ISSN 2415-8860 (online), ISSN 0372-4123 (print)
logoUkrainian Botanical Journal
  • 6 of 6
Up
Ukr. Bot. J. 2022, 79(3): 184–192
https://doi.org/10.15407/ukrbotj79.03.184
Biotechnology, Physiology and Biochemistry

Effect of low-temperature stress on the growth of plants of Secale cereale (Poaceae) and endogenous cytokinin content in roots and shoots

Nina VEDENICHEVA, Mykola SHCHERBATYUK, Iryna KOSAKIVSKA
Abstract

Phytohormones play a key role in the regulation of plant acclimation to low temperature. To elucidate the role of cytokinins in rye plant response to chilling, we studied the dynamics of these hormones in shoots and roots under short-term and prolonged cold stress. The 7-day-old plants were exposed to cold stress (2 °C) for 2 h (alarm phase of response) or for 6 h for two days (acclimation phase of response). Endogenous content of cytokinins was analyzed by HPLC-MS method. Low temperature had a differential effect on the content of individual cytokinins and their localization in rye plants. During the short-term stress, a decrease in the content of active cytokinins (trans-zeatin and trans-zeatin riboside) in the roots and an increase in the shoots were shown. Prolonged low-temperature stress declined the amount of cytokinins except trans-zeatin riboside, which was detected in both roots and shoots. Significant rise in trans-zeatin riboside content in roots and shoots in this period evidenced an important role of this cytokinin during cold acclimation of rye plants.

Keywords: adaptation, cytokinins, growth, low temperature, Secale cereale, stress

Full text: PDF (Eng) 778K

References
  1. Ahres M., Pálmai T., Gierczik K., Dobrev P., Vanková R., Galiba G. 2021. The impact of far-red light supplementation on hormonal responses to cold acclimation in barley. Biomolecules, 11(3): 450. https://doi.org/10.3390/biom11030450
  2. Bahrani H., Båga M., Larsen J., Graf R.J., Laroche A., Chibbar R.N. 2021. The relationships between plant developmental traits and winter field survival in rye (Secale cereale L.). Plants (Basel), 10(11): 2455. https://doi.org/10.3390/plants10112455
  3. Bakhtavar M.A., Afzal I., Basra S.M.A., Ahmad A.H., Noor M.A. 2015. Physiological strategies to improve the performance of spring maize (Zea mays L.) planted under early and optimum sowing conditions. PLoS ONE, 10(4): e0124441. https://doi.org/10.1371/journal.pone.0124441
  4. Belintani N.G., Guerzoni J.T., Moreira R.M., Vieira L.G. 2011. Improving low-temperature tolerance in sugarcane by expressing the ipt gene under a cold inducible promoter. Biologia Plantarum, 56: 71–77. https://doi.org/10.1007/s10535-012-0018-1
  5. Cortleven A., Leuendorf J.E., Frank M., Pezzetta D., Bolt S., Schmülling T. 2019. Cytokinin action in response to abiotic and biotic stress in plants. Plant, Cell & Environonment, 42: 998–1018. https://doi.org/10.1111/pce.13494
  6. Dello Ioio R., Galinha C., Fletcher A.G., Grigg S.P., Molnar A., Willemsen V., Scheres B., Sabatini S., Baulcombe D., Maini P.K., Tsiantis M. 2012. A PHABULOSA/cytokinin feedback loop controls root growth in Arabidopsis. Current Biology, 22: 1699–1704. https://doi.org/10.1016/j.cub.2012.07.005
  7. Deng W., Casao M., Wang P., Sato K., Hayes P.M., Finnegan E.J., Trevaskis B. 2015. Direct links between the vernalization response and other key traits of cereal crops. Nature Communications, 6: 5882. https://doi.org/10.1038/ncomms6882
  8. Dobrá J., Černý M., Štorchová H., Dobrev P., Skalák J., Jedelský P.L., Lukšanová H., Gaudinová A., Pešek B., Malbeck J., Vanek T., Brzobohatý B., Vanková R. 2015. The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis. Plant Science, 231: 52–61. https://doi.org/10.1016/j.plantsci.2014.11.005
  9. Eremina M., Rozhon W., Poppenberger B. 2016. Hormonal control of cold stress responses in plants. Cellular and Molecular Life Sciences, 73(4): 797–810. https://doi.org/10.1007/s00018-015-2089-6
  10. Fenollosa E., Gámez A., Munné-Bosch S. 2018. Plasticity in the hormonal response to cold stress in the invasive plant Carpobrotus edulis. Journal of Plant Physiology, 231: 202–209. https://doi.org/10.1016/j.jplph.2018.09.009
  11. Frébort I., Kowalska M., Hluska T., Frébortová J., Galuszka P. 2011. Evolution of cytokinin biosynthesis and degradation. Journal of Experimental Botany, 62: 2431– 2452. https://doi.org/10.1093/jxb/err004
  12. Hassan M.A., Xiang C., Farooq M., Muhammad N., Yan Z., Hui X., Yuanyuan K., Bruno A.K., Lele Z., Jincai L. 2021. Cold stress in wheat: plant acclimation responses and management strategies. Frontiers in Plant Science, 12:676884. https://doi.org/10.3389/fpls.2021.676884
  13. Heidari P., Reza Amerian M., Barcaccia G. 2021. Hormone profiles and antioxidant activity of cultivated and wild tomato seedlings under low-temperature stress. Agronomy, 11(6): 1146. https://doi.org/10.3390/agronomy11061146
  14. Janda T., Majlath I., Szalai G. 2014. Interaction of temperature and light in the development of freezing tolerance in plants. Journal of Plant Growth Regulation, 33: 460–469. https://doi.org/10.1007/S00344-013-9381-1
  15. Jeon J., Kim N.Y., Kim S., Kang N.Y., Novák O., Ku S.J., Cho C., Lee D.J., Lee E.J., Strnad M., Kim J. 2010. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. The Journal of Biological Chemistry, 285(30): 23371–23386. https://doi.org/10.1074/jbc.M109.096644
  16. Jeon J., Kim J. 2013. Arabidopsis response Regulator1 and Arabidopsis histidine phosphotransfer Protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiology, 161(1): 408–424. https://doi.org/10.1104/pp.112.207621
  17. Kalapos B., Dobrev P., Nagy T., Vítámvás P., Györgyey J., Kocsy G., Marincs F., Galiba G. 2016. Transcript and hormone analyses reveal the involvement of ABA-signalling, hormone crosstalk and genotype-specific biological processes in cold-shock response in wheat. Plant Science, 253: 86–97. https://doi.org/10.1016/j.plantsci.2016.09.017
  18. Kalapos B., Novak A., Dobrev P., Nagy T., Vítámvás 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. Frontiers in Plant Science, 8: 2033. https://doi.org/10.3389/fpls.2017.02033
  19. Khan T.A., Fariduddin Q., Yusuf M. 2017. Low-temperature stress: is phytohormones application a remedy? Environmental Science and Pollution Research International, 24(27): 21574–21590. https://doi.org/10.1007/s11356-017-9948-7
  20. Kieber J.J., Schaller G.E. 2018. Cytokinin signaling in plant development. Development, 145: dev149344. https://doi.org/10.1242/dev.149344
  21. Kolupaev Yu.E., Gorelova E.I., Yastreb T.O. 2018. Mechanisms of plant adaptation to hypothermia: role of antioxidant system. Bulletin of Kharkiv National Agrarian University. Series Biology, 1(43): 6–33. http://nbuv.gov.ua/UJRN/Vkhnau_biol_2018_1_3 https://doi.org/10.35550/vbio2018.01.006
  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. Russian Journal of Plant Physiology, 66: 540–547. https://doi.org/10.1134/S1021443719040058
  23. Kosová K., Prášil I.T., Vítámvás P., Dobrev P., Motyka V., Floková K., Novák O., Turečková V., Rolčik J., Pešek B., Trávničková A., Gaudinová A., Galiba G., Janda T., Vlasáková E., Prášilová P., Vanková R. 2012. Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. Journal of Plant Physiology, 169: 567–576. https://doi.org/10.1016/j.jplph.2011.12.013
  24. Kosová K., Vítámvás P., Urban M.O., Klíma M., Roy A., Prášil I.T. 2015. Biological networks underlying abiotic stress tolerance in temperate crops – a proteomic perspective. International Journal of Molecular Sciences, 16: 20913–20942. https://doi.org/10.3390/ijms160920913
  25. Li R., Sosa J.L., Zavala M.E. 2000. Accumulation of zeatin O-glycosyltransferase in Phaseolus vulgaris and Zea mays following cold stress. Plant Growth Regulation, 32: 295– 305. https://doi.org/10.1023/A:1010755901072
  26. Macková H., Hronková M., Dobrá J., Turečková V., Novák O., Lubovská Z., Motyka V., Haisel D., Hájek T., Prášil I.T., Gaudinová A., Štorchová H., Ge E., Werner T., Schmülling T., Vanková R. 2013. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. Journal of Experimental Botany, 64: 2805–2815. https://doi.org/10.1093/jxb/ert131
  27. Maruyama K., Urano K., Yoshiwara K., Morishita Y., Sakurai N., Suzuki H., Kojima M., Sakakibara H., Shibata D., Saito K., Shinozaki K., Yamaguchi-Shinozaki K. 2014. Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant Physiology, 164(4): 1759–1771. https://doi.org/10.1104/pp.113.231720
  28. Nguyen H.N., Nguyen T.Q., Kisiala A.B., Emery R.J.N. 2021. Beyond transport: cytokinin ribosides are translocated and active in regulating the development and environmental responses of plants. Planta, 254: 45. https://doi.org/10.1007/s00425-021-03693-2
  29. Prerostova S., Černý M., Dobrev P.I., Motyka V., Hluskova L., Zupkova B., Gaudinova A., Knirsch V., Janda T., Brzobohatý B., Vankova R. 2021. Light regulates the cytokinin-dependent cold stress responses in Arabidopsis. Frontiers in Plant Science, 11:608711. https://doi.org/10.3389/fpls.2020.608711
  30. Ritonga F.N., Chen S. 2020. Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants, 9(5): 560. https://doi.org/10.3390/plants9050560
  31. Romanov G.A., Lomin S.N., Schmülling T. 2018. Cytokinin signaling: from the ER or from the PM? That is the question! New Phytologist, 218: 41–53. https://doi.org/10.1111/nph.14991
  32. Romanov G.A., Schmülling T. 2021. On the biological activity of cytokinin free bases and their ribosides. Planta, 255(1): 27. https://doi.org/10.1007/s00425-021-03810-1
  33. Shi Y., Ding Y., Yang S. 2015. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant and Cell Physiology, 56(1): 7–15. https://doi.org/10.1093/pcp/pcu115
  34. Vanková R., Kosová K., Dobrev P., Vitámvás P., Trávnicková A., Cvikrová M., Pešek B., Gaudinová A., Prerostová S., Musilová J., Galiba G., Prásil I.T. 2014. Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level. Environonmental and Experimental Botany, 101: 12–25. https://doi.org/10.1016/j.envexpbot.2014.01.002
  35. Vedenicheva N.P., Al-Maali G.A., Mytropolska N.Yu., Mykhaylova O.B., Bisko N.A., Kosakivska I.V. 2016. Endogenous cytokinins in medicinal basidiomycetes mycelial biomass. Biotechnologia Acta, 9: 55–63. https://doi.org/10.15407/biotech9.01.055
  36. Vedenicheva N., Futorna O., Shcherbatyuk M., Kosakivska I. 2021. Effect of seed priming with zeatin on Secale cereale L. growth and cytokinins homeostasis under hyperthermia. Journal of Crop Improvement. (Published online) https://doi.org/10.1080/15427528.2021.2000909
  37. Veselova S.V., Farhutdinov R.G., Veselov S.Y., Kudoyarova G.R., Veselov D.S., Hartung W. 2005. The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.). Journal of Plant Physiology, 162(1): 21–26. https://doi.org/10.1016/j.jplph.2004.06.001
  38. White P., Cooper H., Earnshaw M., Clarkson D. 1990. Effects of low temperature on the development and morphology of rye (Secale cereale) and wheat (Triticum aestivum). Annals of Botany, 66: 559–566. https://doi.org/10.1093/oxfordjournals.aob.a088065
  39. Xia J.C., Zhao H., Liu W.Z., Li L.G., He Y.K. 2009. Role of cytokinin and salicylic acid in plant growth at low temperatures. Plant Growth Regulation, 57(3): 11–221. https://doi.org/10.1007/s10725-008-9338-8
  40. Xiang N., Hu J., Yan S., Guo X. 2021. Plant hormones and volatiles response to temperature stress in sweet corn (Zea mays L.) seedlings. Journal of Agricultural and Food Chemistry, 69(24): 6779–6790. https://doi.org/10.1021/acs.jafc.1c02275
  41. Zhao B., Liu Q., Wang B., Yuan F. 2021. Roles of phytohormones and their signaling pathways in leaf development and stress responses. Journal of Agricultural and Food Chemistry, 69(12): 3566–3584. https://doi.org/10.1021/acs.jafc.0c07908