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Abscisic Acid-Triggered Persulfidation of the Cys Protease ATG4 Mediates Regulation of Autophagy by Sulfide

Ana M. Laureano-Marín, Ángeles Aroca, M. Esther Pérez-Pérez, Inmaculada Yruela, Ana Jurado-Flores, Inmaculada Moreno, José L. Crespo, Luis C. Romero, Cecilia Gotor
Ana M. Laureano-Marín
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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  • ORCID record for Ana M. Laureano-Marín
Ángeles Aroca
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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M. Esther Pérez-Pérez
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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Inmaculada Yruela
bEstación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas, 50059 Zaragoza, Spain
cGroup of Biochemistry, Biophysics and Computational Biology (BIFI-Unizar) Joint Unit to Consejo Superior de Investigaciones Científicas, 50059 Zaragoza, Spain
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Ana Jurado-Flores
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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Inmaculada Moreno
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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José L. Crespo
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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Luis C. Romero
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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Cecilia Gotor
aInstituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, 41092 Seville, Spain
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  • For correspondence: gotor@ibvf.csic.es

Published December 2020. DOI: https://doi.org/10.1105/tpc.20.00766

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Abstract

Hydrogen sulfide is a signaling molecule that regulates essential processes in plants, such as autophagy. In Arabidopsis (Arabidopsis thaliana), hydrogen sulfide negatively regulates autophagy independently of reactive oxygen species via an unknown mechanism. Comparative and quantitative proteomic analysis was used to detect abscisic acid-triggered persulfidation that reveals a main role in the control of autophagy mediated by the autophagy-related (ATG) Cys protease AtATG4a. This protease undergoes specific persulfidation of Cys170 that is a part of the characteristic catalytic Cys-His-Asp triad of Cys proteases. Regulation of the ATG4 activity by persulfidation was tested in a heterologous assay using the Chlamydomonas reinhardtii CrATG8 protein as a substrate. Sulfide significantly and reversibly inactivates AtATG4a. The biological significance of the reversible inhibition of the ATG4 by sulfide is supported by the results obtained in Arabidopsis leaves under basal and autophagy-activating conditions. A significant increase in the overall ATG4 proteolytic activity in Arabidopsis was detected under nitrogen starvation and osmotic stress and can be inhibited by sulfide. Therefore, the data strongly suggest that the negative regulation of autophagy by sulfide is mediated by specific persulfidation of the ATG4 protease.

  • Received September 16, 2020.
  • Accepted October 8, 2020.
  • Published October 9, 2020.
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Abscisic Acid-Triggered Persulfidation of the Cys Protease ATG4 Mediates Regulation of Autophagy by Sulfide
Ana M. Laureano-Marín, Ángeles Aroca, M. Esther Pérez-Pérez, Inmaculada Yruela, Ana Jurado-Flores, Inmaculada Moreno, José L. Crespo, Luis C. Romero, Cecilia Gotor
The Plant Cell Dec 2020, 32 (12) 3902-3920; DOI: 10.1105/tpc.20.00766

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Abscisic Acid-Triggered Persulfidation of the Cys Protease ATG4 Mediates Regulation of Autophagy by Sulfide
Ana M. Laureano-Marín, Ángeles Aroca, M. Esther Pérez-Pérez, Inmaculada Yruela, Ana Jurado-Flores, Inmaculada Moreno, José L. Crespo, Luis C. Romero, Cecilia Gotor
The Plant Cell Dec 2020, 32 (12) 3902-3920; DOI: 10.1105/tpc.20.00766
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  • Peer Review Report
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The Plant Cell: 32 (12)
The Plant Cell
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Dec 2020
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