Fiziol. rast. genet. 2021, vol. 53, no. 4, 292-306, doi: https://doi.org/10.15407/frg2021.04.292

Endogenous cytokinins of Secale cereale L. under high temperature impact: dynamics and localization in the alarm, acclimation and recovery phase

Vedenicheva N.P., Shcherbatyuk M.M., Kosakivska I.V.

  • M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine  2 Tereshchenkivska St., Kyiv, 01601, Ukraine

The effect of high temperature stress on the cytokinins content in the overground part and roots of winter rye (Secale cereale L.) plants of the Boguslavka variety was studied under conditions of pot experiment. Plants were grown from seeds for 7 days at an air temperature of +16 °С, stress was created by transferring them to a thermostat with a temperature of +35 °С for 2 h (alarm stage) or twice for 6 h for two days (acclimation stage). Plants were also analyzed 5 days after the end of stressor action (recovery stage). The cytokinins qualitative composition and quantitative content were investigated by high performance liquid chromatography on Agilent 1200 LC liquid chromatograph with diode-matrix detector G 1315 B (USA). Significant changes in morphometric parameters, which reflected the inhibition of growth processes in rye plants under heat stress, were detected after two days of the experiment, while the pool of endogenous cytokinins considerable changed after 2 h of hyperthermia. In particular, concentration of trans-zeatin and trans-zeatin riboside notably decreased in the overground part, and in the roots — increased. The accumulation of free cytokinins was observed in the overground part of rye seedlings after two days of exposure to heat stress, at the same time a decrease in their levels was recorded in the roots. After a 5-day recovery period, the experimental plants differed from the control by a higher content of trans-zeatin and trans-zeatin riboside (approximately by 20 %) both in the overground part and in the roots. In general, studies have shown that hyperthermia has a differentiated effect on the content of individual cytokinins and their localization in the overground and underground parts of winter rye seedlings of Boguslavka variety. The detected fluctuations of cytokinins indicate their direct participation in the regulation of winter rye plants adaptation to the hyperthermia action.

Keywords: Sеcale cereale L., cytokinins, growth, hyperthermia, stress, adaptation

Fiziol. rast. genet.
2021, vol. 53, no. 4, 292-306

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References

1. Abhinandan, K., Skori, L., Stanic, M., Hickerson, N., Jamshed, M. & Samuel, M.A. (2018). Abiotic stress signaling in wheat - an inclusive overview of hormonal interactions during abiotic stress responses in wheat. Front. Plant Sci., 9, p. 734. https://doi.org/10.3389/fpls.2018.00734

2. Khan, N., Bano, A., Ali, S. & Babar, M.A. (2020). Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses. Plant Growth Regul., 90, pp. 189-203. https://doi.org/10.1007/s10725-020-00571-x

3. Eyidogan, F., Oz, M.T., Yucel, M. & Oktem, H.A. (2012). Signal transduction of phytohormones under abiotic stresses. Phytohormones and abiotic stress tolerance in plants. Ed. Khan N., Nazar R., Iqbal N., Anjum N. Berlin, Heidelberg: Springer-Verlag, pp. 1-48. https://doi.org/10.1007/978-3-642-25829-9_1

4. Huang, X., Hou, L., Meng, J., You, H., Li, Z., Gong, Z., Yang, S. & Shi, Y. (2018). The antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Mol. Plant., 11 (7), pp. 970-982. https://doi.org/10.1016/j.molp.2018.05.001

5. Javid, M.G., Soroosshzadeh, A., Moradi, F., Sanavy, S.A.M. & Allahdadi, I. (2011). The role of phytohormones in alleviating salt stress in crop plants. Australian J. Crop Plants, 5, pp. 726-734.

6. Musienko, M.M., Zhuk, V.V. & Batsmanova, L.M. (2014). Protective role of cytokinin under the heat stress on wheat plants. Ukr. Bot. J., 71, No. 2, pp. 244-249. [in Ukrainian]. https://doi.org/10.15407/ukrbotj71.02.244

7. Liu, X. & Huang, B. (2002). Cytokinin effects on creeping bentgrass response to heat stress. Crop Sci., 42, pp. 466-472. https://doi.org/10.2135/cropsci2002.4570

8. Mackova, H., Hronkova, M., Dobra, J., Tureckova, V., Novak, O., Lubovska, Z., Motyka, V., Haisel, D., Hajek, T., Prasil, I.T., Gaudinova, A., Storchova, H., Ge, E., Werner, T., Schmulling, T. & Vankova, R. (2013). Enhanced drought and heat stress tole­rance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J. Exp. Bot., 64, pp. 2805-2815. https://doi.org/10.1093/jxb/ert131

9. Reguera, M., Peleg, Z., Abdel-Tawab, Y.M., Tumimbang, E.B., Delatorre, C.A. & Blumwald, E. (2013). Stress-induced cytokinin synthesis increases drought tolerance through the coordinated regulation of carbon and nitrogen assimilation in rice. Plant Physiol., 163, pp. 1609-1622. https://doi.org/10.1104/pp.113.227702

10. Bielach, A., Hrtyan, M. & Tognetti, V.B. (2017). Plants under stress: Involvement of auxin and cytokinin. Int. J. Mol. Sci., 18, No. 7, p. 1427. https://doi.org/10.3390/ijms18071427

11. Cortleven, A., Leuendorf, J.E., Frank, M., Pezzetta, D., Bolt, S. & Schmulling, T. (2018). Cytokinin action in response to abiotic and biotic stress in plants. Plant, Cell & Environment., 42, No. 3, pp. 998-1018. https://doi.org/10.1111/pce.13494

12. Vedenicheva, N.P. & Kosakivska, I.V. (2020). Cytokinins in cereals ontogenesis and adaptation. Fiziol. rast. genet., 52, No. 1, pp. 3-30. [in Ukrainian]. https://doi.org/10.15407/frg2020.01.003

13. Hagenblad, J., Oliveira, H.R., Forsberg, N.E.G. & Leino, M.W. (2016). Geographical distribution of genetic diversity in Secale landrace and wild accessions. BMC Plant Biol., 16, p. 23. https://doi.org/10.1186/s12870-016-0710-y

14. Simonenko, N.V., Skorik, V.V. & Zhemoida, V.L. (2019). Results of selection work with winter rye at Nosivka breeding and research station. Roslynnytstvo i Gruntoznavstvo, 286, pp. 152-163 [in Ukrainian].

15. Bushuk, W. (2001). Rye: Production, Chemistry, and Technology (2nd edition). St. Paul, MN: AACC International, Inc. 239 p. https://doi.org/10.1016/S0144-8617(01)00359-9

16. Targonska, M., Hromada-Judycka, A., Bolibok-Bragoszewska, H. & Rakoczy-Trojanowska, M. (2013). The specificity and genetic background of the rye (Secale cereale L.) tissue culture response. Plant Cell Rep., 32, No. 1, pp. 1-9. https://doi.org/10.1007/s00299-012-1342-9

17. Hossein Pour, A., Aydin, M. & Haliloglu, K. (2020). Plant regeneration system in recalcitrant rye (Secale cereale L.). Biologia, 75, pp. 1017-1028. https://doi.org/10.2478/s11756-019-00395-9

18. Zimny, J. & Michalsky, K. (2019). Development of in vitro culture techniques for advancement of rye (Secale cereale L.) breeding. Acta Biologica Cracoviensia. Series Biologia, 61, No. 1, pp. 7-15. https://doi.org/10.24425/abcsb.2019.127735

19. Andreenko, S.S. (1970). Growth and development of cereals and buckwheat. In: Physiology of agricultural plants, Vol. VI, pp. 466-495 [in Russian].

20. Features of technologies for growing winter cereals for the 2019 harvest (autumn complex of works): recommendations (2018). Lviv: Obroshino [in Ukrainian].

21. Barnabas, B., Jager, K. & Fecher, A. (2008). The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell & Environment., 31, pp. 11-38. https:// doi.org/10.1111/j.1365-3040.2007.01727.x

22. Kolupaev, Y.E., Horielova, E.I., Yastreb, T.O., Ryabchun, N.I. & Kirichenko, V.V. (2019). Stress-protective responses of wheat and rye seedlings whose chilling resistance was induced with a donor of hydrogen sulfide. Rus. J. Plant Physiol., 66, pp. 540-547. https://doi.org/10.1134/S1021443719040058

23. Ndong, C., Danyluk, J., Huner, N.P. & Sarhan, F. (2001). Survey of gene expression in winter rye during changes in growth temperature, irradiance or excitation pressure. Plant Mol. Biol., 45, pp. 691-703. https://doi.org/10.1023/A:1010684719225

24. Chumikina, L.V., Arabova, L.I., Kolpakova, V.V. & Topunov, A.F. (2019). The role of phytohormones in the regulation of the tolerance of wheat, rye, and triticale seeds to the effect of elevated temperatures during germination. Appl. Biochem. Microbiol., 55, pp. 59-66. https://doi.org/10.1134/S0003683819010046

25. Musatenko, L., Vedenicheva, N., Vasjuk, V., Generalova, V., Martyn, G. & Sytnik, K. (2003). Phytohormones in seedlings of maize hybrids differing in their tolerance to high temperatures. Rus. J. Plant Physiol., 50, No. 4, pp. 444-448. https://doi.org/10.1023/A:1024704303406

26. Kosova, K., Vitamvas, P., Urban, M.O., Klima, M., Roy, A. & Prasil, I.T. (2015). Biological networks underlying abiotic stress tolerance in temperate crops - a proteomic perspective. Int. J. Mol. Sci., 16, No. 9, pp. 20913-20942. https://doi.org/10.3390/ijms160920913

27. Vedenicheva, N.P. & Kosakivska, I.V. (2020). Cytokinins as a plant ontogenesis regulators under different living conditions. Kyiv: Nash Format, 200 p. [in Ukrainian].

28. Cheikh, N. & Jones, R.J. (1994). Disruption of maize kernel growth and development by heat stress (role of cytokinin/abscisic acid balance). Plant Physiol., 106, No. 1, pp. 45-51. https://doi.org/10.1104/pp.106.1.45

29. Wang, H.Q., Liu, P., Zhang, J.W., Zhao, B. & Ren, B.Z. (2020). Endogenous hormones inhibit differentiation of young ears in maize (Zea mays L.) under heat stress. Front. Plant Sci., 11, p. 533046. https://doi.org/10.3389/fpls.2020.533046

30. Wu, C., Cui, K., Wang, W., Li, Q., Fahad, S., Hu, Q., Huang, J., Nie, L., Mohapatra, P.K. & Peng, S. (2017). Heat-induced cytokinin transportation and degradation are associated with reduced panicle cytokinin expression and fewer spikelets per panicle in rice. Front. Plant Sci., 8, p. 371. https://doi.org/10.3389/fpls.2017.00371

31. Veselov, S.Yu., Kudoyarova, G.R., Mustafina, A.R. & Valke, R. (1995). Dynamics of the endogenous cytokinins content in the shoots of transgenic and non-transformed tobacco seedlings under the influence of heat shock. Fiziologija rastenij, 42, pp. 694-697 [in Russian].

32. Todorova, D., Genkov, T., Vaseva-Gemisheva, I., Alexieva, V., Karanov, E., Smith, A. & Hall, M. (2005). Effect of temperature stress on the endogenous cytokinin content in Arabidopsis thaliana (L.) Heynh plants. Acta Physiol. Plant., 27, pp. 13-18. https://doi.org/10.1007/s11738-005-0031-5

33. Farkhutdinov, R.G., Kudoyarova, G.R., Veselov, S.Y. & Valke, R. (1997). Influence of temperature increase on evapotranspiration rate and cytokinin content in wheat seedlings. Biol. Plant., 39, pp. 289-291. https://doi.org/10.1023/A:1000627916005

34. Dobra, J., Cerny, M., Storchova, H., Dobrev, P., Skalak, J., Jedelsky, P.L., Luksanova, H., Gaudinova, A., Pesek, B., Malbeck, J., Vanek, T., Brzobohaty, B. & Vankova, R. (2015). The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis. Plant Sci., 231, pp. 52-61. https://doi.org/10.1016/j.plantsci.2014.11.005

35. Vedenicheva, N.P. & Kosakivska, I.V. (2016). Modern aspects of cytokinins studies: evolution and crosstalk with other phytohormones. Fiziol. rast. genet., 48, No. 1, pp. 3-19. [in Ukrainian]. https://doi.org/10.15407/frg2016.01.003

36. Li, M., Jannasch, A.H. & Jiang, Y. (2020). Growth and hormone alterations in response to heat stress in perennial ryegrass accessions differing in heat tolerance. J. Plant Growth Regul., 39, pp. 1022-1029. https://doi.org/10.1007/s00344-019-10043-w

37. Vaseva, I., Todorova, D., Malbeck, J., Travnickova, A. & Machackova, I. (2009). Mild temperature stress modulates cytokinin content and cytokinin oxidase/dehydrogenase activity in young pea plants. Acta Agron. Hung., 57, pp. 33-40. https://doi.org/10.1556/AAgr.57.2009.1.4

38. Cerny, M., Jedelsky, P., Novak, J., Schlosser, A. & Brzobohaty, B. (2014). Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant Cell Environ., 37, pp. 1641-1655. https://doi.org/10.1111/pce.12270

39. Skalak, J., Cerny, M., Jedelsky, P., Dobra, J., Ge, E., Novak, J., Hronkova, M., Dobrev, P.I., Vankova, R. & Brzobohaty, B. (2016). Stimulation of ipt overexpression as a tool to elucidate the role of cytokinins in high temperature responses of Arabidopsis thaliana. J. Exp. Bot., 67, pp. 2861-2873. https://doi.org/10.1093/jxb/erw129

40. Xu, Y., Gianfagna, T. & Huang, B. (2010). Proteomic changes associated with expression of a gene (ipt) controlling cytokinin synthesis for improving heat tolerance in a perennial grass species. J. Exp. Bot., 61, No. 12, pp. 3273-3289. https://doi.org/10.1093/jxb/erq149

41. Veerasamy, M., He, Y. & Yuang, B. (2007). Leaf senescence and protein metabolism in creeping bentgrass exposed to heat stress and treated with cytokinins. J. Amer. Soc. Horticult. Sci., 132, pp. 467-472. https://doi.org/10.21273/JASHS.132.4.467

42. Xu, Y., Tian, J., Gianfagna, T. & Huang, B. (2009). Effects of SAG12-ipt expression on cytokinin production, growth and senescence of creeping bentgrass (Agrostis stolonifera L.) under heat stress. Plant Growth Regul., 57, p. 281. https://doi.org/10.1371/journal.pone.0155437

43. Wu, C., Cui, K., Wang, W., Li, Q., Fahad, S., Hu, Q., Huang, J., Nie, L. & Peng, S. (2016). Heat-induced phytohormone changes are associated with disrupted early reproductive development and reduced yield in rice. Sci. Rep., 6, p. 34978. https://doi.org/10.1038/srep34978

44. Kieber, J.J. & Schaller, G.E. (2018). Cytokinin signaling in plant development. Development, 145, No. 4, pp. dev149344. https://doi.org/10.1242/dev.149344

45. Jing, H. & Strader, L.C. (2019). Interplay of auxin and cytokinin in lateral root development. Int. J. Mol. Sci., 20, p. 486. https://doi.org/10.3390/ijms20030486

46. Balla, K., Karsai, I., Bonis, P., Kiss, T., Berki, Z., Horvath, A., Mayer, M., Bencze, S. & Veisz, O. (2019). Heat stress responses in a large set of winter wheat cultivars (Triticum aestivum L.) depend on the timing and duration of stress. PLoS One, 14, No. 9, p. e0222639. https://doi.org/10.1371/journal.pone.0222639

47. Kalapos, B., Novak, A., Dobrev, P., Nagy, T., Vitamvas, P., Marincs, F., Galiba, G. & Vankova, R. (2017). Effects of the winter wheat Cheyenne 5A substitute chromosome on dynamics of abscisic acid and cytokinins in freezing-sensitive Chinese Spring genetic background. Front. Plant Sci., 8, p. 2033. https://doi.org/10.3389/fpls.2017.02033

48. Veselov, A.P., Lobov, V.P. & Olunina, L.N. (1998). Changes in the phytohormone content in the response of plants to heat shock and during its aftereffect. Fiziologija rastenij, 45, pp. 709-715 [in Russian].

49. Prerostova, S., Dobrev, P.I., Kramna, B., Gaudinova, A., Knirsch, V., Spichal, L., Zatloukal, M. & Vankova, R. (2020). Heat acclimation and inhibition of cytokinin degradation positively affect heat stress tolerance of Arabidopsis. Front. Plant Sci., 11, p. 87. https://doi.org/10.3389/fpls.2020.00087