Hydrogen sulfide signaling in plant adaptations to adverse conditions: molecular mechanisms

Abstract

Hydrogen sulfide (H2S) is a signaling molecule that regulates critical processes and allows plants to adapt to adverse conditions. The molecular mechanism underlying H2S action relies on its chemical reactivity, and the most-well characterized mechanism is persulfidation, which involves the modification of protein thiol groups, resulting in the formation of persulfide groups. This modification causes a change of protein function, altering catalytic activity or intracellular location and inducing important physiological effects. H2S cannot react directly with thiols but instead can react with oxidized cysteine residues; therefore, H2O2 signaling through sulfenylation is required for persulfidation. A comparative study performed in this review reveals 82% identity between sulfenylome and persulfidome. With regard to abscisic acid (ABA) signaling, widespread evidence shows an interconnection between H2S and ABA in the plant response to environmental stress. Proteomic analyses have revealed persulfidation of several proteins involved in the ABA signaling network and have shown that persulfidation is triggered in response to ABA. In guard cells, a complex interaction of H2S and ABA signaling has also been described, and the persulfidation of specific signaling components seems to be the underlying mechanism.

Keywords: Abscisic acid; persulfidation; proteomics; redox modifications; stomatal movement; sulfenylation.

Fig. 1.

Schematic representation of the temporal dynamic of protein sulfenylation (P-SOH) and persulfidation (P-SSH) in different cell types (after Zivanovic et al., 2019). After a transient ROS production induced by developmental or stress signals, the levels of sulfenylation in proteins are increased, accompanied by an increase in the activity of sulfide-generating enzymes and/or induction of low molecular weight (LMW) thiols, followed by a transient increase in protein persulfidation reversed by the action of reducing enzymes such as the thioredoxin system (Trx/TrxR). The rate constants for the reaction of R-SOH with LMW thiols and H₂S at physiological pH 7.4 are shown (Cuevasanta et al., 2015).

Fig. 2.

Comparison of persulfidated and sulfenylated proteins. (A) Venn diagram showing the number of proteins. (B) Fold change enrichment of GO terms of common proteins modified by sulfenylation and persulfidation. Analysis was performed with PANTHER software. The numbers beside the bars indicate the number of proteins associated with each GO term for the input set.

Fig. 3.

Gene Ontology (GO) enrichment. (A) GO enrichment of ABA-induced persulfidated proteins involved in response to stimulus. (B) GO enrichment of persulfidated targets in response to ABA susceptible to sulfenylation. The P-value for each GO term is annotated in red numbers.

Fig. 4.

Graphical model of interconnections between H₂S and ABA signaling networks in guard cells through the persulfidation of specific proteins. Under various environmental stress conditions, in guard cells, ABA concentrations increase and trigger the DES1 activity to induce the production of H₂S to persulfidate specific protein targets. DES1 itself is persulfidated at Cys44 and Cys205, and causes the persulfidation of open stomata 1 (OST1) at Cys131 and Cys137, the NADPH oxidase RBOHD at Cys825 and Cys890, and ABI4 at Cys250. Persulfidated RBOHD produces a ROS burst that results in stomatal closure. Overaccumulation of ROS induces persulfide oxidation leading to ABA desensitivity. Persulfidated ABI4 promotes MAPKKK18 transactivation and MAPK signaling.