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Contributed by Marc Van Montagu, August 30, 2019 (sent for review April 22, 2019; reviewed by Bob B. Buchanan, Lars I. Leichert, and Markus Schwarzländer)
Significance
Cysteine oxidation can induce structural and functional protein alterations in a reversible manner. This process can be regarded as an on-and-off redox switch that regulates cellular signals in plants, but the full repertoire of redox switches remains largely underexplored. The initial oxidation step of a cysteine is known as S-sulfenylation. Thus far, in plants, the current knowledge of S-sulfenylation is mostly limited to the identification of modified proteins. To uncover the S-sulfenylation landscape in Arabidopsis thaliana at the cysteine site level, we applied a state-of-the-art chemoproteomics approach in plants and obtained a quantitative S-sulfenylation site inventory that will encourage future structural and functional redox studies.
Abstract
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.
Footnotes
↵1J.H., P.W., and B.W. contributed equally to this work.
↵2Present address: Genetics and Physiology of Microalgae, Université de Liège, 4000 Liège, Belgium.
↵3M.V.M., J.Y., F.V.B., and J.M. contributed equally to this work.
- ↵4To whom correspondence may be addressed. Email: marc.vanmontagu{at}ugent.be, yangjing54{at}hotmail.com, frank.vanbreusegem{at}psb.vib-ugent.be, or joris.messens{at}vub.vib.be.
Author contributions: J.H., M.V.M., J.Y., F.V.B., and J.M. designed research; J.H., B.W., C.T., R.B.F., N.B., S.A.M.G., K.W., D.V., and J.Y. performed research; R.B.F. and K.S.C. contributed new reagents/analytic tools; P.W., K.L., and J.Y. analyzed data; and J.H., P.W., K.G., J.Y., F.V.B., and J.M. wrote the paper.
Reviewers: B.B.B., University of California, Berkeley; L.I.L., Ruhr University Bochum; and M.S., University of Münster.
The authors declare no competing interest.
Data deposition: Mass spectrometry proteomics data are available at the ProteomeXchange Consortium via the PRIDE partner repository under accession numbers PXD013495 (BTD chemoproteomics) and PXD013588 (recombinant AtMAPK4).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1906768116/-/DCSupplemental.
Published under the PNAS license.
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Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites
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