Visn. Hark. nac. agrar. univ., Ser. Biol., 2020, Issue 3 (51), p. 71-86


O. I. Horielova1, N. I. Ryabchun2, M. A. Shkliarevskyi1, A. M. Reznik2, Yu. E. Kolupaev1

1Dokuchaev Kharkiv National Agrarian University
(Kharkiv, Ukraine)
2Yuryev Рlant Production Institute of the National Academy
 of Agrarian Sciences of Ukraine
(Kharkiv, Ukraine)

Along with specific adaptive reactions, universal defense reactions, in particular activation of antioxidant system, are of great importance for plant survival under cold conditions. We have studied a relationship among the content of low-molecular-weight protective compounds with antioxidant properties (proline, soluble carbohydrates, flavonoids), the activity of antioxidant enzymes (superoxide dismutase, catalase, and guaiacol peroxidase) in seedlings of winter wheat, rye and triticale, and frost resistance of etiolated seedlings and adult plants at tillering stage. It was found that there was a fairly close correlation between the frost resistance of seedlings and adult cereal plants (r = 0,78). It was shown that a pronounced relationship between individual indicators of antioxidant system functioning in unhardened seedlings and their frost resistance was not found. After 6-day hardening of seedlings at 2-4°C, there was a high correlation between the total indicator of the enzymatic antioxidant system (the sum of normalized indicators of superoxide dismutase, peroxidase, and catalase activity) and their frost resistance (r = 0,86), but the correlation coefficient of this index with frost resistance of plants in tillering phase was significantly lower (r = 0,47). At the same time, a high correlation was found between the content of low-molecular-weight protectors in hardened seedlings and frost resistance of tillering adult plants (r = 0.89). The closest correlation was observed between the integral normalized indicator, comprising the sum of normalized values of antioxidant enzymes activity and the content of low-molecular-weight protectors in hardened seedlings, and frost resistance of seedlings (r = 0,94) and plants in tillering phase (r = 0,89). A presence of specific features in the functioning of antioxidant system during cold adaptation of cereal seedlings was established. Rye is characterized by a high content of low-molecular-weight protective compounds; at the same time, increased activity of antioxidant enzymes - superoxide dismutase and catalase - was noted in wheat seedlings. In triticale, depending on the genotype, the values of both enzymatic antioxidant activity and the content of low-molecular-weight protectors varied.

Key words: Secale cereale, × Triticosecale, Triticum aestivum, cold hardening, frost resistance, oxidative stress, antioxidant enzymes, low-molecular-weight protective compounds



1. Gorelova E.I., Kolupaev Yu.E., Yastreb T.O., Shvidenko N.V., Popov Yu.V., Shklyarevskiy M.A., Ryabchun N.I. 2018. Constitutive and induced by cold hardening antioxidant activity in seedlings of winter cereals. Visn. Hark. nac. agrar. univ., Ser. Biol., 2 (44) : 59-68. (In Russian).
2. Diachenko L.F., Totsky V.N., Fait V.I., Toptikov V.A. 2007. Some gene-enzyme systems expression of different wheat lines with vrd1 and vrd2 genes seedlings in adaptation to low temperature. Visn. Odesk. Nats. Un-tu. Biologiya. 12 (5) : 103-111. (In Russian).
3. Ivanisov M.M., Ionova E.V. 2016. Frost tolerance of the varieties and lines of soft winter wheat. Mezhdu-narodnyy Nauchno-Issledovatel'skiy Zhurnal. 9-3 (51) : 110-113. (In Russian).
4. Kirichenko V.V., Petrenkova V.P., Riabchun N.I., Ivanova V.M., Dolgopolova V.I., Khirna G.P. 2008. DSTU 4749:2007 (BZ № 10-2006/654). Winter wheat. A method for determination of frost resistance of varieties. Kyiv : 8 p. (In Ukrainian).
5. Kolupaev Yu.E. 2016. Plant cell antioxidants and their role in ros signaling and plant resistance. Uspekhi Sovrem. Biologii. 136(2) :181-198. (In Russian).
6. Kolupaev Yu.E., Ryabchun N.I., Vayner A.A., Yastreb T.O., Oboznyi A.I. 2015. Antioxidant enzyme activity and osmolyte content in winter cereal seedlings under hardening and cryostress. Russ. J. Plant Physiol. 62 (4) : 499-506.
7. Kolupaev Yu.E., Yastreb T.O., Oboznyi A.I., Ryabchun N.I., Kirichenko V.V. 2016. Constitutive and cold-induced resistance of rye and wheat seedlings to oxidative stress. Russ. J. Plant Physiol. 63 (3) : 326-337.
8. Morgun V.V, Major P.S. 2009. Winter and frost resistance of winter cereals. In: Plant Physiology: Problems and Prospects for Development, vol. 2. Kyiv : 105-165. (In Ukrainian).
9. Naraikina N.V., Sin'kevich M.S., Demin I.N., Selivanov A.A., Moshkov I.E., Trunova, T.I. 2014. 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. 61 : 332-338.
10. Naraikina N.V. 2017. Features of hardening of cold-resistant potato plants to hypothermia and the role of Δ12-acyl-lipid desaturase. PhD Diss. (Biol.). Thesis. Moscow : 20 p. (In Russian).
11. Radyukina N.L., Toaima V.I.M., Zaripova N.R. 2012. The involvement of low-molecular antioxidants in cross-adaptation of medicine plants to successive action of UV-B radiation and salinity. Russ. J. Plant Physiol. 59 (1): 71-78.
12. Ryabchoun N.I., Kolupaev Yu.E., Vayner A.A., Yastreb T.О., Oboznyi A.I., Chetverik A.N. Antioxidant system components of winter wheat seedling genotypes varying in resistance to frost. Agrokhimiya. 1 : 73-81. (In Russian).
13. Samygin G.A. 1967. Rapid determination of the relative hardiness of wheat samples by freezing of germinated seeds. In: Metody opredeleniya morozostoikosti rastenii (Methods for Determination of Frost Resistance), Moscow : 77-84. (In Russian).
14. Sin'kevich M.S., Deryabin A.N., Trunova T.I. 2009. Characteristics of oxidative stress in potato plants with modified carbohydrate metabolism. Russ. J. Plant Physiol. 56 (2) : 168-174.
15. Sinkevich M.S., Naraykina N.V., Trunova T.I. 2010. Involvement of sugars in the antioxidant defense against paraquat-induced oxidative stress in potato transformed with yeast invertase gene. Doklady Biological Sciences. 434 (4) : 338-340.
16. Surinov A., Mkhitaryan V., Agapova G., Mironkina Yu., Luppov A. 2018. Statistic. Pt. 1. Moskow : 249 p. (In Russian).
17. Tarakhovkii Yu.S., Kim Yu.A., Abdrasilov B.S., Muzafarov E.N. 2013. Flavonoids: biochemistry, biophysics, medicine. Puschino : 310 p. (In Russian).
18. Trunova T.I. 2007. Plant and Low Temperature Stress, the 64th Timiryazev Lecture Moscow: Nauka. 54 p. (In Russian).
19. Tumanov I.I. 1979. Fiziologiya zakalivaniya i morozostoykosti rasteniy (Physiology of hardening and frost resistance of plants). Moscow : 352 p. (In Russian).
20. Aghaee A., Moradi F., Zare-Maivan H., Zarinkamar F., Aghaee A., Moradi F., Zare-Maivan H., Zarinkamar F., Pour Irandoost H., Sharifi P. 2011.Physiological responses of two rice (Oryza sativa L.) genotypes to chilling stress at seedling stage. Afr. J. Biotechnol. 10 : 7617-7621.
21. Bates LS., Walden R.P., Tear G.D. 1973. Rapid determination of free proline for water stress studies. Plant Soil. 39 : 205-210.
22. Cacela C., Hincha D.K. 2006. Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes. Biophys. J. 90 : 2831-2842.
23. Chen L.J., Xiang H.Z., Miao Y., Zhang L., Guo Z.F., Zhao X.H., Lin J.W., Li T.L.: 2014. An overview of cold resistance in plants. J. Agron. Crop Sci. 200 : 237-245.
24. Grabelnych O.I., Sumina O.N., Funderat S.P., Pobezhimova T.P., Voinikov V.K., Kolesnichenko A.V. 2004. The distribution of electron transport between the main cytochrome and alternative pathways in plant mitochondria during short-term cold stress and cold hardening. J. Therm. Biol. 29 : 165-175.
25. Guo Z., Ou W., Lu S., Zhong Q. 2006. Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol. Biochem. 44 : 828-836.
26. Havaux M., Kloppstech K. 2001. The protective functions of carotenoid and flavonoids pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta. 213 : 953-966.
27. Hayat S., Hayat Q., Ahead A. 2012. Role of proline under changing environments. Plant Signal. Behav. 7 : 1456-1466.
28. Janda T., Szalai G., Rios-Gonzalez K., Veisz O., Páldi E. 2003. Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci. 164 : 301-306.
29. John R., Anjum N.A., Sopory S.K., Akram N.A., Ashraf M. 2016. Some key physiological and molecular processes of cold acclimation. Biol. Plant. 60 : 603-618.
30. Kamata T., Uemura M. 2004. Solute accumulation in heat seedlings during cold acclimation: Contribution to increased freezing tolerance. Cryo Letters. 25 : 311-322.
31. Kaplan F., Kopka J., Sung D.Y., Zhao W., Popp M., Porat R., Guy C.L. 2007. Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J. 50 : 967-981.
32. Kavi Kishor, P.B., Sreenivasulu, N. 2014. Is proline accumulation per se correlated with stress tolerance or is proline homoeostasis a more critical issue?. Plant Cell Environ. 37 : 300-311.
33. Khlestkina E.K. 2013. The adaptive role of flavonoids: emphasis on cereals. Cereal Res. Commun. 41 : 185-198.
34. Kolupaev Yu. E., Horielova E. I., Yastreb T. O., Ryabchun N. I. 2020. State of antioxidant system in triticale seedlings at cold hardening of varieties of different frost resistance. Cereal Res. Commun. 48(2): 165-171.
35. Korn M., Peterek S., Mock H.-P., Heyer A.G., Hincha D.K. 2008. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ. 31(6) : 813-827.
36. Liang X., Zhang L., Natarajan S.K., Becker D.F. 2013. Proline mechanisms of stress survival. Antioxid. Redox Signal. 19 : 998-1011.
37. Nogues S., Baker N.R. 2000. Effects of drought on photosynthesis in Mediterranean plants grown under UV-B radiation. J. Exp. Bot. 51 : 1309-1317.
38. Patade V.Y., Khatri D., Ahmed Z. 2013.Cold tolerance in Osmotin transgenic tomato (Solanum lycopersicum L.) is associated with modulation in transcript abundance of stress responsive genes. SpringerPlus 2: 117.
39. Penfield S. 2008. Temperature perception and signal transduction in plants. New Phytol. 179 : 615-628.
40. Pennycooke J.C., Jones M.L., Stushnoff C. 2003. Down-regulating alpha-galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol 133 : 901-909.
41. Rasheed R., Wahid A., Ashraf M., Basra S.M.A. 2010.Role of proline and glycinebetaine in improving chilling stress tolerance in sugarcane buds at sprouting. Int. J. Agr. Biol. 12 : 1-8.
42. Ruelland E., Vaultier M.‐N., Zachowski A., Hurry V. 2009. Cold signalling and cold acclimation in plants. Advances in Botanical Research. 49 : 35-150.
43. Sarker B.C., Kulchhum M.U., Roy B., Hossain M.F., Haque M.M. 2015. Cold tolerance mechanism of rice cultivars based on physiomorphological characteristics. Journal of Science and Technology. 13 : 26-34.
44. Taji T., Ohsumi C., Iuchi S., Seki M., Kasuga M., Kobayashi M., Yamaguchi-Shinozaki K., Shinozaki K. 2002. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29 : 417-426.
45. Tantau H., Balko C., Brettschneider B., Melz G., Dorffling K. 2004. Improved frost tolerance and winter survival in winter barley (Hordeum vulgare L.) by in vitro selection of proline overaccumulating lines. Euphytica. 139 : 19-32.
46. Theocharis A., Clement C., Barka E.A. 2012. Physiological and molecular changes in plants grown at low temperatures. Planta. 235 : 1091-1105.
47. Wanner L., Junttila O.1999. Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120 : 391-400.
48. Zhao K., Fan H., Zhou S., Song J. 2003. Study on the salt and drought tolerance of Suaeda salsa and Kalanchoe claigremontiana under isoosmotic salt and water stress. Plant Sci. 165 : 837-844.