Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

[en] Hydrogen peroxide (H2O2) is an important messenger molecule for diverse cellular processes. H2O2 oxidizes proteinaceous cysteinyl thiols to sulfenic acid, also known as S-sulfenylation, thereby affecting the protein conformation and functionality. Although many proteins have been identified as S-sulfenylation targets in plants, site-specific mapping and quantification remain largely unexplored. By means of a peptide-centric chemoproteomics approach, we mapped 1,537 S-sulfenylated sites on more than 1,000 proteins in Arabidopsis thaliana cells. Proteins involved in RNA homeostasis and metabolism were identified as hotspots for S-sulfenylation. Moreover, S-sulfenylation frequently occurred on cysteines located at catalytic sites of enzymes or on cysteines involved in metal binding, hinting at a direct mode of action for redox regulation. Comparison of human and Arabidopsis S-sulfenylation datasets provided 155 conserved S-sulfenylated cysteines, including Cys181 of the Arabidopsis MITOGEN-ACTIVATED PROTEIN KINASE4 (AtMAPK4) that corresponds to Cys161 in the human MAPK1, which has been identified previously as being S-sulfenylated. We show that, by replacing Cys181 of recombinant AtMAPK4 by a redox-insensitive serine residue, the kinase activity decreased, indicating the importance of this noncatalytic cysteine for the kinase mechanism. Altogether, we quantitatively mapped the S-sulfenylated cysteines in Arabidopsis cells under H2O2 stress and thereby generated a comprehensive view on the S-sulfenylation landscape that will facilitate downstream plant redox studies. © 2019 National Academy of Sciences. All rights reserved.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Huang, Jingjing ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

Willems, P.; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, 9052, Belgium, Center for Plant Systems Biology, VIB, Ghent, 9052, Belgium, Department of Biomolecular Medicine, Ghent University, Ghent, 9000, Belgium, Center for Medical Biotechnology, VIB, Ghent, 9000, Belgium

Wei, B.; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, 9052, Belgium, Center for Plant Systems Biology, VIB, Ghent, 9052, Belgium, Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Tian, C.; State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences, Beijing Institute of Lifeomics, Beijing, 102206, China

Ferreira, R. B.; Department of Chemistry, Scripps Research Institute, Jupiter, FL 33458, United States

Bodra, N.; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, 9052, Belgium, Center for Plant Systems Biology, VIB, Ghent, 9052, Belgium, Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Martínez Gache, S. A.; Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Wahni, K.; Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Liu, K.; State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences, Beijing Institute of Lifeomics, Beijing, 102206, China

Vertommen, D.; de Duve Institute, Université Catholique de Louvain, Brussels, 1200, Belgium

More authors (6 more)

Language :

English

Title :

Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

Publication date :

2019

Journal title :

Proceedings of the National Academy of Sciences of the United States of America

ISSN :

0027-8424

eISSN :

1091-6490

Publisher :

National Academy of Sciences

Volume :

116

Issue :

Pages :

20256-20261

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

BOF - Bijzonder Onderzoeksfonds
CSC - China Scholarship Council
F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 30 May 2020

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