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The role of hydrogen sulfide in plant alleviates heavy metal stress

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Abstract

Background

With continuing industrial pollution and other human activities, the problem of heavy metal pollution in the environment is becoming more and more serious. Because heavy metal toxicity does not only inhibit plant growth but also causes many adverse health conditions in humans, heavy metal pollution poses a great challenge across the global. As a food security issue, how to minimize the influence of heavy metals stress on plants has become a major topic of research. This paper explores the mechanism of hydrogen sulfide (H2S) as a plant-signaling molecule, which participates in the response to heavy metal stress and enhances plant tolerance to various stresses.

Conclusion

Here, we reviewed research progress on the role of H2S in plant response to heavy metal stress and discussed the mechanism by which H2S alleviating heavy metal stress. Moreover, a future research direction is also proposed.

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References

  • Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf 94:164–171

    CAS  PubMed  Google Scholar 

  • Ahmad P (2016) Plant metal interaction, pp 263-283

  • Ahmad R, Ali S, Rizwan M, Dawood M, Farid M, Hussain A, Wijaya L, Alyemeni MN, Ahmad P (2019) Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiol Plant. https://doi.org/10.1111/ppl.13001

  • Ali S, Zeng F, Qiu L, Zhang G (2011) The effect of chromium and aluminum on growth, root morphology, photosynthetic parameters and transpiration of the two barley cultivars. Biol Plant 55:291–296

    CAS  Google Scholar 

  • Ali S, Cai S, Zeng F, Qiu B, Zhang G (2012) Effect of salinity and hexavalent chromium stresses on uptake and accumulation of mineral elements in barley genotypes differing in salt tolerance. J Plant Nutr 35:827–839

    CAS  Google Scholar 

  • Ali S, Farooq MA, Hussain S, Yasmeen T, Abbasi GH, Zhang G (2013) Alleviation of chromium toxicity by hydrogen sulfide in barley. Environ Toxicol Chem 32:2234–2239

    CAS  PubMed  Google Scholar 

  • Ali B, Mwamba TM, Gill RA, Chong Y, Ali S, Daud MK, Wu Y, Zhou W (2014a) Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 74:261–273

    CAS  Google Scholar 

  • Ali B, Song WJ, Hu WZ, Luo XN, Gill RA, Wang J, Zhou WJ (2014b) Hydrogen sulfide alleviates lead-induced photosynthetic and ultrastructural changes in oilseed rape. Ecotoxicol Environ Saf 102:25–33

    CAS  PubMed  Google Scholar 

  • Álvarez C, Calo L, Romero LC, García I, Gotor C (2010) An O-acetylserine (thiol) lyase homolog with L-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669

    PubMed  PubMed Central  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Aroca Á, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barnhart J (1997) Occurrences, uses, and properties of chromium. Regul Toxicol Pharmacol 26:3–7

    Google Scholar 

  • Basharat A, Ping Q, Rui S, Farooq MA, Gill RA, Jian W, Muhammad A, Weijun Z (2015) Hydrogen sulfide alleviates the aluminum-induced changes in Brassica napus as revealed by physiochemical and ultrastructural study of plant. Environ Sci Pollut Res Int 22:3068–3081

    Google Scholar 

  • Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58

    CAS  PubMed  Google Scholar 

  • Burkhead JL, Reynolds KA, Abdelghany SE, Cohu CM, Pilon M (2010) Copper homeostasis. New Phytol 182:799–816

    Google Scholar 

  • 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. J Exp Bot 62:4481–4493

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wang W-H, Wu F-H, You C-Y, Liu T-W (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    CAS  Google Scholar 

  • Corpas FJ (2019) Hydrogen sulfide: a new warrior against abiotic stress. Trends Plant Sci 24:983–988

    CAS  PubMed  Google Scholar 

  • Corpas FJ, González-Gordo S, Cañas A, Palma JM (2019) Nitric oxide and hydrogen sulfide in plants: which comes first? J Exp Bot 70:4391–4404

    PubMed  Google Scholar 

  • Cui W, Chen H, Zhu K, Jin Q, Xie Y, Cui J, Xia Y, Zhang J, Shen W (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

    PubMed  PubMed Central  Google Scholar 

  • Dai H, Xu Y, Zhao L, Shan C (2016) Alleviation of copper toxicity on chloroplast antioxidant capacity and photosystem II photochemistry of wheat by hydrogen sulfide. Braz J Bot 39:787–793

    Google Scholar 

  • Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209-210:121–128

    CAS  PubMed  Google Scholar 

  • Delhaize E, Jian FM, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348

    CAS  PubMed  Google Scholar 

  • Deng YQ, Bao J, Yuan F, Liang X, Feng ZT, Wang BS (2016) Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na + content. Plant Growth Regul 79:391–399

    CAS  Google Scholar 

  • Dimkpa CO, Merten D, Svato SA, Büchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162

    CAS  Google Scholar 

  • Du X, Jin Z, Zhang L, Liu X, Yang G, Pei Y (2018) H2S is involved in ABA-mediated stomatal movement through MPK4 to alleviate drought stress in Arabidopsis thaliana. Plant Soil

  • Eija PT, Marja K, Frantisek S, Eva-Mari A, Esa TR (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367

    Google Scholar 

  • Fang H, Jing T, Liu Z, Zhang L, Jin Z, Pei Y (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481

    CAS  PubMed  Google Scholar 

  • Fang H, Liu Z, Jin Z, Zhang L, Liu D, Pei Y (2016) An emphasis of hydrogen sulfide-cysteine cycle on enhancing the tolerance to chromium stress in Arabidopsis ☆. Environ Pollut 213:870–877

    CAS  PubMed  Google Scholar 

  • Flora SJS, Megha M, Ashish M (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128:501–523

    CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu M-M, Dawood M, Wang N-H, Wu F (2019) Exogenous hydrogen sulfide reduces cadmium uptake and alleviates cadmium toxicity in barley. Plant Growth Regul 89:227–237. https://doi.org/10.1007/s10725-019-00529-8

    Article  CAS  Google Scholar 

  • Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984. https://doi.org/10.1111/j.1469-8137.2010.03465.x

    Article  CAS  PubMed  Google Scholar 

  • Guan MY, Zhang HH, Pan W, Jin CW, Lin XY (2018) Sulfide alleviates cadmium toxicity in Arabidopsis plants by altering the chemical form and the subcellular distribution of cadmium. Sci Total Environ 627:663–670

    CAS  PubMed  Google Scholar 

  • He H, Li Y, He L-F (2018) The central role of hydrogen sulfide in plant responses to toxic metal stress. Ecotoxicol Environ Saf 157:403–408

    CAS  PubMed  Google Scholar 

  • Herouart D, Van Montagu M, Inze D (1993) Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proc Natl Acad Sci 90:3108–3112

    CAS  PubMed  Google Scholar 

  • Hou Z, Wang L, Liu J, Hou L, Liu X (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol 55:277–289

    CAS  PubMed  Google Scholar 

  • Huang ZQ, Ye SC, Hu LY, Hu KD, Yan H, Li WJ, Jiao H, Zhang H (2015) Hydrogen sulfide promotes wheat grain germination under cadmium stress. P Natl A Sci India B 86:887–895

  • Jia H, Hu Y, Fan T, Li J (2015) Hydrogen sulfide modulates actin-dependent auxin transport via regulating ABPs results in changing of root development in Arabidopsis. Sci Rep 5:8251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jian S, Wang R, Xuan Z, Yu Y, Rui Z, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74

    Google Scholar 

  • Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46

    CAS  PubMed  Google Scholar 

  • Kabała K, Zboińska M, Głowiak D, Reda M, Jakubowska D, Janicka M (2019) Interaction between the signaling molecules hydrogen sulfide and hydrogen peroxide and their role in vacuolar H+-ATPase regulation in cadmium-stressed cucumber roots. Physiol Plant 166:688–704. https://doi.org/10.1111/ppl.12819

    Article  CAS  PubMed  Google Scholar 

  • Kaya C, Ashraf M, Akram NA (2018) Hydrogen sulfide regulates the levels of key metabolites and antioxidant defense system to counteract oxidative stress in pepper ( Capsicum annuum L.) plants exposed to high zinc regime. Environ Sci Pollut Res Int 25:1–7

    Google Scholar 

  • Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2019) Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol Plant. https://doi.org/10.1111/ppl.13012

  • Kharbech O, Houmani H, Chaoui A, Corpas FJ (2017) Alleviation of Cr (VI)-induced oxidative stress in maize (Zea mays L.) seedlings by NO and H2S donors through differential organ-dependent regulation of ROS and NADPH-recycling metabolisms. J Plant Physiol 219:71–80

    CAS  PubMed  Google Scholar 

  • Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    CAS  PubMed  Google Scholar 

  • Kopittke PM, Blamey FPC, Asher CJ, Menzies NW (2010) Trace metal phytotoxicity in solution culture: a review. J Exp Bot 61:945

    CAS  PubMed  Google Scholar 

  • Lai D, Mao Y, Zhou H, Li F, Wu M, Zhang J, He Z, Cui W, Xie Y (2014) Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa. Plant Sci 225:117–129

    CAS  PubMed  Google Scholar 

  • Li ZG, Liu P (2012) Hydrogen sulfide is a mediator in HO-induced seed germination in Jatropha Curcas. Acta Physiol Plant 34:2207–2213

    CAS  Google Scholar 

  • Li L, Wang Y, Shen W (2012a) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631

    CAS  PubMed  Google Scholar 

  • Li Z-G, Gong M, Xie H, Yang L, Li J (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185:185–189

    PubMed  Google Scholar 

  • Li ZG, Gong M, Xie H, Yang L, Li J (2012c) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco ( Nicotiana tabacum L) suspension cultured cells and involvement of Ca 2+ and calmodulin. Plant Sci 185-186:185–189

    CAS  PubMed  Google Scholar 

  • Li Z-G, Xie L-R, Li X-J (2015) Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J Plant Physiol 177:121–127

    CAS  PubMed  Google Scholar 

  • Lin Y-T, Li M-Y, Cui W-T, Lu W, Shen W-B (2012) Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation. J Plant Growth Regul 31:519–528

    CAS  Google Scholar 

  • Liu J, Zhang H, Zhang Y, Chai T (2013) Silicon attenuates cadmium toxicity in Solanum nigrum L. by reducing cadmium uptake and oxidative stress. Plant Physiol Biochem 68:1–7

    CAS  PubMed  Google Scholar 

  • Liu X, Chen J, Wang GH, Wang WH, Shen ZJ, Luo MR, Gao GF, Simon M, Ghoto K, Zheng HL (2015a) Hydrogen sulfide alleviates zinc toxicity by reducing zinc uptake and regulating genes expression of antioxidative enzymes and metallothioneins in roots of the cadmium/zinc hyperaccumulator Solanum nigrum L. Plant Soil 400:177–192

    Google Scholar 

  • Liu Z-Q, Pei Y-X, Fang H-H, B-H TIAN (2015b) H2S regulates foxtail millet responsing to stress by protein S-sulfhydration. Chin J Biochem Mol Biol 31:1085–1091

    CAS  Google Scholar 

  • Lv W, Yang L, Xu C, Shi Z, Shao J, Xian M, Chen J (2017) Cadmium disrupts the balance between hydrogen peroxide and superoxide radical by regulating endogenous hydrogen sulfide in the root tip of Brassica rapa. Front Plant Sci 8:232

    PubMed  PubMed Central  Google Scholar 

  • Mathai JC, Andreas M, Philipp K, Saparov SM, Zeidel ML, Lee JK, Peter P (2009) No facilitator required for membrane transport of hydrogen sulfide. Proc Natl Acad Sci U S A 106:16633–16638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5

    PubMed  Google Scholar 

  • Mostofa MG, Rahman A, Ansary MMU, Watanabe A, Fujita M, Tran LSP (2014) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078

    Google Scholar 

  • Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, Snyder SH (2009) H2S signals through protein S-sulfhydration. Sci Signal 2:ra72

    PubMed  PubMed Central  Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    CAS  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants - from the field to the test tube and back. Plant Biol 9:582–588

    CAS  PubMed  Google Scholar 

  • Paul BD, Snyder SH (2012) H?S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13:499–507

  • Peng R, Bian Z, Zhou L, Cheng W, Hai N, Yang C, Yang T, Wang X, Wang C (2016) Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.). Plant Cell Rep 35:2325–2340

    CAS  PubMed  Google Scholar 

  • Piscopo M, Ricciardiello M, Palumbo G, Troisi J (2016) Selectivity of metal bioaccumulation and its relationship with glutathione S -transferase levels in gonadal and gill tissues of Mytilus galloprovincialis exposed to Ni (II), Cu (II) and Cd (II). Rendiconti Lincei 27:1–12

    Google Scholar 

  • Poonam RK, Shagun B, Ravinder S, Pati PK, Renu B (2014) Treatment of 24-EBL to Brassica juncea plants under Cu-metal stress lowers oxidative burst by activity of Antioxidative enzymes. J Stress Physiol Biochem 10:315–327

    Google Scholar 

  • Potters G, Pasternak TPG, Yves JMAK (2010) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32:158–169

    Google Scholar 

  • Qian P, Sun R, Ali B, Gill RA, Xu L, Zhou W (2014) Effects of hydrogen sulfide on growth, antioxidative capacity, and ultrastructural changes in oilseed rape seedlings under aluminum toxicity. J Plant Growth Regul 33:526–538

    CAS  Google Scholar 

  • Qiao Z, Jing T, Liu Z, Zhang L, Jin Z, Liu D, Pei Y (2015) H 2 S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant Soil 393:137–146

    CAS  Google Scholar 

  • Qiao Z, Jing T, Jin Z, Liang Y, Zhang L, Liu Z, Liu D, Pei Y (2016) CDPKs enhance Cd tolerance through intensifying H 2 S signal in Arabidopsis thaliana. Plant Soil 398:99–110

    CAS  Google Scholar 

  • Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272:1291–1304

    CAS  PubMed  Google Scholar 

  • Rizwan M, Mostofa MG, Ahmad MZ, Zhou Y, Adeel M, Mehmood S, Ahmad MA, Javed R, Imtiaz M, Aziz O (2019) Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel. Plant Physiol Biochem 138:100–111

    CAS  PubMed  Google Scholar 

  • Rodríguez-Ruiz M, Aparicio-Chacón MV, Palma JM, Corpas FJ (2019) Arsenate disrupts ion balance, sulfur and nitric oxide metabolisms in roots and leaves of pea (Pisum sativum L.) plants. Environ Exp Bot 161:143–156

    Google Scholar 

  • Rose P, Dymock BW, Moore PK (2015) GYY4137, a novel water-soluble, H2S-releasing molecule. Methods in enzymology. Elsevier

  • Rui W (2010) Hydrogen sulfide: the third gasotransmitter in biology and medicine. Antioxid Redox Signal 12:1061–1064

    Google Scholar 

  • Ruíz-Torres C, Feriche-Linares R, Rodríguez-Ruíz M, Palma JM, Corpas FJ (2017) Arsenic-induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH-generating systems in roots. J Plant Physiol 211:27–35

    PubMed  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    PubMed  Google Scholar 

  • Seth CS, Remans T, Keunen E, Jozefczak M, Gielen H, Opdenakker K, Weyens N, Vangronsveld J, Cuypers A (2012) Phytoextraction of toxic metals: a central role for glutathione. Plant Cell Environ 35:334–346

    CAS  PubMed  Google Scholar 

  • Shaban M, Abukhadra MR, Rabia M, Elkader YA, Mai EH (2018) Investigation the adsorption properties of graphene oxide and polyaniline nano/micro structures for efficient removal of toxic Cr(VI) contaminants from aqueous solutions; kinetic and equilibrium studies. Rend Lincei-Sci Fis Nat 29:1–14

  • Shahid A, Ahmad N, Anis M, Alatar AA, Faisal M (2015) Morphogenic responses of Rauvolfia tetraphylla L. cultures to Cu, Zn and Cd ions. Rendiconti Lincei 27:369–374

    Google Scholar 

  • Shahzad B, Tanveer M, Che Z, Rehman A, Cheema SA, Sharma A, Song H, Rehman SU, Dong Z (2018) Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotoxicol Environ Saf 147:935–944

    CAS  PubMed  Google Scholar 

  • Shan CJ, Dai HP, Sun YF (2012) Hydrogen sulfide protects wheat seedlings against copper stress by regulating the ascorbate and glutathione metabolism in leaves. Aust J Crop Sci 6

  • Sharma J, Chakraverty N (2013) Mechanism of plant tolerance in response to heavy metals

  • Shen J, Xing T, Yuan H, Liu Z, Jin Z, Zhang L, Pei Y (2013) Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS One 8:e77047

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107

    CAS  PubMed  Google Scholar 

  • Singh VP, Singh S, Kumar J, Prasad SM (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181:20–29

    CAS  PubMed  Google Scholar 

  • Sohail M, Khan MN, Chaudhry AS, Qureshi NA (2016) Bioaccumulation of heavy metals and analysis of mineral element alongside proximate composition in foot, gills and mantle of freshwater mussels ( Anodonta anatina ). Rendiconti Lincei 27:1–10

    Google Scholar 

  • Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    CAS  PubMed  Google Scholar 

  • Tian B, Qiao Z, Zhang L, Li H, Pei Y (2016) Hydrogen sulfide and proline cooperate to alleviate cadmium stress in foxtail millet seedlings. Plant Physiol Biochemi 109:293–299

    CAS  Google Scholar 

  • Tian B, Zhang Y, Jin Z, Liu Z, Pei Y (2017) Role of hydrogen sulfide in the methyl jasmonate response to cadmium stress in foxtail millet. Front Biosci 22:530–538

    CAS  Google Scholar 

  • Tognetti VB, Mühlenbock P, Van BF (2012) Stress homeostasis - the redox and auxin perspective. Plant Cell Environ 35:321–333

    CAS  PubMed  Google Scholar 

  • Uexküll HRV, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Google Scholar 

  • Valivand M, Amooaghaie R, Ahadi A (2019) Seed priming with H2S and Ca2+ trigger signal memory that induces cross-adaptation against nickel stress in zucchini seedlings. Plant Physiol Biochem 143:286–298

    CAS  PubMed  Google Scholar 

  • Verstraeten SV, Aimo L, Oteiza PI (2008) Aluminium and lead: molecular mechanisms of brain toxicity. Arch Toxicol 82:789–802

    CAS  PubMed  Google Scholar 

  • Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896

    CAS  PubMed  Google Scholar 

  • Wang H, Ji F, Zhang Y, Hou J, Liu W, Huang J, Liang W (2019) Interactions between hydrogen sulphide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminium toxicity. Plant Cell Environ 42:2340–2356. https://doi.org/10.1111/pce.13555

    Article  CAS  PubMed  Google Scholar 

  • Xie Y, Zhang C, Lai D, Sun Y, Samma MK, Zhang J, Shen W (2014) Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J Plant Physiol 171:53–62

    CAS  PubMed  Google Scholar 

  • Yadav S (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    CAS  Google Scholar 

  • Yadav P, Kaur R, Kanwar MK, Sharma A, Verma V, Sirhindi G, Bhardwaj R (2017) Castasterone confers copper stress tolerance by regulating antioxidant enzyme responses, antioxidants, and amino acid balance in B. juncea seedlings. Ecotoxicol Environ Saf 147:725

    PubMed  Google Scholar 

  • Zanganeh R, Jamei R, Rahmani F (2019) Role of salicylic acid and hydrogen sulfide in promoting lead stress tolerance and regulating free amino acid composition in Zea mays L. Acta Physiol Plant 41:94–99. https://doi.org/10.1007/s11738-019-2892-z

    Article  CAS  Google 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. J Integr Plant Biol 50:1518–1529

    CAS  PubMed  Google Scholar 

  • Zhang H, Hu LY, Li P, Hu KD, Jiang CX, Luo JP (2010) Hydrogen sulfide alleviated chromium toxicity in wheat. Biol Plant 54:743–747

    CAS  Google Scholar 

  • Zhang L, Pei Y, Wang H, Jin Z, Liu Z, Qiao Z, Fang H, Zhang Y (2015) Hydrogen sulfide alleviates cadmium-induced cell death through restraining ROS accumulation in roots of Brassica rapa L. ssp. pekinensis. Oxid Med Cell Longev 2015:1–11

    Google Scholar 

  • Zhao X, Sobecky PA, Zhao L, Crawford P, Li M (2016) Chromium(VI) transport and fate in unsaturated zone and aquifer: 3D sandbox results. J Hazard Mater 306:203–209

    CAS  PubMed  Google Scholar 

  • Zhi-Qiang L, Yan-Xi P, Hui-Hui F, Bao-Hua T (2015) H2S Regulates foxtail millet responsing to stress by protein S-sulfhydration. Chin J Biochem Mol Biol 31: 1085-1091

  • Zhu CQ, Zhang JH, Sun LM, Zhu LF, Abliz B, Hu WJ, Zhong C, Bai ZG, Sajid H, Cao XC (2018) Hydrogen sulfide alleviates aluminum toxicity via decreasing Apoplast and Symplast Al contents in rice. Front Plant Sci 9:294

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National key research and development projects (2018YFD0201205), the National Natural Science Foundation of China (No. 31660584), China Agriculture Research System (CARS-23-C-07), Gansu Province Science and Technology Key Project Fund (No.17ZD2NA015) and Natural Science Foundation of Gansu References Province, China (1610RJZA098). No potential conflict of interest was reported by the authors.

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Luo, S., Calderón-Urrea, A., YU, J. et al. The role of hydrogen sulfide in plant alleviates heavy metal stress. Plant Soil 449, 1–10 (2020). https://doi.org/10.1007/s11104-020-04471-x

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