Skip to main content

Hydrogen Sulfide Participation in the Formation of Wheat Seedlings’ Heat Resistance Under the Action of Hardening Temperature

Abstract

The role of hydrogen sulfide (H2S) as a signaling mediator-gasotransmitter in the thermoresistance of plant cells remains poorly understood. The participation of endogenous hydrogen sulfide in heat resistance formation of wheat seedlings (Triticum aestivum L.) caused by short-term exposure to high temperatures was studied. After a 1-min exposure to a temperature of 42°C in roots of wheat seedlings, a transient increase in hydrogen sulfide with a maximum of 1.5 h after heating was observed. At the same time, 24 h after exposure to high temperature, the H2S content in roots decreased to the level of control. The effect of increasing the content of hydrogen sulfide caused by the action of the hardening temperature did not manifest under the treatment of seedlings with scavenger hypotaurine and the inhibitor of L-cysteine desulfhydrase sodium pyruvate. The hardening heating of seedlings caused a rapid increase in the activity of superoxide dismutase (SOD) in the roots and a gradual increase in the activity of catalase and guaiacol peroxidase. The maximum effect of changing the activity of these antioxidant enzymes was observed 24 h after exposure to the hardening temperature. The treatment of seedlings with hypotaurine and sodium pyruvate before hardening heating eliminated the effect of increasing the activity of catalase and guaiacol peroxidase but hardly affected SOD activity. Damaging heating (45°C, 10 min) of seedlings caused an increase in the content of lipid peroxidation (LPO) products in root cells and the subsequent death of a significant part of the seedlings. The preliminary hardening heating significantly increased the heat resistance, decreasing the LPO intensity and the level of seedling death. At the same time, their treatment with the hydrogen sulfide scavenger hypotaurine and the inhibitor of L-cysteine desulfhydrase sodium pyruvate largely neutralized the development of heat resistance caused by hardening heating. A conclusion was made about the role of hydrogen sulfide as a signaling mediator in the regulation of the antioxidant system and the development of seedlings' heat resistance under the action of a hardening temperature.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

REFERENCES

  1. Aleksandrov, V.Ya. and Kislyuk, I.M., Cell response to heat shock, Physiological aspect, Tsitologiya, 1994, vol. 36, no. 1, pp. 5–59.

    Google Scholar 

  2. Ali, S., Anjum, M.A., Nawaz, A., Naz, S., Sardar, H., and Hasa, M.U., Hydrogen sulfide regulates temperature stress in plants, in Hydrogen Sulfide in Plant Biology, Singh, S., Singh, V.P., and Tripathi, D.K., Eds., Elsevier, 2021, pp. 1–24. https://doi.org/10.1016/B978-0-323-85862-5.00003-8

    Book  Google Scholar 

  3. Aroca, A., Benito, J.M., Gotor, C., and Romero, L.C., Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis, J. Exp. Bot., 2017, vol. 68, no. 17, pp. 4915–4927. https://doi.org/10.1093/jxb/erx294

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Aroca, A., Gotor, C., Bassham, D.C., and Romero, L.C., Hydrogen sulfide: from a toxic molecule to a key molecule of cell life, Antioxidant, 2020, vol. 9, no. 7, art. ID 621. https://doi.org/10.1016/S0168-9452(02)00159-010.3390/antiox9070621

    CAS  Article  Google Scholar 

  5. Aroca, A., Zhang, J., Xie, Y., Romero, L.C. and Gotor, C., Hydrogen sulfide signaling in plant adaptations to adverse conditions: molecular mechanisms, J. Exp. Bot., 2021, vol. 72, no. 16, pp. 5893–5904. https://doi.org/10.1093/jxb/erab239

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Bhuyan, M.H.M.B., Hasanuzzaman, M., Parvin, K., Mohsin, S.M., Mahmud, J.A., Nahar, K., and Fujita, M., Nitric oxide and hydrogen sulfide: two intimate collaborators regulating plant defense against abiotic stress, Plant Growth Regul., 2020, vol. 90, pp. 409–424. https://doi.org/10.1007/s10725-020-00594-4

    CAS  Article  Google Scholar 

  7. Chen, X., Chen, Q., Zhang, X., Li, R., Jia, Y., Ef, A.A., Jia, A., Hu, L., and Hu, X., Hydrogen sulfide mediates nicotine biosynthesis in tobacco (Nicotiana tabacum) under high temperature conditions, Plant Physiol. Biochem., 2016, vol. 104, pp. 174–179.https://doi.org/10.1016/j.plaphy.2016.02.033

  8. Christou, A., Filippou, P., Manganaris, G., and Fotopoulos, V., Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin, BMC Plant Biol., 2014, vol. 14, art. ID 42. https://doi.org/10.1186/1471-2229-14-42

    Article  PubMed  PubMed Central  Google Scholar 

  9. Corpas, F.J., Barroso, J.B., González-Gordo, S., Muñoz-Vargas, M.A., and Palma, J.M., Hydrogen sulfide: A novel component in Arabidopsis peroxisomes which triggers catalase inhibition, J. Integr. Plant Biol., 2019, vol. 61, pp. 871–883. https://doi.org/10.1111/jipb.12779

    CAS  Article  PubMed  Google Scholar 

  10. Corpas, F.J. and Palma, J.M., H2S signaling in plants and applications in agriculture, J. Adv. Res., 2020, vol. 24, pp. 131–137. https://doi.org/10.1016/j.jare.2020.03.011

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Cuevasanata, E., Lange, M., Bonanata, J., Coitino, E.L., Ferrer-Sueta, G., Filipovic, M.R., and Alvarez, B., Reaction of hydrogen sulphide with disulfide and sulfenic acid to form the strongly nucleophilic persulfide, J. Biol. Chem., 2015, vol. 290, no. 45, pp. 26866–26880. https://doi.org/10.1074/jbc.M115.672816

    CAS  Article  Google Scholar 

  12. Dar, O.I., Singh, K., Aslam, J., Sharma, S., Kaur, A., Bhardwaj, R., and Sharma, A., Regulation of salinity stress by hydrogen sulfide in plants, in Hydrogen Sulfide in Plant Biology, Singh, S., Singh, V.P., Tripathi, D.K., Eds., Elsevier, 2021, pp. 213–227. https://doi.org/10.1016/B978-0-323-85862-5.00001-4

    Book  Google Scholar 

  13. Fazlieva, E.R., Kiseleva, I.S., and Zhuikova, T.V., Antioxidant activity in the leaves of Melilotus albus and Trifolium medium from man-made disturbed habitats in the Middle Urals under the influence of copper, Russ. J. Plant Physiol., 2012, vol. 59, no. 3, pp. 333–338. https://doi.org/10.1134/S1021443712030065

    CAS  Article  Google Scholar 

  14. Filipovic, M.R., Zivanovic, J., Alvarez, B., and Banerjee, R., Chemical biology of H2S signaling through persulfidation, Chem. Rev., 2018, vol. 118, no. 3, pp. 1253–1337. https://doi.org/10.1021/acs.chemrev.7b00205

    CAS  Article  PubMed  Google Scholar 

  15. Gruhlke, M.C., Reactive sulfur species. A new player in plant physiology?, in Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms, Hasanuzzaman, M., Fotopoulos, V., Nahar, K., and Fujita, M., Eds., John Wiley & Sons, 2019, vol. 2, pp. 715– 728. https://doi.org/10.1002/9781119468677.ch31

    Book  Google Scholar 

  16. Hancock, J.T. and Neill, S.J., Nitric oxide: its generation and interactions with other reactive signaling compounds, Plants, 2019, vol. 8, art. ID 41. https://doi.org/10.3390/plants8020041

    CAS  Article  PubMed Central  Google Scholar 

  17. He, H. and He, L., The role of carbon monoxide signaling in the responses of plants to abiotic stresses, Nitric Oxide, 2014, vol. 42, pp. 40–43. https://doi.org/10.1016/j.niox.2014.08.011

    CAS  Article  PubMed  Google Scholar 

  18. Iqbal, N., Fatma, M., Gautam, H., Umar, S., Sofo, A., D’ippolito, I., and Khan, N.A., The crosstalk of melatonin and hydrogen sulfide determines photosynthetic performance by regulation of carbohydrate metabolism in wheat under heat stress, Plants, 2021, vol. 10, no. 9, art. ID 1778. https://doi.org/10.3390/plants10091778

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Karpets, Yu.V., Kolupaev, Yu.E., and Shkliarevskyi, M.A., Functional interaction of hydrogen sulfide with nitric oxide, calcium, and reactive oxygen species under abiotic stress in plants, in Hydrogen Sulfide and Plant Acclimation to Abiotic Stresses. Plant in Challenging Environments, Khan, M.N., Siddiqui, M.H., Alamri, S., and Corpas, F.J., Eds., Cham: Springer-Verlag, 2021, vol. 1, pp. 31–57. https://doi.org/10.1007/978-3-030-73678-1_3

    Book  Google Scholar 

  20. Karpets, Yu.V., Kolupaev, Yu.E., Yastreb, T.O., and Oboznyi, A.I., Effects of NO-status modification, heat hardening, and hydrogen peroxide on the activity of antioxidant enzymes in wheat seedlings, Russ. J. Plant Physiol., 2015, vol. 62, no. 3, pp. 292–298. https://doi.org/10.1134/S1021443715030097

    CAS  Article  Google Scholar 

  21. Karpets, Yu.V., Shkliarevskyi, M.A., Horielova, E.I., and Kolupaev, Yu.E., Participation of hydrogen sulfide in induction of antioxidant system in roots of wheat plantlets and their heat resistance by salicylic acid, Appl. Biochem. Microbiol., 2020, vol. 56, no. 4, pp. 467–472. https://doi.org/10.1134/S0003683820040079

    CAS  Article  Google Scholar 

  22. Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., and Lugo-vaya, A.A., The participation of calcium ions and reactive oxygen species in the induction of antioxidant enzymes and heat resistance in plant cells by hydrogen sulfide donor, Appl. Biochem. Microbiol., 2017a, vol. 53, no. 5, pp. 573–579. https://doi.org/10.1134/S0003683817050088

    CAS  Article  Google Scholar 

  23. Kolupaev, Yu.E., Firsova, E.N., and Yastreb, Ò.Î., Induction of plant cells heat resistance by hydrogen sulfide donor is mediated by H2O2 generation with participation of NADPH oxidase and superoxide dismutase, Ukr. Biochem. J., 2017b, vol. 89, no. 4, pp. 34–42. https://doi.org/10.15407/ubj89.04.034

    CAS  Article  Google Scholar 

  24. Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., Ryabchun, N.I., and Kirichenko, V.V., Effect of hydrogen sulfide donor on antioxidant state of wheat plants and their resistance to soil drought, Russ. J. Plant Physiol., 2019a, vol. 66, no. 1, pp. 59–66. https://doi.org/10.1134/S1021443719010084

    CAS  Article  Google Scholar 

  25. Kolupaev, Yu.E., Karpets, Yu.V., Beschasniy, S.P., and Dmitriev, A.P., Gasotransmitters and their role in adaptive reactions of plant cells, Cytol. Genet., 2019b, vol. 53, no. 5, pp. 392–406. https://doi.org/10.3103/S0095452719050098

    Article  Google Scholar 

  26. Kolupaev, Y.E., Oboznyi, A.I., and Shvidenko, N.V., Role of hydrogen peroxide in generation of a signal inducing heat tolerance of wheat seedlings, Russ. J. Plant Physiol., 2013, vol. 60, no. 2, pp. 227–234. https://doi.org/10.1134/S102144371302012X

    CAS  Article  Google Scholar 

  27. Krasylenko, Y.A., Yemets, A.I., and Blume, Y.B., Functional role of nitric oxide in plants, Russ. J. Plant Physiol., 2010, vol. 57, no. 4, pp. 451–461. https://doi.org/10.1134/S1021443710040011

    CAS  Article  Google Scholar 

  28. Li, B., Gao, K., Ren, H., and Tang, W., Molecular mechanisms governing plant responses to high temperatures, J. Integr. Plant Biol., 2018, vol. 60, pp. 757–779. https://doi.org/10.1111/jipb.12701

    Article  PubMed  Google Scholar 

  29. Li, H., Li, M., Wei, X., Zhang, X., Xue, R., Zhao, Y., and Zhao, H., Transcriptome analysis of drought-responsive genes regulated by hydrogen sulfide in wheat (Triticum aestivum L.) leaves, Mol. Genet. Genom., 2017, vol. 292, no. 5, pp. 1091–1110. https://doi.org/10.1007/s00438-017-1330-4

    CAS  Article  Google Scholar 

  30. Li, Z.G., Gong, M., and Liu, P., Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas, Acta Physiol. Plant., 2012, vol. 34, no. 6, pp. 2207–2213. https://doi.org/10.1007/s11738-012-1021-z

    CAS  Article  Google Scholar 

  31. Li, Z.G., Yang, S.Z., Long, W.B., Yang, G.X., and Shen, Z.Z., Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings, Plant, Cell Environ., 2013, vol. 36, no. 8, pp. 1564–1572. https://doi.org/10.1111/pce.12092

    CAS  Article  Google Scholar 

  32. Li, Z.G., Luo, L.J., and Zhu, L.P., Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings, Bot. Stud., 2014, vol. 55, art. ID 20. https://doi.org/10.1186/1999-3110-55-20

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Li, Z.G., Long, W.B., Yang, S.Z., Wang, Y.C., Tang, J.H., and Chen, T., 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, 2015, vol. 51, pp. 428–437. https://doi.org/10.1007/s11627-015-9705-x

    CAS  Article  Google Scholar 

  34. Liu, H., Wang, J., Liu, J., Liu, T., and Xue, S., Hydrogen sulfide (H2S) signaling in plant development and stress responses, aBIOTECH, 2021, vol. 2, pp. 32–63. https://doi.org/10.1007/s42994-021-00035-4

  35. Shi, H., Ye, T., and Chan, Z., Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.), Plant Physiol. Biochem., 2013, vol. 71, pp. 226–234. https://doi.org/10.1016/j.plaphy.2013.07.021

    CAS  Article  PubMed  Google Scholar 

  36. Shi, H., Ye, T., Han, N., Bian, H., Liu, X., and Chan, Z., Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis, J. Integr. Plant Biol., 2015, vol. 57, no. 7, pp. 628–640. https://doi.org/10.1111/jipb.12302

    CAS  Article  PubMed  Google Scholar 

  37. Shivaraj, S.M., Vats, S., Bhat, J.A., Dhakte, P., Goyal, V., Khatri, P., Kumawat, S., Singh, A., Prasad, M., Sonah, H., Sharma, T.R., and Deshmukh, R., Nitric oxide and hydrogen sulfide crosstalk during heavy metal stress in plants, Physiol. Plant., 2020, vol. 168, no. 2, pp. 437–455. https://doi.org/10.1111/ppl.13028

    CAS  Article  PubMed  Google Scholar 

  38. Singh, A. and Roychoudhury, A., Hydrogen sulfide and redox homeostasis for alleviation of heavy metal stress, in Hydrogen Sulfide and Plant Acclimation to Abiotic Stresses, Plant in Challenging Environments, Khan, M.N., Siddiqui, M.H., Alamri, S., Corpas, F.J., Eds., Cham: Springer-Verlag, 2021, vol. 1, pp. 59–72. https://doi.org/10.1007/978-3-030-73678-1_4

    Book  Google Scholar 

  39. Singh, S., Kumar, V., Kapoor, D., Kumar, S., Singh, S., Dhanjal, D.S., Datta, S., Samuel, J., Dey, P., Wang, S., Prasad, R., and Singh, J., Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions, Physiol. Plant., 2020, vol. 168, no. 2, pp. 301–317. https://doi.org/10.1111/ppl.13002

    CAS  Article  PubMed  Google Scholar 

  40. Singhal, R.K., Jatav, H.S., Aftab, T., Pandey, S., Mishra, U.N., Chauhan, J., Chand, S., Indu Saha, D., Dadarwal, B.K., Chandra, K., Khan, M.A., Rajput, V.D., Minkina, T., Narayana, E.S., Sharma, M.K., and Ahmed, S., Roles of nitric oxide in conferring multiple abiotic stress tolerance in plants and crosstalk with other plant growth regulators, Plant Growth. Regul., 2021. https://doi.org/10.1007/s00344-021-10446-8

  41. Wang, M. and Liao, W., Carbon monoxide as a signaling molecule in plants, Front. Plant Sci., 2016, vol. 7, art. ID 572. https://doi.org/10.3389/fpls.2016.00572

    Article  PubMed  PubMed Central  Google Scholar 

  42. Yao, Y., Yang, Y., Li, C., Huang, D., Zhang, J., Wang, C., Li, W., Wang, N., Deng, Y., and Liao, W., Research progress on the functions of gasotransmitters in plant responses to abiotic stresses, Plants, 2019, vol. 8, no. 12, art. ID 605. https://doi.org/10.3390/plants8120605

    CAS  Article  PubMed Central  Google Scholar 

  43. Ziogas, V., Molassiotis, A., Fotopoulos, V., and Tanou, G., Hydrogen sulfide: A potent tool in postharvest fruit biology and possible mechanism of action, Front. Plant Sci., 2018, vol. 9, art. ID 1375. https://doi.org/10.3389/fpls.2018.01375

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study did not receive any certain grant from financial organs in governmental, commercial, or noncommercial sectors.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to E. N. Havva or A. P. Dmitriev.

Ethics declarations

The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by V. Mittova

About this article

Verify currency and authenticity via CrossMark

Cite this article

Havva, E.N., Kolupaev, Y.E., Shkliarevskyi, M.A. et al. Hydrogen Sulfide Participation in the Formation of Wheat Seedlings’ Heat Resistance Under the Action of Hardening Temperature. Cytol. Genet. 56, 218–225 (2022). https://doi.org/10.3103/S0095452722030045

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452722030045

Keywords:

  • Triticum aestivum L.
  • hydrogen sulfide
  • hardening
  • heat resistance
  • antioxidant system