Russian Journal of Plant Physiology

, Volume 66, Issue 4, pp 540–547 | Cite as

Stress-Protective Responses of Wheat and Rye Seedlings Whose Chilling Resistance Was Induced with a Donor of Hydrogen Sulfide

  • Yu. E. KolupaevEmail author
  • E. I. Horielova
  • T. O. Yastreb
  • N. I. Ryabchun
  • V. V. Kirichenko


The effect of sodium hydrosulfide (NaHS) as a donor of hydrogen sulfide on the resistance to subzero temperatures was investigated in the seedlings of winter wheat (Triticum aestivum L.) and rye (Secale cereale L.). Treatment of nonhardened seedlings with NaHS at concentrations of 0.1 and 0.5 mM improved their survival after freezing at –5°С. Exposure to NaHS at the same concentrations also improved the survival of wheat and rye seedlings hardened at 2–4°С after their freezing at –9°С. Under the effect of the hydrogen sulfide donor, the seedlings of both species at normal temperature (20–22°С) and upon cold hardening accumulated more sugars and proline. After sodium hydrosulfide treatment, the content of anthocyanins rose only in wheat seedlings. The donor of hydrogen sulfide also induced a rise in the activity of catalase and guaiacol peroxidase in the seedlings of both species at normal and hardening temperatures, while the activity of superoxide dismutase remained essentially the same. Under the effect of NaHS, both species accumulated less malonic dialdehyde caused by cryogenic stress. The contribution of different components of stress-protective systems to chilling resistance induced by hydrogen sulfide and hardening is discussed in relation to plant species.


Triticum aestivum Secale cereale hydrogen sulfide osmolytes antioxidant enzymes cold hardening chilling resistance 



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


  1. 1.
    Hancock, J.T. and Whiteman, M., Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol. Biochem., 2014, vol. 78, pp. 37–42.CrossRefGoogle Scholar
  2. 2.
    Savvides, A., Ali, S., Tester, M., and Fotopoulos, V., Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci., 2016, vol. 21, pp. 329–340.CrossRefGoogle Scholar
  3. 3.
    Lisjak, M., Teklic, T., Wilson, I.D., Whiteman, M., and Hancock, J.T., Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ., 2013, vol. 36, pp. 1607–1616.CrossRefGoogle Scholar
  4. 4.
    Li, Z.G., Gong, M., Xie, H., Yang, L., and Li, J., Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin, Plant Sci., 2012, vols. 185–186, pp. 185–189.Google Scholar
  5. 5.
    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: 42. CrossRefGoogle Scholar
  6. 6.
    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, pp. 1564–1572.CrossRefGoogle Scholar
  7. 7.
    Kolupaev, Yu.E., Firsova, E.N., Yastreb, T.O., and Lugovaya, 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., 2017, vol. 53, pp. 573–579.CrossRefGoogle Scholar
  8. 8.
    Fu, P.N., Wang, W.J., Hou, L.X., and Liu, X., Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L., Acta Soc. Bot. Pol., 2013, vol. 82, pp. 295–302.CrossRefGoogle Scholar
  9. 9.
    Du, X., Jin, Z., Liu, D., Yang, G., and Pei, Y., Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana, Plant Physiol. Biochem., 2017, vol. 120, pp. 112–119.CrossRefGoogle Scholar
  10. 10.
    Janicka, M., Reda, M., Czyżewska, K., and Kabała, K., Involvement of signalling molecules NO, H2O2 and H2S in modification of plasma membrane proton pump in cucumber roots subjected to salt or low temperature stress, Funct. Plant Biol., 2018, vol. 45, pp. 428–439.CrossRefGoogle Scholar
  11. 11.
    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.CrossRefGoogle Scholar
  12. 12.
    Mizuno, N., Sugie, A., Kobayashi, F., and Takumi, S., Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat, Plant Physiol., 2008, vol. 165, pp. 462–467.CrossRefGoogle Scholar
  13. 13.
    Yoshida, M. and Kawakami, A., Molecular analysis of fructan metabolism associated with freezing tolerance and snow mold resistance of winter wheat, in Plant and Microbe Adaptations to Cold in a Changing World, Imai, R., et al., Eds., New York: Springer Science + Business Media, 2013, pp. 231–243.Google Scholar
  14. 14.
    Naraikina, N.V., Sin’kevich, M.S., Demin, I.N., Selivanov, A.A., Moshkov, I.E., and Trunova, T.I., Changes in the activity of superoxide dismutase isoforms in the course of low-temperature adaptation in potato plants of wild type and transformed with δ12-acyl-lipid desaturase gene, Russ. J. Plant Physiol., 2014, vol. 61, pp. 332–338.CrossRefGoogle Scholar
  15. 15.
    Kolupaev, Yu.E., Ryabchun, N.I., Vayner, A.A., Yastreb, T.O., and Oboznyi, A.I., Antioxidant enzyme activity and osmolyte content in winter cereal seedlings under hardening and cryostress, Russ. J. Plant Physiol., 2015, vol. 62, pp. 499–506.CrossRefGoogle Scholar
  16. 16.
    Kolupaev, Yu.E., Yastreb, T.O., Oboznyi, A.I., Ryabchun, N.I., and Kirichenko, V.V., Constitutive and cold-induced resistance of rye and wheat seedlings to oxidative stress, Russ. J. Plant Physiol., 2016, vol. 63, pp. 326–337.CrossRefGoogle Scholar
  17. 17.
    Bates, L.S., Walden, R.P., and Tear, G.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, pp. 205–210.CrossRefGoogle Scholar
  18. 18.
    Havaux, M. and Kloppstech, K., The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants, Planta, 2001, vol. 213, pp. 953–966.CrossRefGoogle Scholar
  19. 19.
    Bradford, M.M.A., Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.CrossRefGoogle Scholar
  20. 20.
    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., 2019, vol. 66, pp. 59–66.CrossRefGoogle Scholar
  21. 21.
    Lai, D.W., Mao, Y., Zhou, H., Li, F., Wu, M., Zhang, J., He, Z., Cui, W., and Xie, Y., 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., 2014, vol. 225, pp. 117–129.CrossRefGoogle Scholar
  22. 22.
    Sin'kevich, M.S., Deryabin, A.N., and Trunova, T.I., Characteristics of oxidative stress in potato plants with modified carbohydrate metabolism, Russ. J. Plant Physiol., 2009, vol. 56, pp. 168–174.CrossRefGoogle Scholar
  23. 23.
    Burbulis, N., Jonytiene, V., Kupriene, R., and Blinstrubiene, A., Changes in proline and soluble sugars content during cold acclimation of winter rapeseed shoots in vitro, J. Food Agricult. Environ., 2011, vol. 9, pp. 371–374.Google Scholar
  24. 24.
    Yu, L., Zhang, C., Shang, H., Wang, X., Wei, M., Yang, F., and Shi, Q., Exogenous hydrogen sulfide enhanced antioxidant capacity, amylase activities and salt tolerance of cucumber hypocotyls and radicles, J. Integr. Agricult., 2013, vol. 12, pp. 445–456.CrossRefGoogle Scholar
  25. 25.
    Chen, J., Shang, Y.T., Wang, W.H., Chen, X.Y., He, E.M., Zheng, H.L., and Shangguan, Z., Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings, Front. Plant Sci., 2016, vol. 7: 1173. Google Scholar
  26. 26.
    Shevyakova, N.I., Bakulina, E.A., and Kuznetsov, Vl.V., Proline antioxidant role in the common ice plant subjected to salinity and paraquat treatment inducing oxidative stress, Russ. J. Plant Physiol., 2009, vol. 56, pp. 663–669.CrossRefGoogle Scholar
  27. 27.
    Li, Q., Wang, Z., Zhao, Y., Zhang, X., Zhang, S., Bo, L., Wang, Y., Ding, Y., and An, L., Putrescine protects hulless barley from damage due to UV-B stress via H2S- and H2O2-mediated signaling pathways, Plant Cell Rep., 2016, vol. 35, pp. 1155–1168.CrossRefGoogle Scholar
  28. 28.
    Aghdam, M.S., Mahmoudi, R., Razavi, F., Rabiei, V., and Soleimani, A., Hydrogen sulfide treatment confers chilling tolerance in hawthorn fruit during cold storage by triggering endogenous H2S accumulation, enhancing antioxidant enzymes activity and promoting phenols accumulation, Sci. Horticult., 2018, vol. 238, pp. 264–271.CrossRefGoogle Scholar
  29. 29.
    Khlestkina, E.K., The adaptive role of flavonoids: emphasis on cereals, Cereal Res. Commun., 2013, vol. 41, pp. 185–198.CrossRefGoogle Scholar
  30. 30.
    Olenichenko, N.A., Zagoskina, N.V., Astakhova, N.V., Trunova, T.I., and Kuznetsov, Yu.V., Primary and secondary metabolism of winter wheat under cold hardening and treatment with antioxidants, Appl. Biochem. Microbiol., 2008, vol. 44: 535. CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • Yu. E. Kolupaev
    • 1
    Email author
  • E. I. Horielova
    • 1
  • T. O. Yastreb
    • 1
  • N. I. Ryabchun
    • 2
  • V. V. Kirichenko
    • 1
    • 2
  1. 1.Dokuchaev National Agrarian UniversityKharkivUkraine
  2. 2.Yur’ev Institute of Plant Breeding, National Academy of Agrarian SciencesKharkivUkraine

Personalised recommendations