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. 2020 Mar 17;15(5):1741987. doi: 10.1080/15592324.2020.1741987

Redox-based protein persulfidation in guard cell ABA signaling

Heng Zhou a,*, Jing Zhang a,*, Jie Shen a, Mingjian Zhou a, Xingxing Yuan b,✉, Yanjie Xie a,✉
PMCID: PMC7238880  PMID: 32178559

ABSTRACT

Hydrogen sulfide (H2S) is a versatile signaling molecule that regulates multiple physiological processes in plants, including growth and development, immunity, and stress response as well. Signaling triggered by H2S is proposed to occur via persulfidation, an oxidative post-translational modification (PTM) of cysteine residues (–SH) to persulfides (–SSH). Notwithstanding the growing body of information for the plant persulfidation proteome, the gap between the molecular mechanism of H2S and physiological functions of protein persulfidation remains large. In this mini-review, we discussed the specific regulatory mechanism of persulfidation on guard cell abscisic acid (ABA) signaling and the possible link of persulfidation, sulfenylation, and S-nitrosylation within the framework of redox-based regulation.

KEYWORDS: Hydrogen sulfide, persulfidation, ABA signaling, sulfenylation

Hydrogen sulfide (H2S) has been recognized as an important bio-active signaling molecule in both animal and plant, and is as important as nitric oxide (NO), carbon monoxide (CO), and hydrogen peroxide (H2O2).1,2 A growing body of reports have demonstrated that H2S is involved in various biological processes during the whole lifespan, including seed dormancy/germination, root growth, development, defense responses to biotic and abiotic stresses.3-7 The exogenously administration of H2S confers to the positive effects in regulating plants adaptation to environmental stress and growth.8-10Despite numerous studies highlighting the importance of H2S-based signaling transduction, its mechanism of action is not fully understood.9 Current knowledge suggested that the primary signaling mechanism of H2S work through a new oxidative posttranslational modification (PTM), called persulfidation, which convert cysteine thiols (–SH) into persulfides (–SSH).12,13 This PTM on target proteins lead to structural and functional changes. Recently, persulfidation proteome revealed that a considerable amount of proteins which involved a wide range of biological functions are sensitive to persulfidation.14,15 The proteomes greatly extend our knowledge of the function of persulfidation and provide potential candidate targets for further investigation. In this review, we summarize and discuss the features of persulfidation in regulating guard cell abscisic acid (ABA) signaling and the potential crosstalk of persulfidation, sulfenylation, and S-nitrosylation.

Persulfidation regulates guard cell ABA signaling

ABA as an important phytohormone involves in the regulation of diverse plant stress resistance and developmental processes. ABA is also the central regulator that triggers a complex signaling network to regulate stomatal movement.16 ABA could bind with PYR/RCAR (PYRABACTINRESISTANCE/REGULATORY COMPONENT OF ABA RECEPTOR) receptors. Binding of ABA to these receptors enhances their interaction with and inhibition of clade A protein phosphatases (PP2Cs).17 PP2Cs inhibition enables the activation of SnRK2/OST1 (Open Stomata 1) protein kinases. These kinases phosphorylate and activate targets, in concert with ROS and Ca2+ together with Ca2+-dependent protein kinases (CDPKs) activate ion channels that mediate stomatal closure.18

The participation of H2S in stomatal closure has also been widely reported.19,20 L-cysteine desulfhydrase (DES1) has been characterized as the major production of endogenous cytosolic H2S.2,21 ABA cannot induce stomatal closure of des1 mutants, while this effect is restored by the application of exogenous H2S.22 Recent study showed that the guard cell itself could be able to produce H2S, which is involved in the ABA-induced stomatal closure.23 Accordingly, a cluster of proteins including protein kinases and phosphatases, which involved in guard cell ABA signaling, was found in the persulfidation proteome (Table 1).24 Recent studies demonstrated that H2S regulates guard cell ABA signaling pathways through persulfidation of specific targets. For example, H2S produced by DES1 positively regulates ABA signaling by persulfidation of SNF1-RELATED PROTEIN KINASE2.6 (SnRK2.6)/open stomata (OST1) in guard cell, which is essential for the control of stomatal closure.25 The persulfidation on Cys131 and Cys137 of SnRK2.6 promotes its phosphorylating activity and the interaction with ABA response element-binding factor 2 (ABF2), and further activate the downstream genes expression. It should be mentioned that SnRK2.6/OST1 is also S-nitrosylated by nitric oxide (NO) at Cys137, lead to the inhibition of its activity, and further negatively regulating guard cell ABA signaling.26 H2S is required for the ABA-induced NO production, and acts as upstream of NO in ABA-dependent stomatal closure.22 It can be deduced that NO forms a feedback loop to fine-tune guard cell ABA/H2S signal by nitrosylating SnRK2.6/OST1. Coincidentally, our recent results revealed that persulfidation of DES1 and NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG PROTEIN D (RBOHD) fine-tunes guard cell ABA signaling.27 ABA triggers the persulfidation of DES1 itself at Cys44 and Cys205 and increase DES1 activity to produce sustainable H2S, which could regard as an amplification of H2S signaling. Enhanced H2S production by DES1 further persulfides RBOHD at Cys825 and Cys 890 to facilitate the rapid induction of ROS and stomatal closure. Interestingly, both persulfidation on DES1 and RBOHD were redox dependent, which could be further oxidized by over-accumulated ROS and inhibit its activity. Thus, these processes form a negative feedback loop through H2S and ROS-mediated modification that fine-tunes guard cell redox homeostasis and ABA signaling. Besides that, our study also implied that the crosstalk between H2S and ROS are essential for the rapid response to environmental changes. Considering the versatile biological function of DES/H2S and the universality of persulfidation modification in plant, it would be reasonable to believe that persulfidation may function in multiple ways in regulating not only stomatal movement, but also other plant developmental and stress-responsive processes.1,28

Table 1.

The list of persulfidated proteins which involved in guard cell ABA signaling.24

Protein description AGI accession
Abscisic acid receptor (PYL1) AT5G46790
Calcium-dependent protein kinase 3 (CPK3) AT4G23650
Calcium-dependent protein kinase 5(CPK5) AT4G35310
Calcium-dependent protein kinase 6(CPK6) AT2G17290
Calmodulin-domain protein kinase 9 (CPK9) AT3G20410
SNF1-related protein kinases 2.1 (SnRK2.1) AT5G08590
SNF1-related protein kinases 2.2 (SnRK2.2) AT3G50500
SNF1-related protein kinases 2.4 (SnRK2.4) AT1G10940
SNF1-related protein kinases 2.6 (SnRK2.6/OST1) AT4G33950
SNF1-related protein kinases 2.10 (SnRK2.10) AT1G60940
Protein phosphatase 1 (PP1) AT1G50370
Protein phosphatase 2A subunit A2 (PP2AA2) AT3G25800
Protein phosphatase 2A subunit A3 (PP2AA3) AT1G13320
Serine/threonine-protein phosphatase catalytic subunit (PP2A-3) AT3G58500
Serine/threonine-protein phosphatase catalytic subunit (PP2A5) AT1G69960
Serine/threonine protein phosphatase 2A subunit B (PP2AB2) AT1G17720
Probable protein phosphatase 2C 20 (PP2C 20) AT2G20630
Probable protein phosphatase 2C 21 (PP2C 21) AT2G25070
Probable protein phosphatase 2C 26 (PP2C 26) AT2G30170
Probable protein phosphatase 2C 28 (PP2C 28) AT2G34740
Probable protein phosphatase 2C 39 (PP2C 39) AT3G15260
Probable protein phosphatase 2C 58 (PP2C 58) AT4G28400
Probable protein phosphatase 2C 62 (PP2C 62) AT4G33500
Probable protein phosphatase 2C 76 (PP2C 76) AT5G53140
Probable protein phosphatase 2C 80 (PP2C 80) AT5G66720
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Redox-based cysteine post-translational modifications

The crosstalk with other signal molecules, including NO and H2O2, is important for biological function of H2S.1,22,29 The protein thiols are the important intermediates that integrate the interaction network, since they can be modified by all of the signal molecules–mediated PTMs.7 The cysteine thiols can be easily oxidized by reactive oxygen species (ROS) to form sulfenic acid (SOH), which usually results in enzymatic inactivation. This reversible modification is proposed to functions as an intermediate for further redox modifications, or overoxidation to sulfinic (SO2H) and sulfonic (SO3H) acids when ROS exposure proceeds.30,31 Overoxidation to sulfinic or sulfonic acid is irreversible and usually leads to permanent functional loss and protein degradation. It should be noted that H2S cannot directly react with cysteine thiols to form persulfides, precondition of oxidation step is required for persulfidation. Reactions of H2S with either disulfides or sulfenic acids yield persulfides.32 Persulfides also can be oxidized to perthiosulfenic acids (–SSOH) and further perthiosulfinic (–SSO2H), and perthiosulfonic (–SSO3H) acid, due to its high reactivity to ROS.12,13 However, this oxidized status could be reduced by thioredoxins or glutaredoxins, which would recycle it back to its thiol form. Hence, it is more plausible that protein persulfidation is an evolutionarily conserved modification that act as a protective mechanism to prevent irreversible thiol overoxidation under oxidative stress.12 It could be confirmed by the results from animal. By using a dimedone-based probe, the authors found the persulfides are mainly produced from the reaction of sulfenic acids with H2S. More importantly, temporal dynamics of persulfidation perfectly matches the sulfenylation, with the latter preceding the former.33

In plants, persulfidation proteome showed that at least 5% of the whole proteome in Arabidopsis is persulfidated, and H2S is involved in regulation of the redox status of cysteine residues of proteins involved in diverse biological processes.24 A comparison of the persulfidation and sulfenylation proteome were performed for the investigation of its potential crosstalk in plants based on two latest studies.24,31 Four hundred thirty-seven proteins were identified in both two modifications (Figure 1(a)), illustrating the overlap between these two PTMs. GO biological process analysis indicated that these proteins are mainly involved in stress responses, oxidation–reduction process, glycolytic process and tricarboxylic acid cycle (Figure 1(b)). Interestingly, several antioxidant enzymes and redox regulatory protein, including glutathione S-transferase (GSTU5 and GSTT1), cytosolic L-ascorbate peroxidase (cAPX1 and cAPXT), thioredoxin, and thioredoxin-like protein were found. As cysteine-rich proteins, antioxidant enzymes such as, APX, catalase (CAT), glutathione peroxidase (GPX), and peroxiredoxin are susceptible to oxidation and thereby function suppressed, especially for APX and peroxiredoxin, which often use thiol-based mechanisms to decompose H2O2.34,35 Nevertheless, the function of persulfidation and sulfenylation are usually opposite. For example, sulfenylation at Cys32 causes cAPX1 inactivation,36 while persulfidation at Cys32 significantly increase the activity of cAPX1.14 Glyceraldehyde-3-phosphate dehydrogenase (GAPC1) was also found persulfidated and sulfenylated at the same cysteine residue, while its activity was enhanced by persulfidation, and inhibited by sulfenylation.14,37 It further indicated that persulfidation function as an efficient mechanism to rescue antioxidant capacity by resolving sulfenylation and enhance activity of thiol-based antioxidant enzyme/proteins in response to oxidative damage.

Figure 1.

Figure 1.

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Comparison of sulfenylation and persulfidation proteome in Arabidopsis. Venn diagram shows the sulfenylated31 and persulfidated24 proteins identified from recent studies (a). GO biological process analysis shows the 11 most enriched terms from the 437 overlapped proteins (b).

Interestingly, the largest nitrosylation proteome identified 927 endogenously S-nitrosylated proteins in Arabidopsis.38 Six hundred thirty-nine of which are susceptible to being persulfidated.7 Although targets of these two PTMs share high coverage scale, the function vary from protein to protein. For example, different from the opposite effect on the activity of SnRK2.6/OST1, both persulfidation and S-nitrosylation at Cys32 significantly enhance the activity of cAPX1.39,40 S-nitrosylation abolishes the catalytic activity of GAPC, whereas the persulfidation increase its activity.14,41 It indicated that these proteins may finely regulate by different PTMs in response to different stress conditions.

Taken together, these proteomic data provide valuable tools for further investigation of function of these oxidative translational modifications and the crosstalk regulation among protein sulfenylation, persulfidation, and S-nitrosylation.

Concluding remarks

A considerable number of articles highlight the important roles of H2S in numerous biological process in plant. Benefit from the continuous improved persulfidation proteome, a number of proteins that undergo persulfidation have been characterized. However, the base of targets is too broad and the function validation will be laborious. Further effort should focus on the comparative proteomic analyses under different developmental process or environmental changes. Additionally, the extent of interaction of persulfidation and sulfenylation on redox regulation and how these two modifications shift on cysteine residues in response to environmental changes need further investigation. Most importantly, the crosstalk among these signal molecules are complicate in response to environment changes and the physiological evidence sometimes are controversial, the research on the regulatory mechanism and biological functions of the specific targets of these PTMs will shed more light on the regulatory role of H2 in plant cells.

Funding Statement

The work was supported by grants from the Chinese Natural Science Foundation [31670255], the Fundamental Research Funds for the Central Universities [KYZ201859], the Natural Science Foundation of Jiangsu Province [BK20161447].

Acknowledgments

We are grateful to Dr. Frantisek Baluska for kindly inviting this review.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

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