Hydrogen sulfide signaling in plant response to temperature stress

Abstract

For the past 300 years, hydrogen sulfide (H₂S) has been considered a toxic gas. Nowadays, it has been found to be a novel signaling molecule in plants involved in the regulation of cellular metabolism, seed germination, plant growth, development, and response to environmental stresses, including high temperature (HT) and low temperature (LT). As a signaling molecule, H₂S can be actively synthesized and degraded in the cytosol, chloroplasts, and mitochondria of plant cells by enzymatic and non-enzymatic pathways to maintain homeostasis. To date, plant receptors for H₂S have not been found. It usually exerts physiological functions through the persulfidation of target proteins. In the past 10 years, H₂S signaling in plants has gained much attention. Therefore, in this review, based on that same attention, H₂S homeostasis, protein persulfidation, and the signaling role of H₂S in plant response to HT and LT stress were summarized. Also, the common mechanisms of H₂S-induced HT and LT tolerance in plants were updated. These mechanisms involve restoration of biomembrane integrity, synthesis of stress proteins, enhancement of the antioxidant system and methylglyoxal (MG) detoxification system, improvement of the water homeostasis system, and reestablishment of Ca²⁺ homeostasis and acid-base balance. These updates lay the foundation for further understanding the physiological functions of H₂S and acquiring temperature-stress-resistant crops to develop sustainable food and agriculture.

Keywords: high and low temperature; hydrogen sulfide; protein persulfidation; stress tolerance; temperature stress.

Figure 1

Hydrogen sulfide (H₂S) anabolism in plants. AS, allyl sulfur; CA, carbonic anhydrase; L-Cys, L-cysteine; D-Cys, D-cysteine; CAS, β-cyanoalanine synthase; Cya, β-cyanoalanine; COS, carbonyl sulfur; CS, cysteine synthetase; LCD, L-cysteine desulfhydrase; DCD, D-cysteine desulfhydrase; DES1, cysteine desulfhydrase1; Fd_red, reduced ferredoxin; Fd_ox, oxidized ferredoxin; Glc, glucose; GRX, glutaredoxin; GSH, glutathione; GSSH, glutathione persulfide; Hcys, homocysteine; ITC, thiocysteine; Met, methionine; MST, 3-mercaptopyruvate sulfur transferase; NH₃, ammonia; NSF, nitrogenase Fe-S cluster; OAS-TL, O-acetylserine (thiol) lyase; P-SH, protein thiols; P-SSH, protein persulfidation P-SSG, glutathionylated proteins; Pyr, pyruvate; SiR, sulfite reductase; TC, isothiocyanate; TRX, thioredoxin; TS, thiosulfate.

Figure 2

Hydrogen sulfide (H₂S) catabolism in plants. Cys, L-cysteine; CS, cysteine synthetase; ETHE1, ethylmalonic encephalopathy 1 protein (persulfide dioxygenase); GSH, glutathione; GSSG, oxidized glutathione; GSSH, glutathione persulfide; H₂O₂, hydrogen peroxide; HOCl, hypochlorite; HS^•, sulfhydryl radical; HSOH, hydrogen thioperoxide; HSOO^•, hydroxysulfinyl radical; HSSH, hydrogen persulfide; NO, nitric oxide; ONOOH, peroxynitrous; P-SH, protein thiols; P-SNO, nitrosylated proteins; P-SOH, sulfenylated proteins; P-SSG, glutathionylated proteins; P-SSH, persulfidated proteins; RNS, reactive nitrogen species; ROOH, hydroperoxides; SO, sulfite oxidase; SQR, sulfite quinone reductase; TMT, thiol-S-methyl-transferase; TST, thiosulfate sulfur transferase; RSSH, hydropersulfides.

Figure 3

high temperature (HT) and low temperature (LT) stress injury to plants. HT and LT stress commonly cause biomembrane damage, protein denaturation, oxidative stress, osmotic stress, methylglyoxal (MG) stress, calcium overload toxicity (mainly calcium phosphate precipitation), acid-base and ion imbalance, and other damage in plants.

Figure 4

Role of hydrogen sulfide (H₂S) in plant response to high temperature (HT) and low temperature (LT) stress. APX, ascorbate peroxidase; CBF, C-repeat binding factor; Ca²⁺, calcium ion; CaM, calmodulin; CAT, catalase; CIE, calcium ion equilibrium; COR, cold regulated proteins; DREB, dehydration response element binding proteins; GSH, glutathione; HSF, heat shock factors; HSP, heat shock proteins; ICE, inducer of CBF expression; IEB, ion equilibrium; MG, methylglyoxal; MGB, MG balance; MAPK, mitogen-activated protein kinase; miRNA, microRNA; OSR, osmoregulation; P-SSG, protein persulfidation; P-MG, protein methylglyoxalation; PVS, pH value stability; RBM, repair of biomembrane; Pro, proline; ROS, reactive oxygen species; ROH, ROS homeostasis; RNS, reactive nitrogen species; SM, secondary metabolites; SOD, superoxide dismutase; SPB, stress protein biosynthesis; SS, soluble sugars; Tre, trehalose.