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Edited by Jonathan D. G. Jones, The Sainsbury Laboratory, Norwich, United Kingdom, and approved July 1, 2019 (received for review January 9, 2019)
Significance
S-nitrosylation, the addition of a nitric oxide (NO) moiety to a reactive protein cysteine (Cys) thiol to form an S-nitrosothiol (SNO), is emerging as a pivotal redox-based, posttranslational modification (PTM) during plant immune function. However, the Cys target sites of NO bioactivity and the associated consequences on cellular signaling are not well defined. Our findings suggest that S-nitrosylation of small ubiquitin-like modifier (SUMO)-conjugating enzyme 1 (SCE1) at Cys139 controls SUMOylation, a protein-based PTM that negatively regulates plant immunity through conjugation of SUMO1/2. This Cys is evolutionary conserved and specifically S-nitrosylated in the human homolog, UBC9, implying that this mechanism might be conserved across phylogenetic kingdoms.
Abstract
SUMOylation, the covalent attachment of the small ubiquitin-like modifier (SUMO) to target proteins, is emerging as a key modulator of eukaryotic immune function. In plants, a SUMO1/2-dependent process has been proposed to control the deployment of host defense responses. The molecular mechanism underpinning this activity remains to be determined, however. Here we show that increasing nitric oxide levels following pathogen recognition promote S-nitrosylation of the Arabidopsis SUMO E2 enzyme, SCE1, at Cys139. The SUMO-conjugating activities of both SCE1 and its human homolog, UBC9, were inhibited following this modification. Accordingly, mutation of Cys139 resulted in increased levels of SUMO1/2 conjugates, disabled immune responses, and enhanced pathogen susceptibility. Our findings imply that S-nitrosylation of SCE1 at Cys139 enables NO bioactivity to drive immune activation by relieving SUMO1/2-mediated suppression. The control of global SUMOylation is thought to occur predominantly at the level of each substrate via complex local machineries. Our findings uncover a parallel and complementary mechanism by suggesting that total SUMO conjugation may also be regulated directly by SNO formation at SCE1 Cys139. This Cys is evolutionary conserved and specifically S-nitrosylated in UBC9, implying that this immune-related regulatory process might be conserved across phylogenetic kingdoms.
Footnotes
↵1M.J.S. and S.I.M. contributed equally to this work.
↵2Present address: Department of Plant Breeding and Genetics, Faculty of Crop and Food Sciences, PMAS-Arid Agriculture University Rawalpindi, 46300 Rawalpindi, Pakistan.
- ↵3To whom correspondence may be addressed. Email: gloake{at}ed.ac.uk.
Author contributions: M.J.S., S.I.M., S.H.S., and G.J.L. designed research; M.J.S. and S.I.M. performed research; T.L.B., Y.B., and J.J. contributed new reagents/analytic tools; M.J.S., S.I.M., and G.J.L. analyzed data; and M.J.S. and G.J.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1900052116/-/DCSupplemental.
Published under the PNAS license.
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A role for S-nitrosylation of the SUMO-conjugating enzyme SCE1 in plant immunity
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