Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Hydrogen sulfide induced by hydrogen peroxide mediates brassinosteroid-induced stomatal closure of Arabidopsis thaliana

Yinli Ma https://orcid.org/0000-0001-7040-3209 A B , Luhan Shao A , Wei Zhang https://orcid.org/0000-0001-8355-5738 A and Fengxi Zheng A
+ Author Affiliations
- Author Affiliations

A College of Life Sciences, Shanxi Normal University, Linfen 041004, People’s Republic of China.

B Corresponding author. Email: mayinli1978@163.com

Functional Plant Biology 48(2) 195-205 https://doi.org/10.1071/FP20205
Submitted: 14 July 2020  Accepted: 17 August 2020   Published: 11 September 2020

Abstract

The role of hydrogen sulfide (H2S) and its relationship with hydrogen peroxide (H2O2) in brassinosteroid-induced stomatal closure in Arabidopsis thaliana (L.) Heynh. were investigated. In the present study, 2,4-epibrassinolide (EBR, a bioactive BR) induced stomatal closure in the wild type, the effects were inhibited by H2S scavenger and synthesis inhibitors, and H2O2 scavengers and synthesis inhibitor. However, EBR failed to close the stomata of mutants Atl-cdes, Atd-cdes, AtrbohF and AtrbohD/F. Additionally, EBR induced increase of L-/D-cysteine desulfhydrase (L-/D-CDes) activity, H2S production, and H2O2 production in the wild type, and the effects were inhibited by H2S scavenger and synthesis inhibitors, and H2O2 scavengers and synthesis inhibitor respectively. Furthermore, EBR increased H2O2 levels in the guard cells of AtrbohD mutant, but couldn’t raise H2O2 levels in the guard cells of AtrbohF and AtrbohD/F mutants. Next, scavengers and synthesis inhibitor of H2O2 could significantly inhibit EBR-induced rise of L-/D-CDes activity and H2S production in the wild type, but H2S scavenger and synthesis inhibitors failed to repress EBR-induced H2O2 production. EBR could increase H2O2 levels in the guard cells of Atl-cdes and Atd-cdes mutants, but EBR failed to induce increase of L-/D-CDes activity and H2S production in AtrbohF and AtrbohD/F mutants. Therefore, we conclude that H2S and H2O2 are involved in the signal transduction pathway of EBR-induced stomatal closure. Altogether, our data suggested that EBR induces AtrbohF-dependent H2O2 production and subsequent AtL-CDes-/AtD-CDes-catalysed H2S production, and finally closes stomata in A. thaliana.

Additional keywords: hydrogen sulphide, hydrogen peroxide, stomatal closure, 2,4-epibrassinolide.


References

AbdElgawad H, Farfan-Vignolo ER, Vos DD, Asard H (2015) Article in press g model elevated CO2 mitigates drought and temperature-induced oxidative stress differently in grasses and legumes. Plant Science 231, 1–10.
Article in press g model elevated CO2 mitigates drought and temperature-induced oxidative stress differently in grasses and legumes.Crossref | GoogleScholarGoogle Scholar | 25575986PubMed |

Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Molecular Biology 69, 451–462.
Hormone interactions in stomatal function.Crossref | GoogleScholarGoogle Scholar | 19031047PubMed |

Ahanger MA, Ashraf M, Bajguz A, Ahmad P (2018) Brassinosteroids regulate growth in plants under stressful environments and crosstalk with other potential phytohormones. Plant Growth Regulation 37, 1007–1024.
Brassinosteroids regulate growth in plants under stressful environments and crosstalk with other potential phytohormones.Crossref | GoogleScholarGoogle Scholar |

Ahmad P, Ahanger MA, Alam P, Alyemeni MN (2018) Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (Hg) toxicity. Plant Growth Regulation 37, 309–322.
Modification of osmolytes and antioxidant enzymes by 24-epibrassinolide in chickpea seedlings under mercury (Hg) toxicity.Crossref | GoogleScholarGoogle Scholar |

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 | 12237396PubMed |

Caño-Delgado A, Yin YH, Yu C, Vafeados D, Mora-García S, Cheng JC, Nam KH, Li JM, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341–5351.
BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15486337PubMed |

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 | 21624977PubMed |

Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology 49, 427–451.
Brassinosteroids: essential regulators of plant growth and development.Crossref | GoogleScholarGoogle Scholar | 15012241PubMed |

Cross AR, Jones OTG (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 | 3800872PubMed |

De Bruyne L, Höfte M, De Vleesschauwer D (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Molecular Plant 7, 943–959.
Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity.Crossref | GoogleScholarGoogle Scholar | 24777987PubMed |

Desikan R, Last K, Harrett-Williams 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 | 16961732PubMed |

García-Mata C, Lamattina L (2010) Hydrogen sulfide, a novel gasotransmitter involved in guard cell signaling. New Phytologist 188, 977–984.
Hydrogen sulfide, a novel gasotransmitter involved in guard cell signaling.Crossref | GoogleScholarGoogle Scholar | 20831717PubMed |

Grove MD, Spencer GF, Rohwedder WK, Mandava N, Cook JLC (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281, 216–217.
Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen.Crossref | GoogleScholarGoogle Scholar |

Ha Y, Shang Y, Nam KH (2016) Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis. Journal of Experimental Botany 67, 6297–6308.
Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27856707PubMed |

Haubrick LL, Torsethaugen G, Assmann SM (2006) Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts. Plant Physiology 128, 134–143.
Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts.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 | 32689127PubMed |

Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
The role of stomata in sensing and driving environmental change.Crossref | GoogleScholarGoogle Scholar | 12931178PubMed |

Hou Z, Wang L, Liu J, Hou L, 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 | 23134300PubMed |

Hu Y, Fang B, Li J (2000) Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis. The Plant Journal 24, 693–701.
Promotive effect of brassinosteroids on cell division involves a distinct CycD3-induction pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11123807PubMed |

Jin Z, Pei Y (2015) Physiological implications of hydrogen sulfide in plants: pleasant exploration behind its unpleasant odour. Oxidative Medicine and Cellular Longevity 2015, 397502
Physiological implications of hydrogen sulfide in plants: pleasant exploration behind its unpleasant odour.Crossref | GoogleScholarGoogle Scholar | 26078819PubMed |

Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO Journal 22, 2623–2633.
NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12773379PubMed |

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 | 10482669PubMed |

Liu J, Hou ZH, Liu GH, Hou LX, Liu X (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 |

Ma YL, Niu J, Zhang W, Wu X (2018) Hydrogen sulfide may function downstream of hydrogen peroxide in mediating darkness-induced stomatal closure in Vicia faba. Functional Plant Biology 45, 533–560.
Hydrogen sulfide may function downstream of hydrogen peroxide in mediating darkness-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar |

Ma YL, Zhang W, Niu J (2019a) Hydrogen sulfide may function downstream of hydrogen peroxide in CdCl2-induced stomatal closure in Vigna radiata L. South African Journal of Botany 124, 39–46.
Hydrogen sulfide may function downstream of hydrogen peroxide in CdCl2-induced stomatal closure in Vigna radiata L.Crossref | GoogleScholarGoogle Scholar |

Ma YL, Zhang W, Niu J, Ren Y, Zhang F (2019b) Hydrogen sulfide may function downstream of hydrogen peroxide in mediating salt stress-induced stomatal closure in Vicia faba. Functional Plant Biology 46, 136–145.
Hydrogen sulfide may function downstream of hydrogen peroxide in mediating salt stress-induced stomatal closure in Vicia faba.Crossref | GoogleScholarGoogle Scholar |

Mandava NB (1988) Plant growth promoting brassinosteriods. Annual Review of Plant Physiology and Plant Molecular Biology 39, 23–52.
Plant growth promoting brassinosteriods.Crossref | GoogleScholarGoogle Scholar |

Mandava N, Kozempel M, Worley JF, Matthees D, Warthen JD, Jacobson M, Steffens GL, Kenney H, Grove MD (1978) Isolation of brassins by extraction of rape (Brassica napus L.) pollen. Industrial & Engineering Chemistry Product Research and Development 17, 351–354.
Isolation of brassins by extraction of rape (Brassica napus L.) pollen.Crossref | GoogleScholarGoogle Scholar |

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 | 12226345PubMed |

Mitchell JW, Mandava N, Worley JF, Plimmer JR, Smith MV (1970) Brassins - a new family of plant hormones from rape pollen. Nature 225, 1065–1066.
Brassins - a new family of plant hormones from rape pollen.Crossref | GoogleScholarGoogle Scholar | 16056912PubMed |

Müssig C, Shin GH, Altmann T (2003) Brassinosteroids promote root growth in Arabidopsis. Plant Physiology 133, 1261–1271.
Brassinosteroids promote root growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 14526105PubMed |

Nazir F, Hussain A, Fariduddin Q (2019) Interactive role of epibrassinolide and hydrogen peroxide in regulating stomatal physiology, root morphology, photosynthetic and growth traits in Solanum lycopersicum L. under nickel stress. Environmental and Experimental Botany 162, 479–495.
Interactive role of epibrassinolide and hydrogen peroxide in regulating stomatal physiology, root morphology, photosynthetic and growth traits in Solanum lycopersicum L. under nickel stress.Crossref | GoogleScholarGoogle Scholar |

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 | 15012235PubMed |

Riemenschneider A, Nikiforova V, Hoefgen RD, Kok LJ, Papenbrock J (2005) 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 | 15914014PubMed |

Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology 141, 336–340.
Production of reactive oxygen species by plant NADPH oxidases.Crossref | GoogleScholarGoogle Scholar | 16760484PubMed |

Saygideger S, Deniz F (2008) Effect of 24-epibrassinolide on biomass, growth and free proline concentration in Spirulina platensis (Cyanophyta) under NaCl stress. Plant Growth Regulation 56, 219–223.
Effect of 24-epibrassinolide on biomass, growth and free proline concentration in Spirulina platensis (Cyanophyta) under NaCl stress.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 | 16662510PubMed |

Shi C, Qi C, Ren H, Huang A, Hei S, She X (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Ga protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. The Plant Journal 82, 280–301.
Ethylene mediates brassinosteroid-induced stomatal closure via Ga protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25754244PubMed |

Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regulation 47, 111–119.
Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato.Crossref | GoogleScholarGoogle Scholar |

Steber CM, McCourt P (2001) A role for brassinosteroids in germination in Arabidopsis. Plant Physiology 125, 763–769.
A role for brassinosteroids in germination in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11161033PubMed |

Sun L, Li Y, Miao W, Piao T, Hao Y, Hao FS (2017) Nadk2 positively modulates abscisic acid-induced stomatal closure by affecting accumulation of H2O2, Ca2+, and nitric oxide in Arabidopsis guard cells. Plant Science 262, 81–90.
Nadk2 positively modulates abscisic acid-induced stomatal closure by affecting accumulation of H2O2, Ca2+, and nitric oxide in Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar | 28716423PubMed |

Tůmová L, Tarkowská D, Řehořová K, Marková H, Kočová M, Rothová O, et al (2018) Drought-tolerant and drought-sensitive genotypes of maize (Zea mays L.) differ in contents of endogenous brassinosteroids and their drought-induced changes. PLoS ONE 13, e0197870
Drought-tolerant and drought-sensitive genotypes of maize (Zea mays L.) differ in contents of endogenous brassinosteroids and their drought-induced changes.Crossref | GoogleScholarGoogle Scholar | 29795656PubMed |

Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB Journal 16, 1792–1798.
Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter?Crossref | GoogleScholarGoogle Scholar | 12409322PubMed |

Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiological Reviews 92, 791–896.
Physiological implications of hydrogen sulfide: a whiff exploration that blossomed.Crossref | GoogleScholarGoogle Scholar | 22535897PubMed |

Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytologist 178, 703–718.
Guard-cell signalling for hydrogen peroxide and abscisic acid.Crossref | GoogleScholarGoogle Scholar | 18373649PubMed |

Witthöft J, Harter K (2011) Latest news on Arabidopsis brassinosteroid perception and signaling. Frontiers in Plant Science 2, 58
Latest news on Arabidopsis brassinosteroid perception and signaling.Crossref | GoogleScholarGoogle Scholar | 22639599PubMed |

Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen Z, Yu J-Q (2009a) Brassinosteroids promote photosynthesis and growth by enhancing activation of rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230, 1185–1196.
Brassinosteroids promote photosynthesis and growth by enhancing activation of rubisco and expression of photosynthetic genes in Cucumis sativus.Crossref | GoogleScholarGoogle Scholar | 19760261PubMed |

Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Yu JQ (2009b) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiology 150, 801–814.
Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber.Crossref | GoogleScholarGoogle Scholar | 19386805PubMed |

Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant, Cell & Environment 37, 2036–2050.
Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. Journal of Integrative Plant Biology 50, 1518–1529.
Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress.Crossref | GoogleScholarGoogle Scholar | 19093970PubMed |

Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) 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 | 20021556PubMed |

Zhang TY, Li FC, Fan CM, Li X, Zhang FF, He JM (2017) Role and interrelationship of MEK1–MPK6 cascade, hydrogen peroxide and nitric oxide in darkness-induced stomatal closure. Plant Science 262, 190–199.
Role and interrelationship of MEK1–MPK6 cascade, hydrogen peroxide and nitric oxide in darkness-induced stomatal closure.Crossref | GoogleScholarGoogle Scholar | 28716416PubMed |