Crosstalk Between Hydrogen Sulfide and Other Signal Molecules
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International Journal of Molecular Sciences Review Crosstalk between Hydrogen Sulfide and Other Signal Molecules Regulates Plant Growth and Development Lijuan Xuan y, Jian Li y, Xinyu Wang and Chongying Wang * Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou 730000, China; [email protected] (L.X.); [email protected] (J.L.); [email protected] (X.W.) * Correspondence: [email protected]; Tel./Fax: +86-093-1891-4155 These authors contributed equally to this work. y Received: 31 May 2020; Accepted: 24 June 2020; Published: 28 June 2020 Abstract: Hydrogen sulfide (H2S), once recognized only as a poisonous gas, is now considered the third endogenous gaseous transmitter, along with nitric oxide (NO) and carbon monoxide (CO). Multiple lines of emerging evidence suggest that H2S plays positive roles in plant growth and development when at appropriate concentrations, including seed germination, root development, photosynthesis, stomatal movement, and organ abscission under both normal and stress conditions. H2S influences these processes by altering gene expression and enzyme activities, as well as regulating the contents of some secondary metabolites. In its regulatory roles, H2S always interacts with either plant hormones, other gasotransmitters, or ionic signals, such as abscisic acid (ABA), ethylene, auxin, 2+ CO, NO, and Ca . Remarkably, H2S also contributes to the post-translational modification of proteins to affect protein activities, structures, and sub-cellular localization. Here, we review the functions of H2S at different stages of plant development, focusing on the S-sulfhydration of proteins mediated by H2S and the crosstalk between H2S and other signaling molecules. Keywords: hydrogen sulfide; reactive oxygen species; S-sulfhydration; plant hormone; gasotransmitter 1. Introduction Sulfur (S) is an essential element and is involved in the synthesis and metabolism of the sulfur-containing amino acids cysteine (Cys) and methionine (Met), as well as co-enzyme A, thiamine, biotin, iron-sulfur clusters, and nitrogenase. Only plants, algae, fungi, and some prokaryotes can 2 take advantage of the inorganic sulfur (sulfate, SO4 −) naturally found in soils and incorporate it into 2 organic forms [1]. During sulfur assimilation in plants, the SO4 − absorbed by roots is first reduced to hydrogen sulfide (H2S) under the catalysis of adenosine-50-phosphoryl sulfate reductase (APSR) and sulfite reductase (SIR) and then transformed into Cys under the catalysis of O-Acetylserine (thiol) lyase (OAS-TL). Therefore, H2S is an extremely important intermediate in the thio-metabolism pathway. H2S can also be generated from chloroplasts and mitochondria through the reduction of Cys by β-cyanoalanine synthase (CAS) and cysteine desulfhydrase (CDes) [2–5]. CAS can transform cyanide (CN−) and L-Cys into β–cyanoalanine and H2S to degrade the toxin cyanogen (Figure1)[ 3,6,7]. CDes, such as L-cysteine desulfhydrase (LCD, at3g62130) [2], L-cysteine desulfhydrase 1 (DES1, at5g28030) [4], D-cysteine desulfhydrase 1 (DCD1, at1g48420), and D-cysteine desulfhydrase 2 (DCD2, at3g26115) in Arabidopsis, catalyze both L-Cys and D-Cys into H2S, pyruvate, and ammonia. LCD and DES1 use L-Cys as substrate and are the two pivotal enzymes in the process of endogenous H2S production [2]. Int. J. Mol. Sci. 2020, 21, 4593; doi:10.3390/ijms21134593 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 4593 2 of 21 (DES1, at5g28030) [4], D-cysteine desulfhydrase 1 (DCD1, at1g48420), and D-cysteine desulfhydrase 2 (DCD2, at3g26115) in Arabidopsis, catalyze both L-Cys and D-Cys into H2S, pyruvate, and ammonia. LCD and DES1 use L-Cys as substrate and are the two pivotal enzymes in the process of endogenousInt. J. Mol. Sci. 2020 H2S, 21production, 4593 [2]. 2 of 22 Figure 1. The synthesis and metabolism of H2S in higher plants. H2S is generated coincident with sulfate reduction in the plant cell. The key enzymes in H2S biosynthesis and metabolism include sulfite Figurereductase 1. (SIR),The synthesis L-cysteine and desulfhydrase metabolism (L-CDes), of H2S in D-cysteine higher plants. desulfhydrase H2S is generated (D-CDes), coincidentβ-cyanoalanine with sulfatesynthase reduction (CAS), andin the O-acetylserine(thiol)lyase plant cell. The key enzymes (OAS-TL). in H2 PlantsS biosynthesis are capable and of metabolism reducing activated include sulfite reductase2 (SIR), L-cysteine2 desulfhydrase (L-CDes), 2D-cysteine desulfhydrase (D-CDes), β- sulfate (SO4 −) to sulfite (SO3 −), after that SIR catalyzes SO3 − to H2S, with ferredoxin (Fdred) as the cyanoalanine synthase (CAS), and O-acetylserine(thiol)lyase (OAS-TL). Plants are capable of reducing electron donor. In the presence of OAS-TL, the generated H2S is reversibly reduced to L-cysteine by 2− 2− 2- activatedreacting withsulfate O-acetylserine (SO4 ) to sulfite (OAS). (SO L-CDes3 ), after and that D-CDes SIR catalyzes catalyze SO3 the to degradation H2S, with ferredoxin of L/D-cysteine (Fdred) as the electron donor. In the presence of OAS-TL, the generated H2S is reversibly reduced to L-cysteine to produce H2S, amine (NH3) and pyruvate to maintain H2S homeostasis. CAS, located in the by reacting with O-acetylserine (OAS). L-CDes and D-CDes catalyze the degradation of L/D-cysteine mitochondria, can also catalyze the production of H2S, using cyanide (CN−) and cysteine as substrates, toremoving produce the H toxin2S, amine cyanogen. (NH3) and pyruvate to maintain H2S homeostasis. CAS, located in the mitochondria, can also catalyze the production of H2S, using cyanide (CN−) and cysteine as substrates, removingH2S is a toxicthe toxin gaseous cyanogen. molecule with the pungent odor of rotten eggs and has serious impacts on animals and plants [8]. Just 30 µmol/LH2S can inhibit the activity of mitochondrial cytochrome c oxidaseH2S is and a toxic reduce gaseous the intensitymolecule ofwith mitochondrial the pungent respirationodor of rotten by eggs 50% and [9]. has Surprisingly, serious impacts H2S also on animalsfunctions and as aplants gasotransmitter, [8]. Just 30 μ withmol/L essential H2S can roles inhibit at dithefferent activity stages of mitochondrial of plant development. cytochrome H2 Sc oxidaseinteracts and with reduce other signals, the intensity such as of plant mitochondrial hormones, other respiration gasotransmitters, by 50% [9]. and Surprisingly, ionic signals. H H2S2S also can functionsalso post-translationally as a gasotransmitter, modify proteinswith essential or affect roles secondary at different metabolism stages [of10 ].plant During development. seed imbibition, H2S interactsthe endogenous with other H2 Ssignals, level increases such as plant in Arabidopsis hormones, underother gasotransmitters, normal growth conditions and ionic signals. [11]. When H2S canthe germinationalso post-translationally of wheat seed modi is inhibitedfy proteins under or copperaffect secondar (Cu) stress,y metabolism treatment with [10]. an During appropriate seed imbibition,concentration the of endogenous exogenous H H22SS level (1.4 mM)increases promotes in Arabidopsis germination under by reducingnormal growth oxidative conditions damage [11]. [12]. WhenIn addition, the germination H2S induces of stomatalwheat seed movement is inhibit ofed guard under cells copper and (Cu) serves stress, as a switchtreatment in stomatalwith an appropriateopening [13 ].concentration The application of exogenous of an exogenous H2S (1.4 H2 mM)S donor promotes (sodium germination hydrosulfide by (NaHS) reducing or oxidative GYY4137 damage(morpholine-4-4-methoxyphenyl)) [12]. In addition, H2S induces reduces stomatal the nitricmovement oxide (NO)of guar accumulationd cells and serves induced as a by switch abscisic in stomatalacid (ABA) opening and promotes [13]. The guardapplication cell movement of an exogenous to allow H stomatal2S donor opening(sodium inhydrosulfide light or darkness (NaHS) [14 or]. GYY4137In Arabidopsis, (morpholine-4-4-methoxyphenyl)) mutation of des1 leads to premature reduces th senescencee nitric oxide of leaves(NO) accumulation [15]. In many induced fruits and by abscisicvegetables, acid H 2(ABA)S treatment and promotes delays premature guard cell leaf movement senescence to and allow the decaystomatal of fruits opening after harvestin light viaor darknessreducing the[14]. accumulation In Arabidopsis, of reactive mutation oxygen of des1 species leads to (ROS) premature [16,17] andsenescence inhibits of the leaves abscission [15]. In of many plant fruitsorgans and via increasingvegetables, the H2 contentS treatment of auxin delays in abscission premature zone leaf tissues senescence [18]. A and recent the report decay has of shownfruits after that harvestthere is avia significant reducing increase the accumulation in the S-sulfhydration of reactive level oxygen of the species actin proteins (ROS) in[16,17] an H 2andS-overproducing inhibits the abscissionline, created of byplant the organs over-expression via increasing of LCD thein content the Arabidopsis of auxin O-acetylserine(thiol)lyasein abscission zone tissues isoform [18]. a1A recent(oasa1) reportmutant has (OE shown LCD-5 that/oas-a1 there). Thisis a si increasegnificant in increase S-sulfhydration in the S-sulfhydration decreased the level distribution of the actin of theproteins actin cytoskeleton, which directly weakened actin polymerization and impaired root hair growth [19]. Here, we comprehensively review the functions of H2S in plant growth and development under normal or adverse