Hydrogen sulfide signaling in plant response to temperature stress

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.


Introduction
Hydrogen sulfide (H 2 S) has long been deemed a toxic gas since its discovery as a sewer gas in the 1700s (Wang, 2012;Modolo and da-Silva, 2023).H 2 S has a high affinity for heme-containing proteins, such as hemoglobin, myoglobin, cytochrome oxidase, catalase (CAT), and peroxidase (POD), and acts through protein persulfidation.Persulfidation can change the conformation and activity of proteins, leading to disruption of cellular metabolism, and even cell death (Li et al., 2016a;Liu et al., 2021;Li et al., 2022;Yang et al., 2022;Huang and Xie, 2023).At the end of the Permian period, a large amount of H 2 S was accumulated on earth due to volcano eruptions, which caused a rapid decrease of oxygen (O 2 ) in seawater.This decrease promoted the mass proliferation of anaerobic green sulfur bacteria, which used sulfate (SO 4 2-) instead of O 2 for respiration and released a mass of H 2 S. The released H 2 S entered the atmosphere and land, therefore leading to the extinction of 95% of marine species and 70% of terrestrial vertebrates (Wang, 2012;Li et al., 2016a, Li et al., 2022).In plants, H 2 S can result in necrosis, shedding, and growth inhibition of leaves and can inhibit the uptake of mineral elements, such as phosphate, by roots (Wang, 2012;Liu et al., 2021;Yang et al., 2022;Huang and Xie, 2023).Recently, Zhang et al. (2017) reported that H 2 S could inhibit taproot growth and regulate root system architecture in Arabidopsis plants by inducing reactive oxygen species (ROS) and nitric oxide (NO) to generate oxidative and nitrosative stress.
Promisingly, H 2 S has now been found to be a novel signaling molecule involved in many physiological processes in plants.These processes include cell metabolism and division, seed germination and dormancy, plant growth and development, organ maturation and senescence, and plant response to environmental stresses, including high temperature (HT) and low temperature (LT) (Li et al., 2016a;Liu et al., 2021;Wang et al., 2021;Yang et al., 2022;Huang et al., 2023).H 2 S, similar to other signaling molecules, such as calcium ion (Ca 2+ ), hydrogen peroxide (H 2 O 2 ), NO, methylglyoxal (MG), and glutamic acid, has a dual role, namely as a signaling molecule at low concentrations and as a toxic agent at high concentrations (Qiu et al., 2020;Iqbal et al., 2022;Pande et al., 2022;Huang and Xie, 2023;Mhamdi, 2023).Therefore, it must maintain homeostasis in plant cells under normal physiological and unfavorable environmental conditions.H 2 S homeostasis can be tightly regulated by enzymatic and non-enzymatic pathways, which are described as follows (Li et al., 2016a;Liu et al., 2021;Moseler et al., 2021;Li et al., 2022;Citi et al., 2023;Pedre et al., 2023).
In the past decade, H 2 S, as a pleiotropic signaling molecule in plants has gained much attention, especially in its metabolism and physiological function under HT and LT stress conditions (Li et al., 2016a;Liu et al., 2021;Moseler et al., 2021;Wang et al., 2021;Yang et al., 2022;Citi et al., 2023;Huang and Xie, 2023;Pedre et al., 2023).Therefore, in this review, based on that same attention, the enzymatic and non-enzymatic pathways of H 2 S homeostasis, protein persulfidation, and the signaling role of H 2 S in plant response to HT and LT stress were updated.This laid the groundwork for further understanding the physiological function of H 2 S and the acquisition of temperature-stress-resistant crops to develop sustainable food and agriculture.

H 2 S homeostasis
Because H 2 S is a toxic agent at high concentrations, it must maintain homeostasis in plant cells.Its homeostasis is tightly controlled by biosynthesis and degradation via enzymatic and non-enzymatic pathways (Figure 1).The mechanisms controlling H 2 S homeostasis in plant cells are detailed below.

Enzymatic pathways for H 2 S biosynthesis
Involvement in multiple pathways is one of the characteristics of signaling molecules in plants (Liu et al., 2021;Wang et al., 2021).In general, H 2 S can be biosynthesized via enzymatic pathways in the cytosol, chloroplasts, and mitochondria of plants.These enzymes include L-cysteine (L-Cys) desulfhydrase (LCD), D-cysteine (D-Cys) desulfhydrase (DCD), O-acetyl-serine (thiol) lyase (OAS-TL), sulfite reductase (SiR), b-cyanoalanine synthase (CAS), and nitrogenase Fe-S cluster-like (NFS) (Liu et al., 2021;Wang et al., 2021;Huang and Xie, 2023) (Figure 1).In the cytosol, H 2 S can be produced from L-Cys or D-Cys under the catalysis of LCD or DCD, meanwhile releasing ammonia (NH 3 ) and pyruvate (Pyr).In addition, L-Cys desulfhydrase 1 (DES1), an LCD homolog, can catalyze L-Cys to H 2 S, resulting in the production of NH 3 and Pyr.H 2 S can also be used to synthesize L-Cys (by OAS-TL, also known as L-Cys synthetase, CS), whose reverse reaction can produce H 2 S and O-acetyl-serine (OAS) (Li et al., 2016a;Yang et al., 2022;Huang and Xie, 2023).In chloroplasts, sulfite (SO 3 2-), which is reduced from SO 4 2-, can be converted to H 2 S by SiR using ferredoxin (Fd red ) as a cofactor.Similarly, NFS can use L-Cys to synthesize H 2 S (Aroca et al., 2020;Saud et al., 2022;Huang and Xie, 2023).In mitochondria, H 2 S can be formed under the catalysis of CAS using hydrogen cyanide (HCN) and L-Cys as substrates, along with the release of cyanoalanine (Cya) and the scavenging of HCN.Analogously, L-Cys can synthesize H 2 S via the catalysis of NFS, similar to the action of NFS in chloroplasts.OAS-TL can also catalyze L-Cys to H 2 S in mitochondria (Liu et al., 2021;Yang et al., 2022;Huang and Xie, 2023) (Figure 1).In addition, carbonyl sulfide (COS), as an atmospheric trace gas, can enter the plant cells through stomata in association with carbon dioxide (CO 2 ).Under the catalysis of carbonic anhydrase (CA), COS can be converted to H 2 S (Stimler et al., 2010;Li et al., 2022;Citi et al., 2023) (Figure 1).In addition, in Arabidopsis plants, 3mercaptopyruvate sulfur transferase (MST) can be persulfidated by 3-mercaptopyruvate to form persulfidated MST (MST-SSH).The MST-SSH can release H 2 S by interacting with either thioredoxin (TRX) or glutaredoxin (GRX).Therefore, the redox systems, TRX and GRX, can not only regulate the activity of MST, but are also one of the biosynthetic pathways of H 2 S in plants (Moseler et al., 2021).Recently, MST was found to directly lead to the persulfidation of target proteins, it is considered a protein persulfidase (Pedre et al., 2023) (Figure 1).

Non-enzymatic pathways for H 2 S production
As mentioned above, MST is a protein persulfidase, and the sulfur in MST-SSH can be transferred to other proteins containing dithiols (two sulfydryl groups) to form protein persulfides (P-SSH).The P-SSH can be oxidized by oxidants, releasing H 2 S (Pedre et al., 2023) (Figure 1).MST-SSH can also be reduced to MST-SH and glutathione persulfide (GSSH) by glutathione (GSH).The GSSH is then converted to H 2 S and GSSG by the GSH.Similarly, P-SSH can interact with other proteins containing sulfydryl groups (P-SH) to form disulfide bonds between proteins (P-S-S-P) and release H 2 S (Pedre et al., 2023).Similarly, P-SH can be converted to glutathionylated proteins (P-SSG) and produce H 2 S under the action of GSSH.In addition, isothiocyanate (ITC), thiocysteine (TC), thiosulfate (TS), and allyl sulfur (AS), as major components of fertilizers and/or industrial pollutants, can release H 2 S under the action of L-Cys or GSH when they are taken up by plant roots (Nakajima et al., 2019;Yu et al., 2019;Moseler et al., 2021;Li et al., 2022;Citi et al., 2023).In addition to these, H 2 S can be released from glucose (Glc) under the influence of L-Cys, homocysteine, or methionine (Met) (Figure 1).

H 2 S degradation
To maintain homeostasis, the excess H 2 S in plant cells must be rapidly scavenged, degraded, or converted.As mentioned above, in the cytosol and mitochondria, CS can utilize H 2 S and OAS to synthesize Cys, which in turn forms peptides and/or proteins (Liu et al., 2021;Yang et al., 2022;Huang and Xie, 2023) (Figure 2).On the other hand, in mitochondria, sulfite quinone reductase (SQR) can catalyze H 2 S and GSH to GSSH in the presence of O 2 .The GSSH can be oxidized to SO 3 2-by persulfide dioxygenase (ETHE1) (Gerush and Ferenchuk, 2019;Yang et al., 2022).Subsequently, SO 3 2-is further oxidized to SO 4 2-and S 2 O 3 2-by sulfite oxidase (SO) and Rhodanese (namely thiosulfate sulfur transferase), respectively (Gerush and Ferenchuk, 2019;Yang et al., 2022) (Figure 2).
H 2 S modulates HT tolerance through crosstalk with other signaling molecules.As discussed above, a large number of signaling molecules and their interactions are involved in the development of HT tolerance (Li et al., 2021;Wang et al., 2021;Zhang et al., 2022).For H 2 S-Ca 2+ crosstalk in tobacco (Nicotiana tabacum) suspension-cultured cells, H 2 S pre-treatment improved HT tolerance by increasing cell viability and survival rate and decreasing electrolyte leakage and MDA accumulation (Li et al., 2012).H 2 S-induced HT tolerance was enhanced by Ca 2+ and its ionophore A23187, whereas it was repaired by the Ca 2+ chelator ethylene glycol-bis(b-aminoethyl-ether)-N,N,N',N'-tetraacetic acid, the plasma membrane channel blocker La 3+ , and the calmodulin (CaM) antagonists chlorpromazine and trifluoperazine (Li et al., 2012).This study is the first to report that H 2 S interacts with Ca 2+ in the acquisition of HT tolerance in plants.Similarly, in tobacco cells, the activity of the H 2 S-generating enzyme LCD could be activated by Ca 2+ and CaM (Li et al., 2015a).Interestingly, H 2 S could persulfidate DES1 at Cys44 and Cys205, which in turn enhanced its activity to achieve self-amplification of H 2 S signaling (Shen et al., 2020).H 2 S was also able to regulate Ca 2+ homeostasis in animal cells through the persulfidation of Ca 2+ channels (Zhang et al., 2015), but this regulatory mechanism needs to be further investigated in the plant system in the future.
For the H 2 S-phytohormone crosstalk, in rice (Oryza sativa L.) cultivars, ethylene (ETH), NO, and H 2 S increased the dry weight of shoots and roots, the levels of Pro, GB, Tre, and SS, and the activity of SOD, CAT, and GR in leaves under normal and HT stress conditions.Also, the treatment improved photosynthetic parameters, such as actual, maximal, and intrinsic efficiency of PSII, in addition to photochemical quenching, non-photochemical quenching, and electron transport rate (Gautam et al., 2022).Similarly, the levels of these signaling molecules and the relative expression of psbA, psbB, Mn-SOD, Fe-SOD, Cu/Zn-SOD, and APX were upregulated by exogenous application (Gautam et al., 2022).These effects of ETH or NO were enhanced by H 2 S, while reversed by the H 2 S scavenger hypotaurine, further supporting that the ameliorative effects of ETH or NO involve H 2 S (Gautam et al.,FIGURE 4 Role of hydrogen sulfide (H 2 S) in plant response to high temperature (HT) and low temperature (LT) stress.APX, ascorbate peroxidase; CBF, C-repeat binding factor; Ca 2+ , 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.
For H 2 S-ROS-NO crosstalk, H 2 S increased H 2 O 2 and NO accumulation, in addition to NR activity in wheat plants.The increased NO was suppressed by the NR inhibitor sodium tungstate, but not by the NG-nitro-L-arginine methyl ester (NO synthase inhibitor) (Karpets et al., 2020).Similarly, NR activity and NO levels were abolished by the H 2 O 2 scavenger dimethylthiourea and the NADPH oxidase inhibitor imidazole, whereas H 2 S-induced H 2 O 2 levels were only weakly affected by the NO scavenger cPTIO and sodium tungstate (Karpets et al., 2020).Furthermore, H 2 Sinduced HT tolerance was abolished by dimethylthiourea, imidazole, cPTIO, and tungstate (Karpets et al., 2020).This study demonstrates the signaling crosstalk of H 2 S with H 2 O 2 and NO in the development of HT tolerance in wheat plants.A similar H 2 S-ROS-NO crosstalk was found in rice seedlings under HT stress (Gautam et al., 2022).Interestingly, in rice seedlings, NIA2 (an NR isoform), a NO-generating enzyme, could be persulfidated by H 2 S, which in turn decreased the enzyme activity, thus regulating nitrate  metabolism and NO levels (Zhou et al., 2021b), further the crosstalk of H 2 S with NO in plants.
H 2 S improves LT tolerance in fruits by enhancing the ROSscavenging system and maintaining the integrity of biomembranes and cell structures.In hawthorn (Crateagus pinnatifida) fruit, H 2 S fumigation increased the endogenous levels of H 2 S by activating LCD and DCD, which in turn increased the activity of SOD, CAT, APX, and phenylalanine ammonia lyase.The levels of phenols, flavonoids, anthocyanins, and AsA in fruits were also increased by H 2 S. The enhanced antioxidant system further reduced the accumulation of MDA and H 2 O 2 under LT stress conditions, thus ameliorating LT injury in fruits (Aghdam et al., 2018).Similarly, H 2 S increased endogenous H 2 S levels by enhancing the activity of LCD, DCD, OAS-TL, and serine acetyltransferase (SAT) in peach (Prunus persica L.) fruits, which in turn accumulated AsA and GSH.In addition, the activity of APX, GR, CAT, and SOD was increased by H 2 S, thereby decreasing the levels of ROS (mainly H 2 O 2 and superoxide radicals) under LT stress conditions (Wang et al., 2022a).In the same way, H 2 S decreased the activity of pectin methylesterase, polygalacturonase, bglucosidase, carboxymethylcellulose, and b-galactosidase in peach fruits under LT stress conditions.The reduced enzyme activity inhibited the degradation of cell-wall polysaccharide fractions, thus maintaining the integrity of the cell structure (Wang et al., 2022a).The identical effects of H 2 S were found in banana (Musa paradisiaca L.) (Luo et al., 2015;Li et al., 2016b) and peach (Wang et al., 2023a) fruits under LT stress conditions through regulation of energy and Pro metabolism.
H 2 S enhances LT tolerance in plants through the inducer of Crepeat-binding factor (CBF) expression (ICE)−CBF−cold regulated proteins (COR) signaling pathways.In grape (Vitis vinifera L) seedlings, foliar application of H 2 S increased SOD activity and VvICE1 and VvCBF3 gene expression in leaves, and reduced superoxide anion radical and MDA levels and biomembrane damage under LT stress conditions (Fu et al., 2013).These effects were reversed by the H 2 S scavenger hypotaurine (Fu et al., 2013), suggesting that H 2 S could improve LT tolerance in grape seedlings.In the same way, H 2 S pre-treatment could improve LT tolerance of cucumber (Cucumis sativus L) seedlings through the CsARF5-CsDREB3 module (Zhang et al., 2021), similar to H 2 S-induced HT tolerance in strawberry (Christou et al., 2011, Christou et al., 2014).In cucumber seedlings, foliar application of H 2 S also increased the activity of APX, CAT, and POD, in addition to the levels of SS, Pro, and GSH in leaves.The enhanced ROS-scavenging system further reduced the accumulation of MDA and H 2 O 2 and electrolyte leakage under LT stress conditions, thus improving LT tolerance of cucumber (Nasibi et al., 2020).
H 2 S modulates LT tolerance in plants through crosstalk with other signaling molecules.For H 2 S-NO-ROS crosstalk, in cucumber seedlings, H 2 S increased plasma membrane H + -ATPase (PMA) activity by upregulating the expression of PMA genes (CsHA2, CsH4, CsH8, CsH9, and CsHA10) under LT stress conditions (Janicka et al., 2018).Similarly, NO and H 2 O 2 upregulated the expression of the gene CsHA2, which in turn slightly increased PMA activity in cucumber under LT stress conditions.More interestingly, NO could nitrosylate PMA, thus promoting its phosphorylation and increasing the H + /ATP coupling ratio under LT stress conditions (Janicka et al., 2018).This study suggests that under LT stress conditions PMA plays a key role in the development of LT tolerance in plants by maintaining PVS via the crosstalk of H 2 S with NO and H 2 O 2 .Similar effects have been observed in cucumber seedlings (Wu et al., 2022), peach fruits (Geng et al., 2019), and other plant species (Kolupaev et al., 2023) through H 2 S-H 2 O 2 crosstalk.Interestingly, in Arabidopsis plants, H 2 S could persulfidate PMA, which in turn enhanced its activity, thus promoting H + efflux and maintaining pH homeostasis in plant cells (Ma et al., 2023).
For the H 2 S-MAPK crosstalk, in the model plant Arabidopsis thaliana, H 2 S upregulated the gene expression of MPK4 under normal and LT stress conditions.The upregulation of MPK4 further activated the transcription of ICE1, CBF3, COR15A, and COR15B, which inhibited stomatal opening and alleviated LT injury (Du et al., 2017).Further studies found that H 2 S-alleviated LT tolerance was attenuated in mpk4 mutants, but not in the upstream mek2 and crlk1 mutants (Du et al., 2021).More interestingly, MPK4, which has a basal persulfidation, could be further persulfidated by H 2 S, which in turn enhanced its activity nearly tenfold, whereas MEK2 was not persulfidated by H 2 S (Du et al., 2021).These data further support the fact that H 2 S alleviates LT tolerance through the MPK4 and ICE-CBF-COR signaling pathways, as discussed above.
For the H 2 S-phytohormone crosstalk, in cucumber seedlings, SA upregulated the gene expression of LCD and DCD, which in turn increased the endogenous levels of H 2 S under normal and LT stress conditions (Pan et al., 2020).This effect was blocked by paclobutrazol and 2-aminoindan-2-phosphonic acid (inhibitors of SA biosynthesis).In contrast, H 2 S and its scavenger hypotaurine and inhibitor DL-propargylglycine had no significant effect on endogenous SA levels in cucumber seedlings under normal and LT stress conditions (Pan et al., 2020).This study suggests that H 2 S plays a signaling role downstream of SA.SA and NaHS also upregulated the expression of chilling response genes (ICE, CBF1, and COR) and antioxidant enzymes (SOD, POD, CAT, APX, and GR).The upregulation of gene expression further increased enzyme activity and AsA and GSH levels.The enhanced antioxidant system reduced ROS and MDA accumulation and electrolyte leakage in cucumber seedlings under LT stress conditions, thus alleviating LT injury in cucumber (Pan et al., 2020).These data further support the fact that H 2 S enhances LT tolerance through the ICE−CBF−COR signaling pathway in grape (Fu et al., 2013), cucumber (Janicka et al., 2018;Zhang et al., 2021), and Arabidopsis (Du et al., 2021), as discussed above.Similarly, Zhang et al. (2020) reported that H 2 S increased the transcription and activity of flavin monooxygenase-like proteins (YUCCA2), thereby increasing indoleacetic acid (IAA) levels in seedlings under LT stress conditions.However, IAA treatment had no significant effect on LCD and DCD activities or H 2 S levels in cucumber seedlings under LT stress conditions (Zhang et al., 2020), indicating that H 2 S plays a signaling role in the upstream of IAA.In addition, H 2 S and IAA improved LT tolerance of cucumber seedlings by reducing electrolyte leakage and ROS accumulation.The H 2 S-induced tolerance was reduced by the IAA polar transport inhibitor (1-naphthylphthalamic acid), while the H 2 S scavenger hypotaurine had little effect on the IAA-induced tolerance (Zhang et al., 2020).These data further support the fact that IAA plays a signaling role downstream of H 2 S in plant LT tolerance through auxin response factor (ARF)−dehydrationresponsive element-binding (DREB) protein signaling pathways.However, whether the ICE−CBF−COR module and plant hormone signaling proteins can be persulfidated by H 2 S needs to be further elucidated in the future.

Conclusion and prospects
Overall, H 2 S, as a novel signaling molecule in plants, plays a pivotal role in plant growth and response to HT and LT stress through crosstalk with other signaling molecules (Shen et al., 2020;Liu et al., 2021;Wang et al., 2021;Yang et al., 2022;Mukherjee et al., 2024).As discussed above, HT and LT jointly result in biomembrane damage, protein denaturation, Ca 2+ overload toxicity, acid-base imbalance, and oxidative, osmotic, and MG stress (Figure 3).To survive, plants have developed the mechanisms of tolerance to HT and LT stress by repairing the biomembrane, biosynthesizing stress proteins, enhancing the ROS-/ MG-detoxification and water homeostasis systems, and maintaining Ca 2+ and H + balance (Figure 4).Hopefully, the tolerance mechanisms can be triggered by the application of H 2 S in the form of seed priming, foliar application, and root treatments (Figure 4).Briefly, under HT and LT stress conditions, the repairing of biomembrane is involved in the change of membrane lipid components, saturation, and chain length.The denatured proteins can be renatured or replaced by stress proteins, such as HSPs and cold shock proteins.Also, oxidative damage can be alleviated by detoxification systems, mainly the ROS detoxification system and the MG detoxification system.The ROS detoxification system consists of enzymes (SOD, APX, CAT, GR, DHAR, and MDHAR) and non-enzymatic antioxidants (AsA, GSH, phenols, flavonoids, and anthocyanins).The MG detoxification system includes the glyoxylase system (glyoxalase I, Gly I; Gly II; and Gly III) and the non-glyoxalase system (MG reductase, MGR; aldose/ aldehyde reductase, ALR; aldo-keto reductase, AKR; and lactate dehydrogenase, LDH) (Table 1).Similarly, osmotic stress can be alleviated by the water homeostasis system consisting of osmolytes (Pro, GB, Tre, SS, and soluble proteins) and their metabolic enzymes (P5CS, ProDH, GDH, and TPP) and water transporters (AQPs).In addition, Ca 2+ and H + balance can be maintained by the synergistic effect of Ca 2+ -ATPase, Ca 2+ channels, PMAs, vacuolar H + -ATPase, and vacuolar pyrophosphatase (Cosse and Seidel, 2021) (Figure 4).
Over the past decade, great progress has been made in understanding H 2 S signaling in plants from seed germination to plant HT and LT tolerance.However, several open questions need to be addressed in the future.For example, the metabolism of H 2 S, especially the non-enzymatic pathways, is not fully understood.Also, H 2 S is an emerging signaling molecule and its receptors have not been found in plants.Moreover, the exact mechanisms of H 2 Sinduced HT and LT tolerance remain to be elucidated using molecular, physiological, biochemical, omics, and multiomics approaches.

FIGURE 3
FIGURE 3high 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), acidbase and ion imbalance, and other damage in plants.

TABLE 1
Effect of hydrogen sulfide (H 2 S) on high temperature (HT) and low temperature (LT) stress tolerance in plants.