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.
Structural analogs of enzyme substrates involved in plant hormone biosynthesis can either inhibit or enhance hormone-related responses depending on their specific chemical characteristics. Ethylene is an important gaseous phytohormone regulating a myriad of physiological and developmental processes. The substrate of the ethylene biosynthesis key enzyme ACC oxidase (ACO), 1-aminocyclopropane-1-carboxylate acid (ACC), is the direct precursor of ethylene. Previous studies have identified a series of ACC analogs as ethylene antagonists competitively binding with ACO. Here, this study identified methyl 1-aminocyclopropanecarboxylate (methyl-ACC), a structural analog of ACC, as an agonist of ethylene response in plants. Methyl-ACC triggered enhanced ethylene-related responses in plants similar to the effects of ACC, such as restrained root elongation, increased root hair number, promoted dark-induced leaf senescence, and accelerated ripening of postharvest tomato fruit. A higher amount of ethylene release was detected from the tomato leaves treated with methyl-ACC than from the mock control. These bioactivities of methyl-ACC render it a potential plant growth regulator (PGR) for the agricultural and postharvest industries. RT-qPCR revealed a generally upregulated expression of the ethylene biosynthesis genes in detached tomato leaves under methyl-ACC treatment. In vivo and in vitro enzymatic activity analyses showed that methyl-ACC had no obvious effect on the total ACO activity in detached tomato leaves nor on the activity of recombinant SlACO1, the predominantly expressed ACO family member in this tissue. This study offers a promising new PGR and adds to the current knowledge on the structure–function-regulation relationship of compounds associated with ethylene biosynthesis. The mechanism by which methyl-ACC exerts its function is discussed.
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