TSitologiya i Genetika 2022, vol. 56, no. 3, 14-23
Cytology and Genetics 2022, vol. 56, no. 3, 218–225, doi: https://www.doi.org/10.3103/S0095452722030045

Seedlings under the action of hardening temperature

Havva E.N., Kolupaev Yu.E., Shkliarevskyi M.A., Kokorev A.I., Dmitriev A.P.

  1. Dokuchaev Kharkiv National Agrarian University, Kharkiv, Dokuchaevske-2, 62483, Ukraine
  2. Yur’ev Institute of Plant Breeding National Academy of Agrarian Sciences of Ukraine, Moskovskyi Ave., 142, Kharkiv, 61060, Ukraine
  3. Institute of Cell Biology and Genetic Engineering, National Academy of Sciences of Ukraine, st. Akademika Zabolotnogo, 148, Kyiv, 03143 Ukrain

SUMMARY. The role of hydrogen sulfide (H2S) as a signaling me-diator-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 one-minute exposure to a temperature of 42 °C in wheat seedlings roots, 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 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 hardening temperature. Treatment of seedlings with hypotaurine and sodium pyruvate before hardening heating eliminated the effect of increasing the activity of catalase and guaiacol peroxidase, but almost did not affect the activity of SOD. Damaging heating (45 °C, 10 min) of seedlings caused an increase in the content of lipid peroxidation products (LPO) in root cells and the subsequent death of a significant part of 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 L-cysteine desulfhydrase inhibitor 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.

Keywords:

TSitologiya i Genetika
2022, vol. 56, no. 3, 14-23

Current Issue
Cytology and Genetics
2022, vol. 56, no. 3, 218–225,
doi: 10.3103/S0095452722030045

Full text and supplemented materials

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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