Hydrogen sulfide may function downstream of hydrogen peroxide in mediating darkness-induced stomatal closure in Vicia faba
Yinli Ma A C , Jiao Niu A , Wei Zhang A and Xiang Wu BA School of Life Sciences, Shanxi Normal University, Gongyuan Street No. 1, Linfen 041004, China.
B Hanzhong Forestry Science Research Institute, Zhengjiaba, Hanzhong 723000, China.
C Corresponding author. Email: mayinli1978@163.com
Functional Plant Biology 45(5) 553-560 https://doi.org/10.1071/FP17274
Submitted: 3 October 2017 Accepted: 21 November 2017 Published: 14 December 2017
Abstract
The relationship between hydrogen sulfide (H2S) and hydrogen peroxide (H2O2) during darkness-induced stomatal closure in Vicia faba L. was investigated by using pharmacological, spectrophotographic and lasers canning confocal microscopic approaches. Darkness-induced stomatal closure was inhibited by H2S scavenger hypotaurine (HT), H2S synthesis inhibitors aminooxy acetic acid (AOA) and hydroxylamine (NH2OH) and potassium pyruvate (N3H3KO3) and ammonia (NH3), which are the products of L-/D-cysteine desulfhydrase (L-/D-CDes). Moreover, darkness induced H2S generation and increased L-/D-CDes activity in leaves of V. faba. H2O2 scavenger and synthesis inhibitors suppressed darkness-induced increase of H2S levels and L-/D-CDes activity as well as stomatal closure in leaves of V. faba. However, H2S scavenger and synthesis inhibitors had no effect on darkness-induced H2O2 accumulation in guard cells of V. faba. From these data it can be deduced that H2S is involved in darkness-induced stomatal closure and acts downstream of H2O2 in V. faba.
Additional keywords: D-/L-cysteine, darkness, desulfhydrase, gasotransmitter, hydrogen sulphide, physiological and biochemical mechanisms.
References
Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. The Plant Cell 9, 1559–1572.| Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsFeltL8%3D&md5=3e282162bc415bf5d81e700f4077afffCAS |
Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. Journal of Experimental Botany 62, 4481–4493.
| Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKisb%2FL&md5=6de73b119621892bd767ab3196dc2c3cCAS |
Cross AR, Jones OT (1986) The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. The Biochemical Journal 237, 111–116.
| The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XksVWjsbY%3D&md5=16c7dea4fbd3460d44bdf33c80903e0eCAS |
Cui WT, Chen HP, Zhu KK, Jin QJ, Xie YJ, Cui J, Xia Y, Zhang J (2014) Cadmium-induced hydrogen sulfide synthesis is involved in cadmium tolerance in Medicago sativa by reestablishment of reduced (Homo) glutathione and reactive oxygen species homeostases. PLoS One 9, e109669
| Cadmium-induced hydrogen sulfide synthesis is involved in cadmium tolerance in Medicago sativa by reestablishment of reduced (Homo) glutathione and reactive oxygen species homeostases.Crossref | GoogleScholarGoogle Scholar |
Desikan R, Cheung MK, Clarke A, Golding S, Sagi M, Fluhr R, Rock C, Hancock J, Neill S (2004) Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum. Functional Plant Biology 31, 913–920.
| Hydrogen peroxide is a common signal for darkness- and ABA-induced stomatal closure in Pisum sativum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsleltbs%3D&md5=f6c57ad4957d2191bc0e632477444f99CAS |
Desikan R, Last K, Harrettwilliams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. The Plant Journal 47, 907–916.
| Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsL%2FP&md5=5a5389990ca1907aa69c7c2c5f153f5cCAS |
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239–247.
| Oxidants, oxidative stress and the biology of ageing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotFGltb0%3D&md5=3834de29b99afbd65229ee2b6f89bcbfCAS |
García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytologist 188, 977–984.
| Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling.Crossref | GoogleScholarGoogle Scholar |
He JM, Xu H, She XP, Song XG, Zhao WM (2005) The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Functional Plant Biology 32, 237–247.
| The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFWjt74%3D&md5=18f0d5e7e87e095beb517740b44df2abCAS |
He JM, Ma XG, Zhang Y, Sun TF, Xu FF, Chen YP, Liu X, Yue M (2013) Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiology 161, 1570–1583.
| Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFKru7c%3D&md5=8d4078b9d51c8b1246eb42284a0172a8CAS |
Hou ZH, Wang LX, Liu J, Hou LX, Liu X (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. Journal of Integrative Plant Biology 55, 277–289.
| Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVagsL0%3D&md5=5dfa9e90bb5cb28b5c615c2e02f8cbd8CAS |
Jin ZP, Xue SW, Luo YN, Tian BH, Fang HH, Li H, Pei YX (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiology and Biochemistry: PPB 62, 41–46.
| Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVCkurvL&md5=eebb457e70c6adc0b27fd4726d2ccd24CAS |
Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Current Opinion in Plant Biology 7, 323–328.
| Reactive oxygen signalling: the latest news.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVamsLg%3D&md5=0e06778b85e45f7968b23faaab517ce6CAS |
Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. Journal of Plant Physiology 161, 405–413.
| Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlCksbg%3D&md5=f65b1569947ce76401e7b4d987381b31CAS |
Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Schroeder Taylor AT, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiology 121, 147–152.
| Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGlsLc%3D&md5=8f3728183ffdec31dba9e120c86037e0CAS |
Li ZG, He QQ (2015) Hydrogen peroxide might be a downstream signal molecule of hydrogen sulfide in seed germination of mung bean (Vigna radiata). Biologia 70, 753–759.
| Hydrogen peroxide might be a downstream signal molecule of hydrogen sulfide in seed germination of mung bean (Vigna radiata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Ons7zL&md5=3a2e90e80071c9b2580f3bc310ad16dbCAS |
Li S, Xue L, Xu S, Feng H, An L (2007) Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber. Plant Growth Regulation 52, 173–180.
| Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsVOjtLs%3D&md5=2e612f33bf2f98ce062bbb576fc69649CAS |
Li ZG, Gong M, Xie H, Yang L, Li J (2012a) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Science 185–186, 185–189.
| Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin.Crossref | GoogleScholarGoogle Scholar |
Li ZG, Gong M, Liu P (2012b) Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha Curcas. Acta Physiologiae Plantarum 34, 2207–2213.
| Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha Curcas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFaqtrc%3D&md5=ddc99ea03dcc5d82f29bc579b9549333CAS |
Li Y, Xu S, Gao J, Pan S, Wang G (2016) Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba. Plant Physiology 156, 252–261.
| Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVOhur7M&md5=9d55958014d3377651bf13a3951fb4aaCAS |
Linden DR, Levitt MD, Farrugia G, Szurszewski JH (2010) Endogenous production of H2S in the gastrointestinal tract: still in search of a physiologic function. Antioxidants & Redox Signalling 12, 1135–1146.
| Endogenous production of H2S in the gastrointestinal tract: still in search of a physiologic function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlyitbk%3D&md5=981b7a3c70557889a3f5df94f5747e5dCAS |
Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiology and Biochemistry: PPB 48, 931–935.
| A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKmsr7M&md5=616b9be2df907367c7ad8f1b54961a60CAS |
Lisjak M, Teklić T, Wilson ID, Wood M, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signaling & Behavior 6, 1444–1446.
| Hydrogen sulfide effects on stomatal apertures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVGhsrY%3D&md5=1c5b4bfbf3571c5c9da080ffa436da2eCAS |
Liu J, Hou ZH, Liu GH, Liu LX (2012) Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L. Journal of Integrative Agriculture 11, 1644–1653.
| Hydrogen sulfide may function downstream of nitric oxide in ethylene-induced stomatal closure in Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKlurbK&md5=36788249ec8db14375e7ace575a2170fCAS |
Ma YL, Niu J (2017) The role of phytosphingosine-1-phosphate (Phyto-S1P) and its relationships with cytosolic pH and hydrogen peroxide (H2O2) during stomatal closure by darkness in broad bean. South African Journal of Botany 108, 237–242.
| The role of phytosphingosine-1-phosphate (Phyto-S1P) and its relationships with cytosolic pH and hydrogen peroxide (H2O2) during stomatal closure by darkness in broad bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVaku7nO&md5=89077c8e8e39e0c3adcfd9523b5baeffCAS |
Ma YL, She XP, Yang SS (2012) Sphingosine-1-phosphate (S1P) mediates darkness induced stomatal closure through raising cytosol pH and hydrogen peroxide (H2O2) levels in guard cells in Vicia faba. Science China. Life Sciences 55, 974–983.
| Sphingosine-1-phosphate (S1P) mediates darkness induced stomatal closure through raising cytosol pH and hydrogen peroxide (H2O2) levels in guard cells in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWru7bM&md5=25e262449cb704110ee9e94bae38d418CAS |
Ma YL, She XP, Yang SS (2013) Cytosolic alkalization-mediated H2O2 and NO production are involved in darkness-induced stomatal closure in Vicia faba. Canadian Journal of Plant Science 93, 119–130.
| Cytosolic alkalization-mediated H2O2 and NO production are involved in darkness-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivVSru74%3D&md5=37ac3803ba478f921bed8c2938ea9923CAS |
McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiology 111, 1031–1042.
| Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltVGgtrY%3D&md5=d021e98204d62573f81d786dd7c571b8CAS |
Mostofa MG, Saegusa D, Fujita M, Tran LSP (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Frontiers in Plant Science 6, 662
| Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress.Crossref | GoogleScholarGoogle Scholar |
Neill S, Desikan RJ, Hancock J (2002) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
| Hydrogen peroxide signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtlGjtL8%3D&md5=d1c2e42f252aac11ca7d3a964044f521CAS |
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
| Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVShtrc%3D&md5=7277270934194e36ae6e5c15bf98cab6CAS |
Pallaghy CK (1971) Stomatal movement and potassium transport in epidermal strips of Zea mays: the effect of CO2. Planta 101, 287–295.
| Stomatal movement and potassium transport in epidermal strips of Zea mays: the effect of CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XntVejug%3D%3D&md5=4baa60de213646dee8e904f55c2cfa70CAS |
Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiology 119, 849–858.
| The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFymtb4%3D&md5=f4324ada382cb75e2b7c32ccffcf5459CAS |
Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytologist 174, 742–751.
| Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth.Crossref | GoogleScholarGoogle Scholar |
Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. Journal of Biological Chemistry 277, 559–565.
| Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjslGntg%3D%3D&md5=1090ee609f8383f4ee409a8f161ed3eaCAS |
Rennenberg H, Arabatzis N, Grundel I (1987) Cysteine desulphydrase activity in higher plants: evidence for the action of L- and D-cysteine specific enzymes. Phytochemistry 26, 1583–1589.
| Cysteine desulphydrase activity in higher plants: evidence for the action of L- and D-cysteine specific enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXkslChu7Y%3D&md5=bf81306c2fd252bd9cc5e8b889604b9cCAS |
Riemenschneider A, Nikiforova V, Hoefgen R, De Kok LJ, Papenbrock J (2005a) Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiology and Biochemistry 43, 473–483.
| Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFCktr8%3D&md5=f9014ece47642531b76fee7e0b38f9d6CAS |
Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005b) Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. The FEBS Journal 272, 1291–1304.
| Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit12ru7g%3D&md5=bab81e929f8665370fdaf9a4639d9bf5CAS |
Schwartz A (1985) Role of Ca2+ and EGTA on stomatal movements in Commelina communis L. Plant Physiology 79, 1003–1005.
| Role of Ca2+ and EGTA on stomatal movements in Commelina communis L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xms1Whtw%3D%3D&md5=8934b0bde5d239de6c7c8b16ac0ae2e2CAS |
Scuffi D, Alvarez C, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiology 166, 2065–2076.
| Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure.Crossref | GoogleScholarGoogle Scholar |
Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to L-cysteine. Plant Physiology 70, 430–436.
| Emission of hydrogen sulfide by leaf tissue in response to L-cysteine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlsVWku7Y%3D&md5=d4da4826cfa4fa719e3b8138c123a803CAS |
She XP, Song XG (2008) Carbon monoxide-induced stomatal closure involves generation of hydrogen peroxide in Vicia faba guard cells. Journal of Integrative Plant Biology 50, 1539–1548.
| Carbon monoxide-induced stomatal closure involves generation of hydrogen peroxide in Vicia faba guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVWks70%3D&md5=b0713361575bd1056918499cfd9750e0CAS |
She XP, Song XG, He JM (2004) Role and relationship of nitric oxide and hydrogen peroxide in light/dark-regulated stomatal movement in Vicia faba. Acta Botanica Sinica 46, 1292–1300.
Song XG, She XP, Zhang B (2008) Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiologia Plantarum 132, 514–525.
| Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktbg%3D&md5=555f7d4b4c12881c4cad0f73211b429eCAS |
Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter. The FASEB Journal 16, 1792–1798.
| Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVChs7o%3D&md5=9d534881dde086ed203f76fc248d1bf0CAS |
Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant and Soil 351, 107–119.
| Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOks7g%3D&md5=989437778436e3eb282e9db21f857334CAS |
Wang LX, Ma XY, Che YM, Hou LX, Liu X, Zhang W (2015a) Extracellular ATP mediates H2S-regulatedstomatal movements and guard cell K+ current in a H2O2-dependent manner in Arabidopsis. Science Bulletin 60, 419–427.
| Extracellular ATP mediates H2S-regulatedstomatal movements and guard cell K+ current in a H2O2-dependent manner in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXis1yrtLw%3D&md5=8e53aa595c634181053a7d083c5b9bb4CAS |
Wang H, Xiao W, Niu Y, Chai R, Jin C, Zhang Y (2015b) Elevated carbon dioxide induces stomatal closure of Arabidopsis thaliana, (L.) Heynh. through an increased production of nitric oxide. Journal of Plant Growth Regulation 34, 372–380.
| Elevated carbon dioxide induces stomatal closure of Arabidopsis thaliana, (L.) Heynh. through an increased production of nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXls1aitQ%3D%3D&md5=bb064d82deffdb022cac4fb5cbc370caCAS |
Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. The Biochemical Journal 322, 681–692.
| Oxidative burst: an early plant response to pathogen infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXit1Ojsrs%3D&md5=d0fb6ec1363261cc82cc5946e8701d9bCAS |
Zeiger E (1983) The biology of stomatal guard cells. Plant Biology 34, 441–474.
Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei JZ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. Journal of Integrative Plant Biology 51, 1086–1094.
| Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmt1Cnug%3D%3D&md5=21991b4cb02cd769d9ed94742ff13548CAS |
Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regulation 58, 243–250.
| Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKntbo%3D&md5=3b2bf82dddca968257e210be7fe71f61CAS |
Zhang LP, Pei YX, Wang HJ, Jin ZP, Liu ZQ, Qiao ZJ, Fang HH, Zhang YJ (2015) Hydrogen sulfide alleviates cadmium-induced cell death through restraining ROS accumulation in roots of Brassica rapa L. ssp. pekinensis. Oxidative Medicine and Cellular Longevity 2015, 1–11.