Hydrogen sulfide (H2S) signaling in plant development and stress responses

Abstract

Abstract: Hydrogen sulfide (H₂S) was initially recognized as a toxic gas and its biological functions in mammalian cells have been gradually discovered during the past decades. In the latest decade, numerous studies have revealed that H₂S has versatile functions in plants as well. In this review, we summarize H₂S-mediated sulfur metabolic pathways, as well as the progress in the recognition of its biological functions in plant growth and development, particularly its physiological functions in biotic and abiotic stress responses. Besides direct chemical reactions, nitric oxide (NO) and hydrogen peroxide (H₂O₂) have complex relationships with H₂S in plant signaling, both of which mediate protein post-translational modification (PTM) to attack the cysteine residues. We also discuss recent progress in the research on the three types of PTMs and their biological functions in plants. Finally, we propose the relevant issues that need to be addressed in the future research.

Supplementary information: The online version contains supplementary material available at 10.1007/s42994-021-00035-4.

Keywords: Biotic and abiotic stresses; Growth and development; Hydrogen sulfide; Nitric oxide; Persulfidation; Reactive oxygen species; S-Nitrosylation; S-Sulfenylation; Sulfur metabolism.

Fig. 1

H₂S acts as a node in plant sulfur metabolism. The transport of sulfate from roots is the main way for plants to absorb S elements, which are then transported to all parts of the plant through the xylem vessels. Part of the sulfate entering the cells will be stored in vacuoles, and the other part will enter the assimilation pathway in the chloroplast. After being activated to APS, sulfate is further reduced to sulfite via APS reductase with GSH as the reducing molecule. Then, through a six-electron reaction with reduced ferredoxin, sulfite is reduced to sulfide under the catalysis by SiR. The produced sulfide is a substrate for the synthesis of cysteine. Together with OAS, cysteine is synthesized under the catalysis of OAS-TL enzyme. Cysteine can be degraded to generate H₂S by CDes. Another mode for obtaining S elements is from the atmosphere. H₂S, COS and SO₂ are captured by plants through the stomata. COS can be hydrolyzed to produce H₂S under the action of CA, while SO₂ can be hydrolyzed into sulfite and enter the assimilation pathway. The two absorption pathways interact and restrain each other

Fig. 2

H₂S positively responds to biotic and abiotic stresses in plants. The brown shadow is the items related to oxidative damage; yellow shadow is the antioxidant system; green shadow is the photosynthetic system and pigments; and pink shadow is transporters. AAOs, ABA-aldehyde oxidase; ALS, aluminum sensitive; APX, ascorbate peroxidase; ATGs, autophagy proteins; CAS, cyanoalanine synthase; CaM, calmodulin; CAT, catalase; CBF, C-repeat-binding factors; CBL, calcineurin B-like proteins; CDPK, Ca-dependent protein kinase; CIPK, CBL-interacting protein; COR15, cold responsive 15; Deg, D1 protein degradation-related genes; DHAR, dehydroascorbate reductase; d/l-CDes, d/l-cysteine desulfhydrase; EL, electrolyte leakage; EGase, endo-β-1,4-glucanase; ETR, electron transfer rate; Fv/Fm, potential photochemical efficiency; GSNOR, S-nitrosoglutathione reductase; GR, glutathione reductase; HA, proton pump; Hsp, heat shock protein; H₂S, hydrogen sulfide; ICE, inducer of CBF expression; MDA, malondialdehyde; MDHAR, monodehydroascorbate reductase; NCED, 9-cis-epoxy-carotenoid dioxygenase; NO, nitric oxide; NPQ, non-photochemical quenching; NRT, nitrate transporter; OAS-TL, O-acetylserine (thiol)lyase; PCD, programmed cell death; PDH: proline dehydrogenase; PG, polygalacturonase; PLD, phospholipase D isoforms; PIPs, aquaporins; POD, peroxidase; PPO, polyphenol oxidase; Pro, proline; P5CS, proline synthase; qN, non-photochemical quenching; qP, photochemical quenching; ROS, reactive oxygen species; RNS, reactive nitrogen species; SATs, serine acetyltransferase; SAGs, senescence-associated genes; SOD: superoxide dismutase; SOS, salt overly sensitive; STN8, D1 protein phosphatase; ΦPS II, actual photochemical efficiency; –SH, persulfidation. Arrowheads indicate positive regulatory interaction and flat arrow heads indicate negative regulation

Fig. 3

Endogenous chemical signals in plants involving H₂S, NO and ROS. N₂O₃ is synthesized by NO and O₂ accumulated in the bilayer of cell membrane, and then forms HSNO with H₂S. Extracellularly, HSNO can be directly synthesized by H₂S and NO. HSNO can enhance the membrane permeability of H₂S and NO, which is also the transmembrane transfer mode of cysteine thiols. Intracellularly, H₂S undergoes oxidation and generates sulfate (SO₄²⁻), sulfite (SO₃²⁻), thiosulfate (S₂O₃²⁻), persulfides (RSS⁻), organic (RSS_nSR), inorganic (H₂S_n) polysulfides, and elemental sulfur (S_n), which is controlled by different ratios of H₂S and ROS level

Fig. 4

Multiple post-translational modifications on cysteine residues of proteins. Protein cysteine thiols (RSH) can be sulfonated to produce RSOH with increasing ROS. Upon continuous exposure to ROS, RSOH could further generate irreversible sulfinic (RSO₂H) and sulfonic acids (RSO₃H). On the basis of RSOH, H₂S and NO can be persulfidated and S-nitrosylated, respectively, to produce RSSH and RSNO. In the presence of nitrotransferase, NO can also react directly with RSH to produce RSNO. Once persulfidated cysteine thiols encounter ROS, RSSH will rapidly react with ROS to form adducts (RSSOH, RSSO₂H and RSSO₃H). Among them, RSSH and RSSOH can be reduced back to thiols by the action of the thioredoxin (Trx)