Hydrogen Sulfide Signaling in Plants: Emerging Roles of Protein Persulfidation

Abstract

Hydrogen sulfide (H2S) has been largely referred as a toxic gas and environmental hazard, but recent years, it has emerged as an important gas-signaling molecule with effects on multiple physiological processes in both animal and plant systems. The regulatory functions of H2S in plants are involved in important processes such as the modulation of defense responses, plant growth and development, and the regulation of senescence and maturation. The main signaling pathway involving sulfide has been proven to be through protein persulfidation (alternatively called S-sulfhydration), in which the thiol group of cysteine (-SH) in proteins is modified into a persulfide group (-SSH). This modification may cause functional changes in protein activities, structures, and subcellular localizations of the target proteins. New shotgun proteomic approaches and bioinformatic analyses have revealed that persulfidated cysteines regulate important biological processes, highlighting their importance in cell signaling, since about one in 20 proteins in Arabidopsis is persulfidated. During oxidative stress, an increased persulfidation has been reported and speculated that persulfidation is the protective mechanism for protein oxidative damage. Nevertheless, cysteine residues are also oxidized to different post-translational modifications such S-nitrosylation or S-sulfenylation, which seems to be interconvertible. Thus, it must imply a tight cysteine redox regulation essential for cell survival. This review is aimed to focus on the current knowledge of protein persulfidation and addresses the regulation mechanisms that are disclosed based on the knowledge from other cysteine modifications.

Inhibition of NADP‐malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits

“…Other secondary sulfur compounds, including polysulfides (Münchberg et al ), glucosinolates (Hasanuzzaman et al ) and phytochelatins, which play important physiological roles, are involved in mechanisms of response to stress (Gupta et al 2013, Ruíz‐Torres et al , Rodríguez‐Ruiz et al ). Hydrogen sulfide (H 2 S), which is generated in the Cys metabolism, is now recognized as an important signaling molecule capable of regulating proteins through a posttranslational modification called persulfidation (Filipovic and Jovanovic , Aroca et al ). This molecule is involved in the regulation of physiological processes such as seed germination, root development, stomatal movements, senescence, fruit ripening as well as responses to environmental changes (Zhang 2016, Corpas et al ).…”

HCN Regulates Cellular Processes through Posttranslational Modification of Proteins by S-cyanylation

“…The reaction of cyanide with cystine-containing proteins results in the formation of an S-cyanylated Cys motif that cycles and is subsequently cleaved to release an amino terminal peptide at one end and a 2-imino-thiazolidine-4-carboxylyl COOH-terminal peptide at the other (Catsimpoolas and Wood, 1966;Fasco et al, 2007). The reaction of cyanide ions with disulfide bridges within polypeptides has been considered to be similar to that of other small molecules, such as nitric oxide (NO) or H 2 S, that react with Cys residues to produce Cys modifications (Yamasaki et al, 2016;Aroca et al, 2017bAroca et al, , 2018.…”

Reactive Sulfur Species Interact with Other Signal Molecules in Root Nodule Symbiosis in Lotus japonicus

“…However, the target molecules and mechanism of H 2 S have yet to be clarified. Zou et al [38] reported that providing an H 2 S donor promoted nodulation and symbiotic nitrogen fixation in soybean, suggesting that H 2 S positively participates in root nodule symbiosis.Reactive sulfur species (RSS), such as polysulfides, which interact with NO, ROS, and H 2 S in animals and bacteria, are garnering increasing interest [39,40]. RSS are characterized as redox-active sulfur-containing molecules that are able, under physiological conditions, to either oxidize or reduce biomolecules [39].…”

“…The production and function of RSS have been analyzed since the 1960s, mainly in animals and bacteria [44][45][46][47][48][49][50]. RSS interact with NO, ROS, and H 2 S and are expected to function collaboratively with these molecules in plants as well as in animals and bacteria [39,40]. Although the production and function of RSS in plants have been discussed [51][52][53], few reports based on experimental evidence have been published.The purpose of the present study was to investigate whether RSS was involved in root nodule symbiosis.…”

“…Reactive sulfur species (RSS), such as polysulfides, which interact with NO, ROS, and H 2 S in animals and bacteria, are garnering increasing interest [39,40]. RSS are characterized as redox-active sulfur-containing molecules that are able, under physiological conditions, to either oxidize or reduce biomolecules [39].…”