A role for S-nitrosylation of the SUMO-conjugating enzyme SCE1 in plant immunity

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.

Nitric oxide signalling in plant nanobiology: current status and perspectives

“…Nitric oxide has long been known as a regulator of pathogen defence responses in plants (Durner et al, 1998;Delledonne et al, 1998;Wang et al, 2009;Yun et al, 2011;Trapet et al, 2015;Skelly et al, 2019). Recently, Chandra et al, (2017) examined the involvement of the NO signal in CNP-triggered innate immunity in tea (Camellia sinensis).…”

Crosstalk between Ubiquitination and Other Post-translational Protein Modifications in Plant Immunity

“…While less studies have been reported, the crosstalk between PTMs other than ubiquitination might also play important roles in the regulation of plant immunity. For example, the Arabidopsis SUMO E2 enzyme SCE1 is S -nitrosylated at Cys139 as a result of increased nitric oxide levels upon pathogen infection ( Skelly et al., 2019 ). Disabling the S -nitrosylation by mutation of Cys139 resulted in increased levels of SUMO1/2 conjugates, compromised immune responses, and elevated pathogen susceptibility.…”

“…Disabling the S -nitrosylation by mutation of Cys139 resulted in increased levels of SUMO1/2 conjugates, compromised immune responses, and elevated pathogen susceptibility. Thus, S -nitrosylation inhibits the SUMO-conjugating activity of SCE1, leading to relief of SUMO1/2-mediated suppression to drive immune activation ( Skelly et al., 2019 ). Interestingly, the SUMO-conjugating activity of UBC9, the human homolog of SCE1, is also inhibited following S -nitrosylation at Cys139, suggesting that this PTM crosstalk is conserved across phylogenetic kingdoms.…”

Structural and functional insights into nitrosoglutathione reductase from Chlamydomonas reinhardtii

“…Protein S-nitrosylation has emerged as an important regulatory process in plants and hundreds of proteins have been identified as putative S-nitrosylated targets both in vitro and in vivo [ [14] , [15] , [16] , [17] , [18] , [19] , [20] , [21] , [22] ]. However, •NO itself cannot directly react with cysteine thiols, but can readily condense with oxygen leading to the formation of nitrogen dioxide (•NO 2 ).…”