TSitologiya i Genetika 2023, vol. 57, no. 2, 3-14
Cytology and Genetics 2023, vol. 57, no. 2, 117–127, doi: https://www.doi.org/10.3103/S0095452723020068

Induction by melatonin of cell protective reactions of Triticum aestivum and Secale cereale to high temperatures action

Kolupaev Yu.E., Taraban D.A., Karpets Yu.V., Makaova B.E., Ryabchun N.I., Dyachenko A.I., Dmitriev O.P.

  1. Інститут рослинництва ім. В.Я. Юр’єва НААН України, пр­т Героїв Харкова, 142, Харків, 61060, Україна
  2. Полтавський державний аграрний університет, вул. Сковороди, Полтава, 36003, Україна
  3. Державний біотехнологічний університет, вул. Алчевських, 44, Харків, 61022, Україна
  4. Інститут клітинної біології та генетичної інженерії НАН України, вул. Академіка Заболотного, 148, Київ, 03143, Україна

SUMMARY. Currently, melatonin (N-acetyl-5-methoxytryptamine) is considered as a multifunctional bioregulator not only in mammals, but also in plants. The aim of the work was to study the effect of melatonin on the resistance of wheat (Triticum aestivum L., var. Doskonala) and rye (Secale cereale L., var. Pam’yat Khudoyerka) seedlings to high temperatures and the functioning of key cellular defense systems – antioxidant and osmoprotective. Rye seedlings differed from wheat seedlings in higher heat resistance, which was manifested in less inhibition of growth after 6-hour heating at the temperature of 44 °С and in less manifestation of the effects of oxidative stress. Treatment of wheat grains with melatonin at concentrations ranging from 20–100 µM significantly reduced shoot and root growth inhibition caused by high temperature. Rye seedlings were less affected by melatonin, reducing only the inhibition of shoot growth. Treatment with melatonin prevented the development of oxidative stress caused by the effect of high temperature, which was manifested in decrease of the rate of superoxide radical generation, the content of hydrogen peroxide and malondialdehyde in the shoots of wheat and rye seedlings. Treatment of grains of both types of cereals with melatonin caused an increase in catalase activity under the heat stress. Treatment with melatonin also contributed to the stabilization of peroxidase activity in wheat under the stress conditions and caused its increase in rye. In addition, treatment of grains with melatonin caused an increase in the content of soluble carbohydrates under the stress conditions, but did not significantly affect the content of proline in the shoots of seedlings of both species. In general, a less noticeable effect of melatonin treatment on the functioning of protective systems of rye was noted. The key effects of melatonin under the stress conditions are the reduction of oxidative damage to cells, increased activity of antioxidant enzymes, and increased accumulation of soluble carbohydrates.

Keywords:

TSitologiya i Genetika
2023, vol. 57, no. 2, 3-14

Current Issue
Cytology and Genetics
2023, vol. 57, no. 2, 117–127,
doi: 10.3103/S0095452723020068

Full text and supplemented materials

References

Alam, M.N., Zhang, L., Yang, L., et al., Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide, BMC Genomics, 2018, vol. 19, no. 1, p. 224. https://doi.org/10.1186/s12864-018-4588-y

Antoniou, C., Chatzimichail, G., Xenofontos, R., et al., Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism, J. Pineal Res., 2017, vol. 62, no. 4, p. e12401. https://doi.org/10.1111/jpi.12401

Arnao, M.B. and Hernandez-Ruiz, J., Functions of melatonin in plants: a review, J. Pineal Res., 2015, vol. 59, pp. 133–150. https://doi.org/10.1111/jpi.12253

Arnao, M.B. and Hernández-Ruiz, J., Melatonin: A New plant hormone and/or a plant master regulator?, Trends Plant Sci., 2019a, vol. 24, no. 1, pp. 38–48. https://doi.org/10.1016/j.tplants.2018.10.010

Arnao, M. and Hernández-Ruiz, J., Melatonin and reactive oxygen and nitrogen species: a model for the plant redox network, Melatonin Res., 2019b, vol. 2, no. 3, pp. 152–168. https://doi.org/10.32794/11250036

Barrs, H. and Weatherley, P., A re-examination of the relative turgidity technique for estimating water deficits in leaves, Aust. J. Biol. Sci., 1962, vol. 15, no. 3, pp. 413–428.

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. https://doi.org/10.1007/BF00018060

Buttar, Z.A., Wu, S.N., Arnao, M.B., et al., Melatonin suppressed the heat stress-induced damage in wheat seedlings by modulating the antioxidant machinery, Plants (Basel), 2020, vol. 9, no. 7, p. 809. https://doi.org/10.3390/plants9070809

Chang, J., Guo, Y., Li, J., et al., Positive interaction between H2O2 and Ca2+ mediates melatonin-induced CBF pathway and cold tolerance in watermelon (Citrullus lanatus L.), Antioxidants, 2021, vol. 10, p. 1457. https://doi.org/10.3390/antiox10091457

Cui, G., Sun, F., Gao, X., et al., Proteomic analysis of melatonin-mediated osmotic tolerance by improving energy metabolism and autophagy in wheat (Triticum aestivum L.), Planta, 2018, vol. 248, no. 1, pp. 69–87. https://doi.org/10.1007/s00425-018-2881-2

Dubbels, R., Reiter, R.J., Klenke, E., et al., Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry, J. Pineal Res., 1995, vol. 18, pp. 28–31. https://doi.org/10.1111/j.1600-079x.1995.tb00136.x

Fan, J., Xie, Y., Zhang, Z., and Chen, L., Melatonin: A multifunctional factor in plants, Int. J. Mol. Sci., 2018, vol. 19, p. 1528. https://doi.org/10.3390/ijms19051528

Gong, B., Yan, Y., Wen, D., and Shi, Q., Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum, Physiol. Plant., 2017, vol. 160, no. 4, pp. 396–409. https://doi.org/10.1111/ppl.12581

Hardeland, R., Neurobiology, pathophysiology, and treatment of melatonin deficiency and dysfunction, Sci. World J., 2012, vol. 2012, p. 640389. https://doi.org/10.1100/2012/640389

Iqbal, N., Fatma, M., Khan, N.A., and Umar, S., Regulatory role of proline in heat stress tolerance: modulation by salicylic acid, in Plant Signaling Molecules, Khan, M.I.R., Reddy, P.S., Ferrante, A., and Khan, N.A., Eds., Elsevier, 2019, pp. 437–448. https://doi.org/10.1016/B978-0-12-816451-8.00027-7

Iqbal, N., Fatma, M., Gautam, H., et al., The crosstalk of melatonin and hydrogen sulfide determines photosynthetic performance by regulation of carbohydrate metabolism in wheat under heat stress, Plants, 2021, vol. 10, p. 1778. https://doi.org/10.3390/plants10091778

Jahan, M.S., Shu, S., Wang, Y., et al., Melatonin alleviates heat-induced damage of tomato seedlings by balancing redox homeostasis and modulating polyamine and nitric oxide biosynthesis, BMC Plant Biol., 2019, vol. 19, no. 1, p. 414. https://doi.org/10.1186/s12870-019-1992-7

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., Khripach, V.A., and Kolupaev, Yu.E., State of enzymatic antioxidative system and heat resistance of wheat plantlets treated by combination of 24-epibrassinolide and NO donor, Cereal Res. Commun., 2021, vol. 49, no. 2, pp. 207–216. https://doi.org/10.1007/s42976-020-00090-5

Kolupaev, Yu.E., Ryabchun, N.I., Vayner, A.A., et al., Antioxidant enzyme activity and osmolyte content in winter cereal seedlings under hardening and cryostress, Russ. J. Plant Physiol., 2015, vol. 62, no. 4, pp. 499–506. https://doi.org/10.1134/S1021443715030115

Kolupaev, Yu.E., Yastreb, T.O., Oboznyi, A.I., et al., Constitutive and cold-induced resistance of rye and wheat seedlings to oxidative stress, Russ. J. Plant Physiol., 2016, vol. 63, no. 3, pp. 326–337. https://doi.org/10.1134/S1021443716030067

Kolupaev, Yu.E., Makaova, B.E., Ryabchun, N.I., et al., Adaptation of cereal seedlings to oxidative stress induced by hyperthermia, Agriculture and Forestry, 2022, vol. 68, no. 4, pp. 7–18. https://doi.org/10.17707/AgricultForest.68.4.01

Kolupaev, Yu.E., Yastreb, T.O., Ryabchun, N.I., et al., Cellular mechanisms for the formation of plant adaptive responses to high temperatures, Cytol. Genet., 2023, vol. 57, no. 1, pp. 55–75. https://doi.org/10.3103/S0095452723010048

Koster, K.L. and Lynch, D.V., Solute accumulation and compartmentation during the cold acclimation of puma rye, Plant Physiol., 1992, vol. 98, no. 1, pp. 108–113. https://doi.org/10.1104/pp.98.1.108

Lei, K., Sun, S., Zhong, K., et al., Seed soaking with melatonin promotes seed germination under chromium stress via enhancing reserve mobilization and antioxidant metabolism in wheat, Ecotoxicol. Environ. Saf., 2021, vol. 220, p. 112241. https://doi.org/10.1016/j.ecoenv.2021.112241

Meng, J.F., Xu, T.F., Wang, Z.Z., et al., The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology, J. Pineal Res., 2014, vol. 57, no. 2, pp. 200–212. https://doi.org/10.1111/jpi.12159

Nawaz, K., Chaudhary, R., Sarwar, A., et al., Melatonin as master regulator in plant growth, development and stress alleviator for sustainable agricultural production: current status and future perspectives, Sustainability, 2021, vol. 13, p. 294. https://doi.org/10.3390/su13010294

Oboznyi, O.I., Kryvoruchenko, R.V., Shevchenko, M.V., and Kolupaev, Yu.E., Antioxidant activity of winter wheat seedlings of different ecotypes in connection with sustainable hyperthermia and dehydration, Vìsnik Harkìvs’kogo Nacìonal’nogo Agrarnogo Unìversitetu, Serìâ Bìologiâ, 2013, vol. 1, no. 28, pp. 52–59.

Romanenko, O., Kushch, I., Zayets, S., and Solodushko, M., Viability of seeds and sprouts of winter crop varieties under drought conditions of Steppe, Agroecol. J., 2018, vol. 1, pp. 87–95. https://doi.org/10.33730/2077-4893.1.2018.160584

Romanenko, K.O., Babenko, L.M., Smirnov, O.E., and Kosakivska, I.V., Antioxidant protection system and photosynthetic pigment composition in Secale cereale subjected to short-term temperature stresses, Open Agric. J., 2022, vol. 16, p. e187433152206273. https://doi.org/10.2174/18743315-v16-e220627

Sagisaka, S., The occurrence of peroxide in a perennial plant, Populus gelrica, Plant Physiol., 1976, vol. 57, pp. 308–309. https://doi.org/10.1104/pp.57.2.308

Siddiqui, M.H., Alamri, S., Al-Khaishany, M.Y., et al., Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings, Int. J. Mol. Sci., 2019, vol. 20, no. 2, p. 353. https://doi.org/10.3390/ijms20020353

Signorelli, S., Coitino, E.L., Borsani, O., and Monsa, J., Molecular mechanisms for reactions between OH radicals and proline, J. Phys. Chem., 2014, vol. 118, no. 1, pp. 137–147. https://doi.org/10.1021/jp407773u

Sun, Q., Zhang, N., Wang, J., et al., Melatonin promotes ripening and improves quality of tomato fruit during postharvest life, J. Exp. Bot., 2015, vol. 66, no. 3, pp. 657–668. https://doi.org/10.1093/jxb/eru332

Tan, D.X., Chen, L.D., Poeggeler, B., et al., Melatonin: a potent, endogenous hydroxyl radical scavenger, J. Pineal Res., 1993, vol. 1, pp. 57–60.

Taraban, D.A., Karpets, Yu.V., Yastreb, Ò.O., et al., Ca2+- and ROS-dependent induction of heat resistance of wheat seedlings by exogenous melatonin, Rep. Natl. Acad. Sci. Ukr., 2022, vol. 4, pp. 98–105. https://doi.org/10.15407/dopovidi2022.04.098

Wang, P., Yin, L., Liang, D., et al., Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle, J. Pineal Res., 2012, vol. 53, no. 1, pp. 11–20. https://doi.org/10.1111/j.1600-079X.2011.00966.x

Wang, Y., Reiter, R.J., and Chan, Z., Phytomelatonin: a universal abiotic stress regulator, J. Exp. Bot., 2018, vol. 69, no. 5, pp. 963–974. https://doi.org/10.1093/jxb/erx473

Wei, J., Li, D., Zhang, J., et al., Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana, J. Pineal Res., 2018, vol. 65, no. 2, p. e12500. https://doi.org/10.1111/jpi.12500

Xu, W., Cai, S.Y., Zhang, Y., et al., Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants, J. Pineal Res., 2016, vol. 61, no. 4, pp. 457–469. https://doi.org/10.1111/jpi.12359

Yadav, R., Saini, R., Adhikary, A., and Kumar, S., Unravelling cross priming induced heat stress, combinatorial heat and drought stress response in contrasting chickpea varieties, Plant Physiol. Biochem., 2022, vol. 180, no. 1, pp. 91–105. https://doi.org/10.1016/j.plaphy.2022.03.030

Yatsyshyn, V.Yu., Kvasko, A.Yu., and Yemets, A.I., Genetic approaches in research on the role of trehalose in plants, Cytol. Genet., 2017, vol. 51, no. 5, pp. 371–383. https://doi.org/10.3103/S0095452717050127

Yu, Y., Lv, Y., Shi, Y., et al., The role of phytomelatonin and related metabolites in response to stress, Molecules, 2018, vol. 23, no. 8, p. 1887. https://doi.org/10.3390/molecules23081887

Zhang, J., Shi, Y., Zhang, X., et al., Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.), Environ. Exp. Bot., 2017, vol. 138, pp. 36–45. https://doi.org/10.1016/j.envexpbot.2017.02.012

Zhang, H., Liu, L., Wang, Z., et al., Induction of low temperature tolerance in wheat by presoaking and parental treatment with melatonin, Molecules, 2021, vol. 26, p. 1192. https://doi.org/10.3390/molecules26041192

Zhao, K., Fan, H., Zhou, S., and Song, J., Study on the salt and drought tolerance of Suaeda salsa and Kalanchoe claigremontiana under iso-osmotic salt and water stress, Plant Sci., 2003, vol. 165, no. 4, pp. 837–844. https://doi.org/10.1016/S0168-9452(03)00282-6