Ethylene-Induced Hydrogen Sulfide Negatively Regulates Ethylene Biosynthesis by Persulfidation of ACO in Tomato Under Osmotic Stress

Abstract

A number of recent studies identified hydrogen sulfide (H2S) as an important signal in plant development and adaptation to environmental stress. H2S has been proven to participate in ethylene-induced stomatal closure, but how the signaling pathways of H2S and ethylene interact is still unclear. Here, we reveal how H2S controls the feedback-regulation of ethylene biosynthesis in tomato (Solanum lycopersicum) under osmotic stress. We found that ethylene induced the production of H2S in guard cells. The supply of hypotaurine (HT; a H2S scavenger) or DL-pro-pargylglycine (PAG; a synthetic inhibitor of H2S) removed the effect of ethylene or osmotic stress on stomatal closure. This suggests that ethylene-induced H2S is a downstream component of osmotic stress signaling, which is required for ethylene-induced stomatal closure under osmotic stress. We further found that H2S inhibited ethylene synthesis through inhibiting the activity of 1-aminocyclopropane-1-carboxylic acid (ACC) oxidases (ACOs) by persulfidation. A modified biotin-switch method (MBST) showed that H2S can induce persulfidation of LeACO1 and LeACO2 in a dose-dependent manner, and that persulfidation inhibits the activity of LeACO1 and LeACO2. We also found that LeACO1 is persulfidated at cysteine 60. These data suggested that ethylene-induced H2S negatively regulates ethylene biosynthesis by persulfidation of LeACOs. In addition, H2S was also found to inhibit the expression of LeACO genes. The results provide insight on the general mode of action of H2S and contribute to a better understanding of a plant’s response to osmotic stress.

Abscisic acid‐triggered guard cell l‐cysteine desulfhydrase function and in situ hydrogen sulfide production contributes to heme oxygenase‐modulated stomatal closure

“…These results strongly indicated that other unknown components may be involved in the ABA-activated DES1 transcription. Subsequently, a H 2 S-specific fluorescent probe (7-Azido-4-methylcoumarin) was adopted to monitor the changes in H 2 S production in the guard cells (Jia et al, 2018), which displayed high selectivity for H 2 S in animal cells. Clearly, the fluorescence intensity was reduced in two independent des1 mutants but enhanced in the pMYB60:DES1 transgenic line, which could be increased by the application of H 2 S donor in both Col-0 and des1 mutant lines (Figures 2a and 4c).…”

“…For H 2 S production in guard cells, epidermal strips of each ecotype were preincubated for 3 hr in opening buffer (10 mM MES, pH 6.15, and 50 mM KCl) under light (120 μE m −2 s −1 ) and loaded with 7‐Azido‐4‐methylcoumarin (10 μM; a fluorogenic probe useful for the detection of H 2 S; Sigma‐Aldrich; Jia et al, ) for 40 min before washing in MES buffer three times for 15 min each. Subsequently, samples were treated for 1 hr with different chemicals indicated in the figure legends.…”

Hydrogen Sulfide: From a Toxic Molecule to a Key Molecule of Cell Life

“…The actin cytoskeleton and root hair growth are regulated through persulfidation of ACTIN2 [115]. Furthermore, ethylene biosynthesis is regulated by persulfidation of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO1) in tomato [116]. Recently, a peroxisomal proteome study in Arabidopsis revealed that the interplay of different PTMs such as s-nitrosation, nitration, persulfidation, and acetylation regulates redox signaling to protect proteins against oxidative damage [117].…”

“…Several authors have described how exogenous treatments with ET induce L-and D-cysteine desulfhydrase activity, and this H 2 S regulates ethylene-induced stomatal closure in Arabidopsis thaliana and Vicia faba [168,175,176]. A new study revealed that treatments with ET induced H 2 S generation, and feedback regulation was also observed since ethylene-induced H 2 S negatively regulated ethylene biosynthesis; this regulation occurred through the persulfidation of ACO1 in tomato plants [116]. Further investigations have shown that H 2 S may have an antagonistic effect on ethylene, reducing oxidative stress and repressing ethylene synthesis-related gene expression [177].…”

Nitric oxide and hydrogen sulfide crosstalk during heavy metal stress in plants

“…Furthermore, H 2 S was found to repress the expression of genes such as 1‐aminocyclopropane‐1‐carboxylic acid synthase and 1‐aminocyclopropane‐1‐carboxylic acid oxidase (ACO) involved in ethylene biosynthesis. Recently, the mechanism of crosstalk between H 2 S and ethylene during osmotic stress was revealed in tomato (Jia et al ). Ethylene induces the production of H 2 S in guard cells causing stomatal closure.…”