2020. DOI: https://doi.org/10.1105/tpc.19.00826

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  • © 2020 American Society of Plant Biologists. All rights reserved.

Abstract

Hydrogen sulfide (H2S) is a gaseous signaling molecule that regulates diverse cellular signaling pathways through persulfidation, which involves the post-translational modification of specific Cys residues to form persulfides. However, the mechanisms that underlie this important redox-based modification remain poorly understood in higher plants. We have, therefore, analyzed how protein persulfidation acts as a specific and reversible signaling mechanism during the abscisic acid (ABA) response in Arabidopsis (Arabidopsis thaliana). Here we show that ABA stimulates the persulfidation of l-CYSTEINE DESULFHYDRASE1, an important endogenous H2S enzyme, at Cys44 and Cys205 in a redox-dependent manner. Moreover, sustainable H2S accumulation drives persulfidation of the NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG PROTEIN D (RBOHD) at Cys825 and Cys890, enhancing its ability to produce reactive oxygen species. Physiologically, s-persulfidation-induced RBOHD activity is relevant to ABA-induced stomatal closure. Together, these processes form a negative feedback loop that fine-tunes guard cell redox homeostasis and ABA signaling. These findings not only expand our current knowledge of H2S function in the context of guard cell ABA signaling, but also demonstrate the presence of a rapid signal integration mechanism involving specific and reversible redox-based post-translational modifications that occur in response to changing environmental conditions.

  • Received October 22, 2019.
  • Revised January 17, 2020.
  • Accepted February 5, 2020.
  • Published February 5, 2020.
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Persulfidation-based Modification of Cysteine Desulfhydrase and the NADPH Oxidase RBOHD Controls Guard Cell Abscisic Acid Signaling
Jie Shen, Jing Zhang, Mingjian Zhou, Heng Zhou, Beimi Cui, Cecilia Gotor, Luis C. Romero, Ling Fu, Jing Yang, Christine Helen Foyer, Qiaona Pan, Wenbiao Shen, Yanjie Xie
The Plant Cell Apr 2020, 32 (4) 1000-1017; DOI: 10.1105/tpc.19.00826

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Persulfidation-based Modification of Cysteine Desulfhydrase and the NADPH Oxidase RBOHD Controls Guard Cell Abscisic Acid Signaling
Jie Shen, Jing Zhang, Mingjian Zhou, Heng Zhou, Beimi Cui, Cecilia Gotor, Luis C. Romero, Ling Fu, Jing Yang, Christine Helen Foyer, Qiaona Pan, Wenbiao Shen, Yanjie Xie
The Plant Cell Apr 2020, 32 (4) 1000-1017; DOI: 10.1105/tpc.19.00826
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The Plant Cell: 32 (4)
The Plant Cell
Vol. 32, Issue 4
Apr 2020
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