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

Hydrogen sulfide may function downstream of hydrogen peroxide in salt stress-induced stomatal closure in Vicia faba

Yinli Ma A B , Wei Zhang https://orcid.org/0000-0001-8355-5738 A , Jiao Niu A , Yu Ren A and Fan Zhang A
+ Author Affiliations
- Author Affiliations

A School of Life Sciences, Shanxi Normal University, Linfen 041004, China.

B Corresponding author. Email: mayinli1978@163.com

Functional Plant Biology 46(2) 136-145 https://doi.org/10.1071/FP18096
Submitted: 13 April 2018  Accepted: 3 September 2018   Published: 17 October 2018

Abstract

The roles of hydrogen sulfide (H2S) and hydrogen peroxide (H2O2) in signalling transduction of stomatal closure induced by salt stress were examined by using pharmacological, spectrophotographic and laser scanning confocal microscopic (LSCM) approaches in Vicia faba L. Salt stress resulted in stomatal closure, and this effect was blocked by H2S modulators hypotaurine (HT), aminooxy acetic acid (AOA), hydroxylamine (NH2OH), potassium pyruvate (C3H3KO3) and ammonia (NH3) and H2O2 modulators ascorbic acid (ASA), catalase (CAT), diphenylene iodonium (DPI). Additionally, salt stress induced H2S generation and increased L-/D-cysteine desulfhydrase (L-/D-CDes, pyridoxalphosphate-dependent enzyme) activity in leaves, and caused H2O2 production in guard cells, and these effects were significantly suppressed by H2S modulators and H2O2 modulators respectively. Moreover, H2O2 modulators suppressed salt stress-induced increase of H2S levels and L-/D-CDes activity in leaves as well as stomatal closure of V. faba. However, H2S modulators had no effects on salt stress-induced H2O2 production in guard cells. Altogether, our data suggested that H2S and H2O2 probably are involved in salt stress-induced stomatal closure, and H2S may function downstream of H2O2 in salt stress-induced stomatal movement in V. faba.

Additional keywords: broad bean, desulfhydrase, D-/L-cysteine, gasotransmitter, hydrogen sulphide, physiological and biochemical mechanisms, salt stress.


References

Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiology 123, 1047–1056.
Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp.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 |

An GY, Li BZ, Wu GL, Song CP (2012) H2O2 could act as root source signal to mediate stomatal closure induced by salt stress of Vicia faba L. Plant Physiology Journal 48, 265–271.

Boughanmi N, Michonneau P, Daghfous D, Fleuratlessard P (2005) Adaptation of Medicago sativa cv. Gabès to long-term NaCl stress. Journal of Plant Nutrition and Soil Science 168, 262–268.
Adaptation of Medicago sativa cv. Gabès to long-term NaCl stress.Crossref | GoogleScholarGoogle Scholar |

Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 non-halophytes. Plant Physiology 95, 628–635.
Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 non-halophytes.Crossref | GoogleScholarGoogle Scholar |

Che YM, Zou X, Wang LX, Zhang DD, Liu X (2012) H2S signals salt-induced stomatal closure in Arabidopsis thaliana by SOS pathway. Plant Physiology Journal 48, 1098–1104.

Che YM, Zhang DD, Hou LX, Wang LX, Liu X (2015) Extracellular adenosine triphosphate functions downstream of hydrogen sulfide in ethylene-induced stomatal closure in Arabidopsis thaliana. Chinese Bulletin of Botany 50, 22–31.

Chen SS, Lin HY (2011b) Signal transduction pathways in response to salt stress in plants. Plant Physiology Journal 47, 119–128.

Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011a) 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 |

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 |

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 |

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 |

Downton WJS, Loveys BR, Grant WJR (1990) Salinity effects on the stomatal behaviour of grapevine. New Phytologist 116, 499–503.
Salinity effects on the stomatal behaviour of grapevine.Crossref | GoogleScholarGoogle Scholar |

Fang T, Cao Z, Li J, Shen W, Huang L (2014) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiology and Biochemistry 76, 44–51.
Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato.Crossref | GoogleScholarGoogle Scholar |

Finkel T (2000) Redox-dependent signal transduction. FEBS Letters 476, 52–54.
Redox-dependent signal transduction.Crossref | GoogleScholarGoogle Scholar |

Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of aging. Nature 408, 239–247.
Oxidants, oxidative stress and the biology of aging.Crossref | GoogleScholarGoogle Scholar |

Gadalla MM, Snyder SH (2010) Hydrogen sulfide as a gasotransmitter. Journal of Neurochemistry 113, 14–26.
Hydrogen sulfide as a gasotransmitter.Crossref | GoogleScholarGoogle Scholar |

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 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 interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean.Crossref | GoogleScholarGoogle Scholar |

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 |

Hou ZH, Liu J, Hou LX, Li XD, Liu X (2011) H2S may function downstream of H2O2 in jasmonic acid-induced stomatal closure in Vicia faba. Chinese Bulletin of Botany 46, 396–406.

Hou ZH, Che YM, Wang LX, Hou LX, Liu X (2012) H2S functions downstream of H2O2 in mediating ethylene-induced stomatal closure in Arabidopsis thaliana. Plant Physiology Journal 48, 1193–1199.

Hou ZH, Liu GH, Hou LX, Liu X (2013a) Regulatory function of polyamine oxidase-generated hydrogen peroxide in ethylene-induced stomatal closure in Arabidopsis thaliana. Journal of Integrative Agriculture 12, 251–262.
Regulatory function of polyamine oxidase-generated hydrogen peroxide in ethylene-induced stomatal closure in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Hou ZH, Wang LX, Liu J, Hou LX, Liu X (2013b) 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 |

Huang H, Guo SS, Chen LC, Xiao B (2017) Effects of exogenous hydrogen sulfide on the antioxidant characteristics of tea plant (Camellia sinensis) under salt stress. Plant Physiology Journal 53, 497–504.

Jia W, Zhang J (2008) Stomatal movements and long-distance signaling in plants. Plant Signaling & Behavior 3, 772–777.
Stomatal movements and long-distance signaling in plants.Crossref | GoogleScholarGoogle Scholar |

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 62, 41–46.
Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Kimura H (2011) Hydrogen sulfide: its production, release and functions. Experimental Physiology 41, 113–121.

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 |

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 |

Li S, Xue L, Xu S, Feng H, An L (2007) Hydrogen peroxide involvement in generation and development of adventitious roots in cucumber. Plant Growth Regulation 52, 173–180.
Hydrogen peroxide involvement in generation and development of adventitious roots in cucumber.Crossref | GoogleScholarGoogle Scholar |

Li ZG, Gong M, Xie H, Yang L, Li J (2012) 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 Y, Xu S, Gao J, Pan S, Wang G (2014) Chlorella induces stomatal closure via NADPH oxidase-dependent ROS production and its effects on instantaneous water use efficiency in Vicia faba. PLoS One 9,
Chlorella induces stomatal closure via NADPH oxidase-dependent ROS production and its effects on instantaneous water use efficiency in Vicia faba.Crossref | GoogleScholarGoogle Scholar |

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. Physiologia Plantarum 156, 252–261.
Glucose- and mannose-induced stomatal closure is mediated by ROS production, Ca2+ and water channel in Vicia faba.Crossref | GoogleScholarGoogle Scholar |

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 |

Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson L, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiology and Biochemistry 48, 931–935.
A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation.Crossref | GoogleScholarGoogle Scholar |

Lisjak M, Hancock JT, Wilson ID, Whiteman M, Špoljarević M, Teklić T (2011) H2S and NO interactions in stomatal control and salt stress response in plants. Hinyokika Kiyo. Acta Urologica Japonica 35, 1431–1437.

Liu J, Hou LX, Liu GH, Liu X, Wang XC (2011) Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Science Bulletin 56, 3547–3553.
Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana.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, 553–560.
Hydrogen sulfide may function downstream of hydrogen peroxide in mediating darkness-induced stomatal closure in Vicia faba.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 |

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 of Plant Science 6, 1055
Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress.Crossref | GoogleScholarGoogle Scholar |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar |

Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388–395.
Hydrogen peroxide signalling.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 |

Parida AK, Das AB (2004) Effects of NaCl stress on nitrogen and phosphorous metabolism in a true mangrove Bruguiera parviflora grown under hydroponic culture. Journal of Plant Physiology 161, 921–928.
Effects of NaCl stress on nitrogen and phosphorous metabolism in a true mangrove Bruguiera parviflora grown under hydroponic culture.Crossref | GoogleScholarGoogle Scholar |

Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60, 324–349.
Salt tolerance and salinity effects on plants: a review.Crossref | GoogleScholarGoogle Scholar |

Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.
Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.Crossref | GoogleScholarGoogle Scholar |

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 |

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 AX, Wang YM (2010) Effects of salt stress on stomatal differentiation and movements of amaranth (Amaranthus tricolor L.) leaves. Acta Horticulturae Sinica 37, 479–484.

Rennenberg H (1984) The fate of excess sulfur in higher plants. Annual Review of Plant Biology 35, 121–153.
The fate of excess sulfur in higher plants.Crossref | GoogleScholarGoogle Scholar |

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 |

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 |

Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005b) Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS Journal 272, 1291–1304.
Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Robinson MF, Very AA, Sanders D, Mansfield TA (1997) How can stomata contribute to salt tolerance? Annals of Botany 80, 387–393.
How can stomata contribute to salt tolerance?Crossref | GoogleScholarGoogle Scholar |

Scuffi D, Álvarez 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 |

Scuffi D, Nietzel T, Di Fino LM, Meyer AJ, Lamattina L, Schwarzländer M, Laxalt AM, García-Mata C (2018) Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling. Plant Physiology 176, 2532–2542.
Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling.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 |

Sergey S, Tracey AC (2012) ‘Plant salt tolerance.’ (Humana Press: New York)

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.

Véry AA, Robinson MF, Mansfield TA, Sanders D (1998) Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. The Plant Journal 14, 509–521.
Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte.Crossref | GoogleScholarGoogle Scholar |

Wang LX, Hou ZH, Hou LX, Zhao FG, Liu X (2012a) H2S induced by H2O2 mediates drought-induced stomatal closure in Arabidopsis thaliana. Chinese Bulletin of Botany 47, 217–225.

Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012b) 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 |

Wang LX, Ma XY, Che YM, Hou LX, Liu X, Zhang W (2015) Extracellular ATP mediates H2S- regulated stomatal movements and guard cell K+ current in a H2O2-dependent manner in Arabidopsis. Chinese Science Bulletin 60, 419–427.

Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiology 61, 184–189.
Light-dependent emission of hydrogen sulfide from plants.Crossref | GoogleScholarGoogle Scholar |

Wu YP, Li HW, Hou LX, Zhang DD, Liu X (2014) ATP-binding cassettee transporter signals salt-induced stomatal closure in Arabidopsis thaliana L. by H2S pathway. Plant Physiology Journal 50, 401–406.

Ye Q, Hou ZH, Liu J, Liu RQ, Liu X (2011) H2O2 involvement in H2S-induced stomatal closure of Arabidopsis thaliana L. Plant Physiology Journal 47, 1195–1200.

Zeiger E (1983) The biology of stomatal guard cells. Plant Biology 34, 441–474.

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 |

Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei JZ, 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 |

Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiologiae Plantarum 32, 849–857.
Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar |

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.

Zhao X, Wang YL, Wang YJ, Wang XL, Zhang X (2008) Effects of exogenous Ca2+ on stomatal movement and plasma membrane K+ channels of Vicia faba guard cell under salt stress. Acta Agronomica Sinica 34, 1970–1976.
Effects of exogenous Ca2+ on stomatal movement and plasma membrane K+ channels of Vicia faba guard cell under salt stress.Crossref | GoogleScholarGoogle Scholar |

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar |