Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis.

Cecilia Gotor,Juan M Benito,Luis C Romero,Angeles Aroca

doi:10.1093/jxb/erx294

Abstract

Hydrogen sulfide-mediated signaling pathways regulate many physiological and pathophysiological processes in mammalian and plant systems. The molecular mechanism by which hydrogen sulfide exerts its action involves the post-translational modification of cysteine residues to form a persulfidated thiol motif, a process called protein persulfidation. We have developed a comparative and quantitative proteomic analysis approach for the detection of endogenous persulfidated proteins in wild-type Arabidopsis and L-CYSTEINE DESULFHYDRASE 1 mutant leaves using the tag-switch method. The 2015 identified persulfidated proteins were isolated from plants grown under controlled conditions, and therefore, at least 5% of the entire Arabidopsis proteome may undergo persulfidation under baseline conditions. Bioinformatic analysis revealed that persulfidated cysteines participate in a wide range of biological functions, regulating important processes such as carbon metabolism, plant responses to abiotic and biotic stresses, plant growth and development, and RNA translation. Quantitative analysis in both genetic backgrounds reveals that protein persulfidation is mainly involved in primary metabolic pathways such as the tricarboxylic acid cycle, glycolysis, and the Calvin cycle, suggesting that this protein modification is a new regulatory component in these pathways.

Highlights

Hydrogen sulfide (H2S) has been referred to as the third gasotransmitter in animal and plant cells and is as important as nitric oxide (NO), carbon monoxide (CO), and hydrogen peroxide (H2O2) (García-Mata and Lamattina, 2010; Vandiver and Snyder, 2012; Kimura, 2014)
We recently reported the presence of persulfidation-modified cysteine residues in 106 proteins from Arabidopsis leaf extracts by using the modified biotin switch method (Aroca et al, 2015)
Protein persulfidation of cysteine residues is an important mechanism involved in diverse biological processes

Summary

Introduction

Hydrogen sulfide (H2S) has been referred to as the third gasotransmitter in animal and plant cells and is as important as nitric oxide (NO), carbon monoxide (CO), and hydrogen peroxide (H2O2) (García-Mata and Lamattina, 2010; Vandiver and Snyder, 2012; Kimura, 2014). These small molecules possess high permeability that allows them to cross biological membranes and to act as signaling molecules. H2S is involved in regulating important physiological processes in plants, such as stomatal closure/ aperture (García-Mata and Lamattina, 2010; Lisjak et al, 2010; Jin et al, 2013; Scuffi et al, 2014; Papanatsiou et al, 2015), the modulation of photosynthesis (Chen et al, 2011), and autophagy regulation (Alvarez et al, 2012b; Gotor et al, 2013; Romero et al, 2014; Laureano-Marin et al, 2016)

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