Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling (original) (raw)

8-Mercapto-Cyclic GMP Mediates Hydrogen Sulfide-Induced Stomatal Closure in Arabidopsis

Plant & cell physiology, 2015

Plants are exposed to hydrogen sulfide (H2S) both exogenously, as it exists as a pollutant gas in the environment, and endogenously, as it is synthesized in cells. H2S has recently been found to function as a gaseous signaling molecule, but its signaling cascade remains unknown. Here, we examined H2S-mediated guard cell signaling in Arabidopsis. The H2S donor GYY4137 (morpholin-4-ium-4-methoxyphenyl [morpholino] phosphinodithioate) induced stomatal closure, which peaked after 150 min at 1 µM or after 90 min at 10 and 100 µM. After reaching maximal closure, stomatal apertures gradually increased in size in response to further exposure to GYY4137. GYY4137 induced nitric oxide (NO) generation in guard cells, and GYY4137-induced stomatal closure was reduced by an NO scavenger and inhibitors of NO-producing enzymes. Mass spectrometry analyses showed that GYY4137 induces the synthesis of 8-nitro-cGMP and 8-mercapto-cGMP and that this synthesis is mediated by NO. In addition, 8-mercapto-cG...

Hydrogen sulfide signaling in plant adaptations to adverse conditions: molecular mechanisms

Journal of Experimental Botany, 2021

Hydrogen sulfide (H2S) is a signaling molecule that regulates critical processes and allows plants to adapt to adverse conditions. The molecular mechanism underlying H2S action relies on its chemical reactivity, and the most-well characterized mechanism is persulfidation, which involves the modification of protein thiol groups, resulting in the formation of persulfide groups. This modification causes a change of protein function, altering catalytic activity or intracellular location and inducing important physiological effects. H2S cannot react directly with thiols but instead can react with oxidized cysteine residues; therefore, H2O2 signaling through sulfenylation is required for persulfidation. A comparative study performed in this review reveals 82% identity between sulfenylome and persulfidome. With regard to abscisic acid (ABA) signaling, widespread evidence shows an interconnection between H2S and ABA in the plant response to environmental stress. Proteomic analyses have reve...

Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana

Plant and Soil, 2017

Background and aims In many plant species, hydrogen sulfide (H 2 S) triggers stomatal closure, which is produced mainly by two classes of enzymes, cysteine desulfhydrases (CDes) and O-acetyl-L-serine (thiol) lyases (OASTLs). Stomatal movement is accompanied by several ion fluxes across the plasma membranes of guard cells. Methods In this paper, we detected the fluxes of H + , Ca 2+ , K + and Cl − in guard cells of wild-type Arabidopsis thaliana and the mutants associated with H 2 S production (lcd, OE-LCD, des, OE-DES, oastl-a1, oastl-a2, oastl-b and oastl-c), using a non-invasive micro-test technique. Results The results showed that endogenous H 2 S induced a transmembrane K + efflux, and Ca 2+ and Cl − influxes, while not affecting the flow of H +. Furthermore, the K + channel was the main osmolyte responder during the regulation of stomatal movement by H 2 S in response to drought stress. Finally, the two classes of enzymes produced H 2 S, CDes and OASTLs, played different roles in regulating stomatal movements. Conclusions Thus, H 2 S mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana.

Hydrogen Sulfide Signaling in Plants: Emerging Roles of Protein Persulfidation

Frontiers in plant science, 2018

Hydrogen sulfide (HS) has been largely referred as a toxic gas and environmental hazard, but recent years, it has emerged as an important gas-signaling molecule with effects on multiple physiological processes in both animal and plant systems. The regulatory functions of HS in plants are involved in important processes such as the modulation of defense responses, plant growth and development, and the regulation of senescence and maturation. The main signaling pathway involving sulfide has been proven to be through protein persulfidation (alternatively called sulfhydration), in which the thiol group of cysteine (-SH) in proteins is modified into a persulfide group (-SSH). This modification may cause functional changes in protein activities, structures, and subcellular localizations of the target proteins. New shotgun proteomic approaches and bioinformatic analyses have revealed that persulfidated cysteines regulate important biological processes, highlighting their importance in cell...

Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure

Plant physiology, 2014

Abscisic acid (ABA) is a well-studied regulator of stomatal movement. Hydrogen sulfide (H2S), a small signaling gas molecule involved in key physiological processes in mammals, has been recently reported as a new component of the ABA signaling network in stomatal guard cells. In Arabidopsis (Arabidopsis thaliana), H2S is enzymatically produced in the cytosol through the activity of l-cysteine desulfhydrase (DES1). In this work, we used DES1 knockout Arabidopsis mutant plants (des1) to study the participation of DES1 in the cross talk between H2S and nitric oxide (NO) in the ABA-dependent signaling network in guard cells. The results show that ABA did not close the stomata in isolated epidermal strips of des1 mutants, an effect that was restored by the application of exogenous H2S. Quantitative reverse transcription polymerase chain reaction analysis demonstrated that ABA induces DES1 expression in guard cell-enriched RNA extracts from wild-type Arabidopsis plants. Furthermore, stoma...

Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling

New Phytologist, 2010

• Hydrogen sulphide (H 2 S) has been proposed as the third gasotransmitter. In animal cells, H 2 S has been implicated in several physiological processes. H 2 S is endogenously synthesized in both animals and plants by enzymes with L-Cys desulphydrase activity in the conversion of L-Cys to H 2 S, pyruvate and ammonia. • The participation of H 2 S in both stomatal movement regulation and abscisic acid (ABA)-dependent induction of stomatal closure was studied in epidermal strips of three plant species (Vicia faba, Arabidopsis thaliana and Impatiens walleriana). The effect of H 2 S on stomatal movement was contrasted with leaf relative water content (RWC) measurements of whole plants subjected to water stress. • In this work we report that exogenous H 2 S induces stomatal closure and this effect is impaired by the ATP-binding cassette (ABC) transporter inhibitor glibenclamide; scavenging H 2 S or inhibition of the enzyme responsible for endogenous H 2 S synthesis partially blocks ABA-dependent stomatal closure; and H 2 S treatment increases RWC and protects plants against drought stress. • Our results indicate that H 2 S induces stomatal closure and participates in ABAdependent signalling, possibly through the regulation of ABC transporters in guard cells.

Hydrogen sulfide: A versatile gaseous molecule in plants

Plant Physiology and Biochemistry, 2021

Hydrogen sulfide (H 2 S) is a gasotransmitter and signaling molecule associated with seed germination, plant growth, organogenesis, photosynthesis, stomatal conductance, senescence, and post-harvesting. H 2 S is produced in plants via both enzymatic and non-enzymatic pathways in different subcellular compartments. Exogenous application of H 2 S facilitates versatile metabolic processes and antioxidant machinery in plants under normal and environmental stresses. This compound interacts with phytohormones like auxins, abscisic acid, gibberellins, ethylene, jasmonic acid, and salicylic acid. Furthermore, H 2 S participates in signal transductions of other signaling molecules like nitric oxide, carbon monoxide, calcium, methylglyoxal, and hydrogen peroxide. It also mediates post-translational modification, which is a protective mechanism against oxidative damage of proteins. This review summarizes the roles of H 2 S as intriguing molecule in plants.

Phospholipase D 1 and Phosphatidic Acid Regulate NADPH Oxidase Activity and Production of Reactive Oxygen Species in ABA-Mediated Stomatal Closure in Arabidopsis

Plant Cell, 2009

We determined the role of Phospholipase Da1 (PLDa1) and its lipid product phosphatidic acid (PA) in abscisic acid (ABA)induced production of reactive oxygen species (ROS) in Arabidopsis thaliana guard cells. The plda1 mutant failed to produce ROS in guard cells in response to ABA. ABA stimulated NADPH oxidase activity in wild-type guard cells but not in plda1 cells, whereas PA stimulated NADPH oxidase activity in both genotypes. PA bound to recombinant Arabidopsis NADPH oxidase RbohD (respiratory burst oxidase homolog D) and RbohF. The PA binding motifs were identified, and mutation of the Arg residues 149, 150, 156, and 157 in RbohD resulted in the loss of PA binding and the loss of PA activation of RbohD. The rbohD mutant expressing non-PA-binding RbohD was compromised in ABA-mediated ROS production and stomatal closure. Furthermore, ABA-induced production of nitric oxide (NO) was impaired in plda1 guard cells. Disruption of PA binding to ABI1 protein phosphatase 2C did not affect ABA-induced production of ROS or NO, but the PA-ABI1 interaction was required for stomatal closure induced by ABA, H 2 O 2 , or NO. Thus, PA is as a central lipid signaling molecule that links different components in the ABA signaling network in guard cells. Ga to a GDP-bound Ga, thus producing PA that acts upstream of Ga to inhibit stomatal opening . PLD and PA are both implicated in ROS production. The depletion of PLDa1 in Arabidopsis decreases ROS production in 1 These authors contributed equally to this work.

Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis

Journal of Experimental Botany, 2017

Hydrogen sulfide-mediated signaling pathways regulate many physiological and pathophysiological processes in mammalian and plant systems. The molecular mechanism by which hydrogen sulfide exerts its action involves the post-translational modification of cysteine residues to form a persulfidated thiol motif, a process called protein persulfidation. We have developed a comparative and quantitative proteomic analysis approach for the detection of endogenous persulfidated proteins in wild-type Arabidopsis and L-CYSTEINE DESULFHYDRASE 1 mutant leaves using the tag-switch method. The 2015 identified persulfidated proteins were isolated from plants grown under controlled conditions, and therefore, at least 5% of the entire Arabidopsis proteome may undergo persulfidation under baseline conditions. Bioinformatic analysis revealed that persulfidated cysteines participate in a wide range of biological functions, regulating important processes such as carbon metabolism, plant responses to abiotic and biotic stresses, plant growth and development, and RNA translation. Quantitative analysis in both genetic backgrounds reveals that protein persulfidation is mainly involved in primary metabolic pathways such as the tricarboxylic acid cycle, glycolysis, and the Calvin cycle, suggesting that this protein modification is a new regulatory component in these pathways.