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Involvement of sulfhydryl compounds and antioxidant enzymes in H2S-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension-cultured cells

  • Plant Physiology
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Abstract

Hydrogen sulfide (H2S) is a multifunctional second messenger involved in plant growth, development, and acquisition of stress tolerance, including heat tolerance, but the mechanism of H2S-induced heat tolerance in tobacco suspension-cultured cells is not completely clear. This study investigated the effects of pretreatment with the H2S donor sodium hydrosulfide (NaHS) and its precursors cysteine and potassium bisulfite (KHSO3) on the heat tolerance of tobacco suspension-cultured cells and the involvement of sulfhydryl compounds and antioxidant enzymes in conferring heat tolerance. Pretreatment with NaHS, cysteine, and KHSO3 significantly increased the survival percentage of tobacco suspension-cultured cells under heat stress, while treatment with the H2S scavenger hypotaurine in combination with NaHS eliminated heat tolerance induced by treatment with NaHS alone. In addition, NaHS treatment increased the levels of water-soluble sulfhydryl compounds such as H2S, total sulfhydryl compounds, total sulfhydryl proteins, cysteine, and glutathione (GSH) as well as the activities of antioxidant enzymes superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidase (GPX), and glutathione reductase (GR) under normal culture conditions (26°C). Under heat stress at 43°C, the levels of water-soluble sulfhydryl compounds and the activities of antioxidant enzymes all dropped, but the cells treated with NaHS sustained significantly higher levels of water-soluble sulfhydryl compounds and activities of antioxidant enzymes than the control. These results suggest that the pretreatment with NaHS could improve the heat tolerance of tobacco suspension-cultured cells and that the acquisition of this heat tolerance is caused by the elevated levels of water-soluble sulfhydryl compounds and elevated activities of antioxidant enzymes induced by NaHS.

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References

  • Bloem E, Rubekin K, Haneklaus S, Banfalvi Z, Hesse H, Schnug E (2011) H2S and COS gas exchange of transgenic potato lines with modified expression levels of enzymes involved in sulphur metabolism. J Agron Crop Sci 197:311–321

    Article  CAS  Google Scholar 

  • Chen J, Wang WH, Wu FH, You CY, Liu WT, Dong XK, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    Article  CAS  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Kok LJ, Bosma W, Maas FM, Kuiper PJC (1985) The effect of short-term H2S fumigation on water-soluble sulphydryl and glutathione levels in spinach. Plant Cell Environ 8:189–194

    Article  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fu PN, Wang WJ, Hou LX, Liu X (2013) Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc Bot Pol 82:295–302

    Article  CAS  Google Scholar 

  • Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627–633

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grant OM, Brennan DP, Salas CDM, Dix PJ (2014) Impact of enhanced capacity to scavenger reactive oxygen species on cold tolerance of tobacco. Int J Plant Sci 175:544–554

    Article  CAS  Google Scholar 

  • Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol Biochem 78:37–42

    Article  CAS  PubMed  Google Scholar 

  • Jaleel CA, Riadhm K, Gopi R, Manivannan P, Ines J, Al-Juburi HJ, Zhao CX, Shao HB, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  Google Scholar 

  • Jin ZP, Xue SW, Luo YN, Fang BH, Tian HH, Li H, Pei YX (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:628–695

    Article  Google Scholar 

  • Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187

    Article  CAS  PubMed  Google Scholar 

  • Li ZG (2013) Hydrogen sulfide: a multifunctional gaseous molecule in plants. Russ J Plant Physiol 6:733–740

    Article  Google Scholar 

  • Li ZG (2015a) Analysis of some enzymes activities of hydrogen sulfide metabolism in plants. Methods Enzymol 555:253–269

    Article  PubMed  Google Scholar 

  • Li ZG (2015b) Quantification of hydrogen sulfide concentration using methylene blue and 5,5′-dithiobis(2-nitrobenzoic acid) methods in plants. Methods Enzymol 554:101–110

    Article  PubMed  Google Scholar 

  • Li ZG, Gong M, Liu P (2012a) Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas. Acta Physiol Plant 34:2207–2213

    Article  CAS  Google Scholar 

  • Li ZG, 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(186):185–189

    Article  PubMed  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013a) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yuan LX, Wang QL, Ding ZL, Dong CY (2013b) Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:2127–2136

    Article  CAS  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T, Cival 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 Physiol Biochem 48:931–935

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607–1616

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Hou L, Liu G, Liu X, Wang X (2011) Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull 56:3547–3553

    Article  CAS  Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–479

    Article  CAS  Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509

    Article  CAS  PubMed  Google Scholar 

  • Riemenschneider A, Nikiforova V, Hoefgen R, DeKok LJ, Papenbrock J (2005) Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473–483

    Article  CAS  PubMed  Google Scholar 

  • Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 190:556–565

    Article  CAS  PubMed  Google Scholar 

  • Scheibe R, Dietz KJ (2012) Reduction–oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant Cell Environ 35:202–216

    Article  CAS  PubMed  Google Scholar 

  • Shan CJ, Zhang SL, Li DF, Zhao YZ, Tian XL, Zhao XL, Wu YX, Wei XY, Liu RQ (2011) Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol Plant 33:2533–2540

    Article  CAS  Google Scholar 

  • Shi H, Ye T, Chan Z (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71:226–234

    Article  CAS  PubMed  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231:1301–1309

    Article  CAS  PubMed  Google Scholar 

  • 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 Soil 351:107–119

    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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zhang H, Hua SL, Zhang ZJ, Hua LY, Jiang CX, Wei ZJ, Liu J, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257

    Article  CAS  Google Scholar 

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Wang MF, Hua LY, Wang SH, Hua KD, Bao LJ, Luo JP (2010b) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol 57:532–539

    Article  CAS  Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31360057). We appreciate the editors and reviewers for their exceptionally helpful comments about the manuscript.

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Authors and Affiliations

  1. School of Life Sciences, Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092, People’s Republic China

    Zhong-Guang Li, Wei-Biao Long, Shi-Zhong Yang, Yang-Cai Wang, Ji-Hong Tang & Tao Chen

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  1. Zhong-Guang Li
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  2. Wei-Biao Long
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  3. Shi-Zhong Yang
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  4. Yang-Cai Wang
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  5. Ji-Hong Tang
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  6. Tao Chen
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Correspondence to Zhong-Guang Li.

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Editor: David Duncan

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Li, ZG., Long, WB., Yang, SZ. et al. Involvement of sulfhydryl compounds and antioxidant enzymes in H2S-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension-cultured cells. In Vitro Cell.Dev.Biol.-Plant 51, 428–437 (2015). https://doi.org/10.1007/s11627-015-9705-x

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