SpringerLink
Log in

Exogenous hydrogen sulfide alleviates salt stress by improving antioxidant defenses and the salt overly sensitive pathway in wheat seedlings

  • Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Hydrogen sulfide (H2S) has the ability to strengthen plant stress tolerance; however, the effects of H2S on wheat seedlings under salt stress and the underlying molecular mechanism are still unclear. This study examined the effects of exogenous NaHS as H2S donor on photosynthesis, antioxidant system, and the expression profile of genes related to antioxidant defense responses, the salt overly sensitive (SOS) and mitogen-activated protein kinase (MAPK) pathways in wheat seedlings treated with NaCl stress. H2S application improved photosynthesis, and decreased H2O2 and malondialdehyde (MDA) contents in wheat seedling leaves under NaCl stress. In addition, antioxidant enzyme activity and the content of ascorbic acid and reduced glutathione increased with H2S application. Moreover, H2S pretreatment up-regulated expression levels of genes related to antioxidant system, SOS pathway and MAPK pathway as well as the transcription factor dehydration-responsive element binding gene. Overall, these findings suggest that H2S alleviates salt stress in wheat seedlings not only by strengthening antioxidant defense systems, but by coordinating signal transduction pathways related to the stress response at a transcriptional level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig.2
Fig.3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plant. Plant Cell Rep 25:1263–1274

    Article  CAS  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1334–1337

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  Google Scholar 

  • Buwalda F, Kok LJD, Srulen I, Kuiper PJC (1988) Cysteine, γ-glutamyl-cysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. Physiol Plantarum 74:663–668

    Article  CAS  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530

    Article  CAS  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulfide enhance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516

    Article  CAS  Google Scholar 

  • Christou A, Manganaris G, 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  CAS  Google Scholar 

  • Christou A, Filippou P, Manganaris G, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14:42

    Article  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

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Ding HN, Han QX, Ma DY, Hou JF, Huang X, Wang CY, **e YX, Kang GZ, Guo TC (2018) Characterizing physiological and proteomic analysis of the action of H2S to mitigate drought stress in young seedling of wheat. Plant Mol Biol Rep 36:45–57

    Article  CAS  Google Scholar 

  • Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8(4):e62048

    Article  CAS  Google Scholar 

  • Du X, ** Z, Liu D, Yang G, Pei Y (2017) Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana. Plant Physiol Bioch 120:112–119

    Article  CAS  Google Scholar 

  • Duan BB, Ma YH, Jiang MR, Yang F, Ni L, Lu W (2015) Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul 75:33–34

    Article  CAS  Google Scholar 

  • Foyer C, Rowell J, Walker D (1983) Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239–244

    Article  CAS  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  CAS  Google Scholar 

  • Hancock JT (2017) Harnessing evolutionary toxins for signaling: reactive oxygen species, nitric oxide and hydrogen sulfide in plant cell regulation. Front Plant Sci 8:189

    Article  Google Scholar 

  • Hao L, Wen YL, Zhao YY, Lu WJ, **ao K (2015) Wheat mitogen-activated protein kinase gene TaMPK4 improves plant tolerance to multiple stresses through modifying root growth, ROS metabolism, and nutrient acquisition. Plant Cell Rep 34:2081–2097

    Article  CAS  Google Scholar 

  • ** ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Bioph Res Co 414:481–486

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc T 11:591–592

    Article  CAS  Google Scholar 

  • Ma DY, Sun DX, Wang CY, Qin HX, Ding HN, Li YG, Guo TC (2015) Silicon application alleviates drought stress in wheat through transcriptional regulation of multiple antioxidant defense pathways. J Plant Growth Regul 35:1–10

    Article  Google Scholar 

  • Ma DY, Ding HN, Wang CY, Qin HX, Han QX, Hou JF, Lu HF, **e YX, Guo TC (2016) Alleviation of drought stress by hydrogen sulfide is partially related to the abscisic acid signaling pathway in wheat. PLoS One 11(9):e0163082

    Article  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Archi Biochem Biophys 444:139–158

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  Google Scholar 

  • Mostofal MG, Saegusa D, Fujita M, Tran LS (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci 6:662–676

    Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665

    Article  CAS  Google Scholar 

  • Qiu SH, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1 a plasma membrane Na+/H+exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441

    Article  CAS  Google Scholar 

  • Qiu SH, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu JK (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279:207–215

    Article  CAS  Google Scholar 

  • Robinson MJ, Cobb MH (1997) Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 9:180–186

    Article  CAS  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  CAS  Google Scholar 

  • Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, Albert A (2005) The structure of the Arabidopsis thaliana SOS3: molecular mechanism of sensing calcium for salt stress response. J Mol Biol 345:1253–1264

    Article  CAS  Google Scholar 

  • Sathee L, Sairam RK, Chinnusamy V, Jha SK (2015) Differential transcript abundance of salt overly sensitive (sos) pathway genes is a determinant of salinity stress tolerance of wheat. Acta Physiol Plant 37:1–10

    Article  Google Scholar 

  • Shan C, Zhang S, Ou X (2018) The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. Protoplasma 21:1–6

    Google Scholar 

  • Smirnoff N (2006) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58

    Article  Google Scholar 

  • Wen YL, Li XJ, Guo CJ, Ma CY, Duan WW, Lu WJ, **ao K (2015) Characterization and expression analysis of mitogen-activated protein kinase cascade genes in wheat subjected to phosphorus and nitrogen deprivation, high salinity, and drought. J Plant Biochem Biot 24:184–196

    Article  Google Scholar 

  • **ong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    Article  CAS  Google Scholar 

  • Zhang J, Kirkham MB (1994) Drought stress induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zheng YH, Jia AJ, Ning TY, Xu JL, Li ZJ, Jiang GM (2008) Potassium nitrate application alleviates sodium chloride stress in winter wheat cultivars differing in salt tolerance. J Plant Physiol 165:1455–1465

    Article  CAS  Google Scholar 

  • Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The study is part of a national science and technology support program of China [grant number BAD26B00] and a research project of educational commission of Henan province [grant number 15A210004].

Author information

Authors and Affiliations

  1. Agronomy College/National Engineering Research Center for Wheat, Henan Agricultural University, Zhengzhou, 450002, China

    Huina Ding, Dongyun Ma, **n Huang, Junfeng Hou, Chenyang Wang, Yingxin **e, Yonghua Wang, Haixia Qin & Tiancai Guo

  2. The Collaborative Innovation Center of Henan Food Crops, Henan Agricultural University, Zhengzhou, 45002, China

    Yingxin **e, Yonghua Wang & Tiancai Guo

  3. The National Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, 450002, China

    Dongyun Ma & Chenyang Wang

Authors
  1. Huina Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dongyun Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. **n Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junfeng Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chenyang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yingxin **e
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yonghua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Haixia Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tiancai Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Dongyun Ma or Tiancai Guo.

Additional information

Communicated by G. Bartosz.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, H., Ma, D., Huang, X. et al. Exogenous hydrogen sulfide alleviates salt stress by improving antioxidant defenses and the salt overly sensitive pathway in wheat seedlings. Acta Physiol Plant 41, 123 (2019). https://doi.org/10.1007/s11738-019-2918-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-019-2918-6

Keywords

Search

Navigation