Visn. Hark. nac. agrar. univ., Ser. Biol., 2018, Issue 1 (43), с. 6-33


Yu. Е. Kolupaev1, 2, Е. I. Gorelova1, Т. О. Yastreb1

1Dokuchaev Kharkiv National Agrarian University
(Kharkiv, Ukraine)
2Karazin Kharkiv National University
(Kharkiv, Ukraine)

Oxidative stress, associated primarily with violation of electron transport in electron transport chains due to changes in state of lipids, is considered as one of the important causes of cold damage to plants. When plants are exposed to negative temperatures, an additional reason for enhancing formation of reactive oxygen species (ROS) may be a disruption of functions of biomacromolecules and membrane complexes due to dehydration caused by extracellular ice formation. An antioxidant system, which provides control of ROS content, is an important protective system necessary for survival of plants at extreme low temperatures. Numerous studies performed on plants of different taxonomic affiliation showed its activation during hardening and moderate cold stress. The role of a complex of antioxidant enzymes and low-molecular antioxidants in cold adaptation has been established. Of particular importance for plant resistance to low temperatures are proline, sugars and some other compounds that manifest along with antioxidant osmoprotective, membrane-protective and chaperone effects. As components of antioxidant protection, alternative oxidase and other uncoupling proteins are also considered, functioning of which reduces the likelihood of ROS formation in mitochondria under stress conditions. The review deals with the functional interaction of the components of antioxidant and osmoprotective systems under cold stress. The need to take into account the specific features of functioning of these systems under screening of resistance donors for breeding needs is emphasized. The role of cold-induced activation of antioxidant system in manifestation of the cross-tolerance effect of plants to an action of other stressors is evaluated.

Key words: reactive oxygen species, antioxidant system, osmoprotective system, cold resistance, frost resistance, plants cross-tolerance



1. Ahmad P., Jaleel C.A., Sharma S. 2010. Antioxidant defense system, lipid peroxidation, proline-metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. Russ. J. Plant Physiol. 57(4) : 509-517.
2. Borovik O.A., Grabelnych O.I., Koroleva N.A., Pobezhimova T.P., Voinikov V.K. 2014. The influence of carbohydrate status and low temperature on the respiratory metabolism of mitochondria from etiolated leaves of winter wheat. J. Stress Physiol. Biochem. 10(4) : 118-130.
3. Borovik O.A. 2015. Functioning of alternative oxidase and NAD(F)H-dehydrogenases II type in mitochondria from etiolated and green shoots of winter wheat during cold hardening. PhD Diss. (Biol.). Thesis. Irkutsk : 22 p.
4. Voinikov V.K. 2013. The energy and information systems of plant cells in hypothermia. Novosidirsk : 212 p.
5. Gamburg K.Z., Korotaeva N.E., Baduev K., Borovsky G.B.. Voinikov VK. 2014. The relationship between the differences in frost resistance of Arabidopsis and Thellungiella and heat shock proteins and dehydrins. Russ. J. Plant Physiol. 61(3) : 318-323.
6. Gimalov F.R., Baymiev A.Kh., Matniyazov R.T., Chemeris A.V., Vakhitov V.A. 2004. Initial stages of low-temperature induction of cabbage cold shock protein gene csp5. Biochemistry (Mosc.). 69(5) : 575-579.
7. Grabelnych O.I., Borovik O.A., Tauson E.L., Pobezhimova T.P., Katyshev A.I., Pavlovskaya N.S., Koroleva N.A., Lyubushkina I.V., Bashmakov V.Yu., Popov V.N., Borovskii G.B., Voinikov V.K. 2014. Mitochondrial energy-dissipating systems (alternative oxidase, uncoupling proteins, and external NADH dehydrogenase) are involved in development of frost-resistance of winter wheat seedlings. Biochemistry (Mosc.). 79(6) : 506-519.
8. Grabelnych O.I., Pobezhimova T.P., Korzun A.M., Voznenko S.A., Koroleva N.A., Pavlovskaya N.S., Borovik O.A., Voinikov V.K. 2011. The participation of cyanide-resistant respiration in heat generation and antioxidative defense of cell in winter wheat shoots under cold influence. J. Stress Physiol. Biochem. 7(4) : 446-456.
9. Demin I.N., Deryabin A.N., Sinkevich M.S., Trunova T.I. Insertion of cyanobacterial desA gene coding for Δ12-acyl-lipid desaturase increases potato plant resistance to oxidative stress induced by hypothermia. Russ. J. Plant Physiol. 2008, Volume 55, Issue 5, pp 639-648.
10. Demin I.N., Naraikina N.V., Tsedendambaev V.D., Moshkov I.E., Trunova T.I. Integration of the cyanobacterial DesA gene for Δ12-acyl-lipid desaturase improves potato tolerance to paraquat-induced oxidative stress. Russi. J. Plant Physiol. 2011, 58 (4) : 660.
11. Javadian N., Karimzadeh G., Mahfoozi S., Ghanati F. 2010. Cold-induced changes of enzymes, proline, carbohydrates, and chlorophyll in wheat. Russ. J. Plant Physiol. 57(4) : 540-547.
12. 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.
13. Ignatenko A.A., Repkina N.  , Titov A.F., Talanova V.V. 2016. The response of cucumber plants to low temperature impacts of varying intensity. Trudy Karelsk. Nauchn. Tsentra RAN. 11 : 57-67.
14. Ivaschenko O.O., Ivaschenko O.O. 2008. Ways of adapting agriculture to climate change. Zbirn. Nauk. Pats Nats. Nauk. Tsentru "Institun Zemlerobstva" UAAN. Kyiv : 15-21.
15. Klimov S.V., Burakhanova E.A., Dubinina I.M., Alieva G.P., Sal'nikova E.B. Olenichenko N.A., Zagoskina N.V., Trunova T.I. 2008. Suppression of the source activity affects carbon distribution and frost hardiness of vegetating winter wheat plants. Russ. J. Plant Physiol. 55 (3) : 308-314.
16. Kolesnichenko A.V., Voinikov V.K. 2003. Proteins of low temperature plant stress. Irkutsk : 196 p.
17. Kolupaev, Yu.E. 2016. Plant cell antioxidants and their role in ros signaling and plant resistance. Uspekhi Sovrem. Biologii. 136(2) :181-198.
18. Kolupaev Yu.E., Karpets Yu.V. 2017. Role of signal mediators and stress hormones in regulation of plants antioxidative system. Fiziol. rast. genet. 49(6) : 463-481.
19. Kolupaev Yu.E., Oboznyi A.I., Shvidenko N.V. 2013. Role of hydrogen peroxide in generation of a signal inducing heat tolerance of wheat seedlings. Russ. J. Plant Physiol. 60(2) : 227-234.
20. 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.
21. Kolupaev Yu.E., Trunova T.I. 1992. Features of metabolism and protective functions of plant carbohydrates under stress. Fiziol. i Biokhim. Kult. Rast. 24(6) : 523-533.
22. 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.
23. Kolupaev Yu.E., Yastreb T.O. 2015. Physiological functions of nonenzymatic antioxidants in plants. Visn. Hark. nac. agrar. univ., Ser. Biol. 2(35) : 6-25.
24. Levitt J. 1978. An overview of freezing injury and survival, and its interrelationships to other stresses. In: Plant Cold Hardiness and Freezing Stress Mechanisms and Crop Implications. Eds. Li P.H., Sakai A. New York, San Francisco, London : 3-16.
25. Los D.A. 2005. Molecular mechanisms of plants cold tolerance. Vestnik Ross. AN. 75(4) : 338-345.
26. Los D.A. 2010. Sensory systems of cyanobacteria. Moscow : 218 p.
27. Lukatkin A.S. 2002. Cold damage to thermophilic plants and oxidative stress. Saransk : 208 p.
28. Major P.S., Zakharova V.P., Velykozhon L.G. 2009. Changes of free proline content in winter wheat plants during autumn-winter period. Fiziol. i Biokhim. Kult. Rast. 41(5) : 371-383.
29. Major P.S., Zakharova V.P., Velykozhon L.G. 2011. Activity of some antioxidant enzymes in wheat plants under natural conditions of hardening. Fiziol. i Biokhim. Kult. Rast. 43(6) : 507-512.
30. Markovskaya E.F., Sherudilo E.G., Galibina N.A., Sysoeva M.I. 2010. The role of carbohydrates in the responses of chilling-sensitive plants to short- and long-term low-temperature treatments. Russ. J. Plant Physiol. 57(5) : 641-647.
31. Markovskaya E.F., Shibaeva T.G. 2017. Low temperature sensors in plants: Hypotheses and assumptions. Biology Bulletin. 44(2) : 150-158.
32. Medvedev S.S. 2005. Calcium signaling system in plants. Russ. J. Plant Physiol. 52(2) : 249-270.
33. Medvedev S.S., Tankelyun O.V., Batov A.Yu., Voronina O.V., Martinec J., Macháčková I. 2006. Ionophorous functions of phosphatidic acid in the plant cell. Russ. J. Plant Physiol., 53(1) : 39-47.
34. 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.
35. 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.
36. Olenichenko N.A., Zagoskina N.V., Astakhova N.V., Trunova T.I., Kuznetsov Yu.V. 2008. Primary and secondary metabolism of winter wheat under cold hardening and treatment with antioxidants. Appl Biochem Microbiol. 44(5): 535-540.
37. Piotrovskii M.S., Shevyreva T.A., Zhestkova I.M., Trofimova M.S. 2011. Activation of plasmalemmal NADPH oxidase in etiolated maize seedlings exposed to chilling temperatures Russ. J. Plant Physiol. 58(2) : 290-298.
38. Ponomarev A.G., Tatarinova T.D., Perk A.A., Vasilieva I.V., Bubyakina V.V. 2014. Dehydrins associated with the development of frost resistance of Asian white birch. Russ. J. Plant Physiol. 61(1) : 105-111.
39. Radyuk M.S., Domanskaya I.N., ShcherbakovR.A., Shalygo N.V. 2009. Effect of low above-zero temperature on the content of low-molecular antioxidants and activities of antioxidant enzymes in green barley leaves. Russ. J. Plant Physiol. 56(2) : 175-180.
40. Radyukina N.L., Shashukova A.V., Makarova S.S., Kuznetsov Vl.V. 2011. Exogenous proline modifies differential expression of superoxide dismutase genes in UV-B-irradiated Salvia officinalis plants. Russ. J. Plant Physiol. 58(1) : 51-59.
41. 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.
42. Repkina N.S., Ignatenko A.A., Panfilova K.M., Titov A.F., Talanova V.V. 2017. The dynamics of superoxid dismutase activity and its gene expression in wheat leaves during cold adaptation. Trudy Karelsk. Nauchn. Tsentra RAN. 5 : 89-98.
43. Rogov A.G., Zvyagilskaya R.A. 2015. Physiological role of alternative oxidase (from yeasts to plants) Biochemistry (Mosc.)., 80(4) : 400-407.
44. Samygin G.A. 1974. Causes of Plant Freezing. Moscow : 196 p.
45. Semenova E.F., Presnyakova E.V. 2007. Biochemical monitoring of the frost-resistance in winter plants of Camelina sativa. Sel'skokhozyaistvennaya biologiya 3 : 106-109.
46. 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.
47. 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.
48. Tarakhovkii Yu.S., Kim Yu.A., Abdrasilov B.S., Muzafarov E.N. 2013. Flavonoids: biochemistry, biophysics, medicine. Puschino : 310 p.
49. Tarchevskii I.A. 2002. Signal Systems of Plant Cells. Moscow : 294 p.
50. Trunova T.I. 2007. Plant and Low Temperature Stress, the 64th Timiryazev Lecture Moscow: Nauka. 54 p.
51. Shakirova F.M., Allagulova Ch.R., Bezrukova M.V., Aval'baev A.M., Gimalov F.R. 2009. The role of endogenous ABA in cold-induced expression of the TADHN dehydrin gene in wheat seedlings. Russ. J. Plant Physiol. 56(5) : 720-723.
52. 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.
53. Alscher R.G., Erturk N., Heath L.S. 2002. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53 : 1331-1341.
54. Amtmann A. 2009. Learning from evolution: Thellungiella. Mol. Plant. 2 : 3-12.
55. Ao P.X., Li Z.G., Gong M. 2013. Involvement of compatible solutes in chill hardening-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol. Plant. 35 : 3457-3464.
56. Apostolova P., Yordanova R., Popova L. 2008. Response of antioxidative defence system to low temperature stress in two wheat cultivars. Gen. Appl. Plant Physiol. 34 : 281-294.
57. Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 : 601-639.
58. Asadi-Sanam S., Pirdashti H., Hashempour A., Zavareh M., Nematzadeh G.A., Yaghoubian Y. 2015. The Physiological and biochemical responses of eastern purple coneflower to freezing stress. Russ. J. Plant Physiol. 62 : 515-523.
59. Awasthi R., Bhandari K., Nayyar H. 2015. Temperature stress and redox homeostasis in agricultural crops. Front. Environ. Sci. 3 : 11.
60. Baek K.H., Skinner D.Z. 2003. Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Sci. 165 : 1221-1227.
61. Baxter A., Mittler R., Suzuki N. 2014. ROS as key players in plant stress signaling. J. Exp. Bot. 65(5) : 1229-1240.
62. Brush RA, Griffith M, Mlynarz A. 1994. Characterization and quantification of intrinsic ice nucleators in winter rye (Secale cereale) leaves. Plant Physiol. 104 : 725-735.
63. Burbulis N., Jonytiene V., Kupriene R., Blinstrubiene A. 2011. Changes in proline and soluble sugars content during cold acclimation of winter rapeseed shoots in vitro. J. Food Agricult. Environ. 9 : 371-374.
64. Carvalho K., Campos M.K., Domingues D.S., Pereira L.F., Vieira L.G. 2013.The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol. Biol. Rep. 40 : 3269-3279.
65. Cheeseman J.M. 2007. Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress. 1(1) : 4-15.
66. Chen Y., Jiang J., Chang Q., Gu C., Song A., Chen S., Dong B., Chen F. 2014. Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol. Biol. Rep. 41 : 815-822.
67. Christie P.J., Alfenito M.R., Walbot V. 1994. Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: Enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta. 194 : 541-549.
68. Colton-Gagnon K., Ali-Benali M.A., Mayer B.F., Dionne R., Bertrand A., Do Carmo S., Charron J.B. 2014. Comparative analysis of the cold acclimation and freezing tolerance capacities of seven diploid Brachypodium distachyon accessions. Ann. Bot. 113 : 681-693.
69. Costa J.H., Mota E.F., Cambursano M.V., Lauxmann M.A., de Oliveira L.M., Silva Lima Mda G., Orellano E.G., Fernandes de Melo D. 2010. Stress-induced co-expression of two alternative oxidase (VuAox1 and 2b) genes in Vigna unguiculata. J. Plant Physiol. 167 : 561-570.
70. Couee I., Sulmon C., Gouesbet G., Amrani A.E. 2006. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J. Exp. Bot. 57 : 449-459.
71. Cvetkovska M., Vanlerberghe G.C. 2013. Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ. 36 : 721-732.
72. Engvild K.C. 2003. A review of the risks of sudden global cooling and its effects on agriculture. Agricult. Forest Meteorol. 115(3-4) : 127-137.
73. Es-Safi N. E., Ghidouche S., Ducrot P.H. 2007. Flavonoids: hemisynthesis, reactivity, characterization and free radical scavenging activity. Molecules. 12 : 2228-2258.
74. Foyer C.H., Noctor G. 2009.Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11 : 861-906.
75. Galiba G., Vanková R., Tari I., Bánfalvi Z., Poór P., Dobrev P., Boldizsár Á., Vágújfalvi A., Kocsy G. 2013. Hormones, NO, antioxidants and metabolites as key players in plant cold acclimation. In: Plant and Microbe Adaptations to Cold in a Changing World. Eds. R. Imai et al. New York : Springer Science+Business Media : 73-87.
76. Gill S.S., Tuteja N. 2010.Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 : 909-930.
77. Grabelnych O.I., Borovik O.A., Pobezhimova T.P., Koroleva N.A., Lyubushkina I.V., Zabanova N.S., Voinikov V.K. Change of AOX1a expression, encoding mitochondrial alternative oxidase, influence on the frost-resistance of arabidopsis plants. J. Stress Physiol.Biochem. 12(4) : 78-90.
78. Guan L.M., Scandalios J.G. 2000. Hydrogen peroxide-mediated catalase gene expression in response to wounding. Free Radical Biol. Med. 28 : 1182-1190.
79. 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.
80. Gupta S., Webb P.R., Holaday A.S., Allen R.D. 1993. Overexpression of superoxide dismutase protects plants from oxidative stress (Induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol. 103 : 1067-1073.
81. Gusta L.V., Wisniewski M. 2013. Understanding plant cold hardiness: an opinion. Physiol. Plant. 147 : 4-14.
82. Guy C., Kaplan F., Kopka J., Selbig J., Hincha D.K. 2008. Metabolomics of temperature stress. Physiol. Plant. 132 : 220-235.
83. Hale H.B. 1969. Cross adaptation. Environm. Res. 2(2) : 323-334.
84. Hassan N.S., Shaaban L.D., Hashem E.-S.A., Seleem E.E. 2004. In vitro selection for water stress tolerant callus line of Helianthus annus L. cv. Myak. Int. J. Agr. Biol. 1 : 13-18.
85. 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.
86. Ho L. H., GiraudE., Uggalla V., Lister R., Clifton R., Glen A., Thirkettle-Watts D., Van Aken O., Whelan J. 2008. Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147 : 1858-1873.
87. Huang S., Millar A.H. 2013. Succinate dehydrogenase: the complex roles of a simple enzyme. Curr. Opin. Plant Biol. 16(3) : 344-349.
88. Islam M., Hoque A., Okuma E., Banu M.N., Shimoishi Y., Nakamura Y., Murata Y. 2009. Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J. Plant Physiol. 166 : 1587-1597.
89. Janda T., Szalai G., Leskó K., Yordanova R., Apostol S., Popova L.P. 2007. Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochem. 68. : 1674-1682.
90. 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.
91. Janmohammadi M., Enayati V., Sabaghnia N. 2012.Impact of cold acclimation, de-acclimation and re-acclimation on carbohydrate content and antioxidant enzyme activities in spring and winter wheat. Icel. Agric. Sci. 25 : 3-11.
92. Jian L.C., Li P.H., Sun L.H., Chen T.H.H. 1997. Alterations in ultrastructure and subcellular localization of Ca2+ in poplar apical bud cells during the induction of dormancy. J. Exp. Bot. 48 : 1195-1207.
93. Jian L.C., Li J.H., Chen W.P., Li P.H., Ahlstrand G.G. 1999. Cytochemical localization of calcium and Ca2+-ATPase activity in plant cells under chilling stress: a comparative study between the chillingsensitive maize and the chilling-insensitive winter wheat. Plant Cell Physiol. 40 : 1061-1071.
94. Kaur R., Nayyar H. 2014. Ascorbic acid a potent defender against environmental stresses. In: Oxidative Damage to Plants Antioxidant Networks and Signaling. Ed. Ahmad P. Academic Press is an imprint of Elsevier : 235-287.
95. Klíma M., Vítámvás P., Zelenková S., Vyvadilová M., Prášil I.T. 2012. Dehydrin and proline content in Brassica napus and B. Carinata under cold stress at two irradiances. Biol. Plant. 56 : 157-161.
96. Knight M.R., Campbell A.K., Smith S.M., Trewavas A.J. 1991. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature. 352 : 524-526.
97. Kocsy G., Simon-Sarkadi L., Kovács Z., Boldizsár Á., Sovány C., Kirsch K., Galiba G. 2011. Regulation of free amino acid and polyamine levels during cold acclimation in wheat. Acta Biol. Szeged. 55 : 91-93.
98. Konstantinova T., Parvanova D., Atanassov A., Djilianov D. 2002. Freezing tolerant tobacco, transformed to accumulate osmoprotectants. Plant Sci. 163 : 157-164.
99. Kosova K., Prasil I.T., Vitamvas P. 2010. Role of dehydrins in plant stress response. In: Handbook of Plant and Crop Stress. Ed. M. Pessarakli. Tucson : 239-285.
100. Koster K.L., Lynch D.V. 1992.Solute accumulation and compartmentation during the cold acclimation of puma rye. Plant Physiol. 98 : 108-113.
101. Kozloff L.M., Turner M.A., Arellano F.J. 1991. Formation of bacterial membrane ice-nucleating lipoglycoprotein complexes. Bacteriol. 173 : 6528-6536.
102. Kurimoto K., MillarA.H., Lambers H., Day D.A., Noguchi K. 2004. Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant Cell Physiol. 45 : 1015-1022.
103. Levitt J. 1980. Responses of plants to environmental stresses, vol. 1. London : 497 p.
104. Liang X., Zhang L., Natarajan S.K., Becker D.F. 2013. Proline mechanisms of stress survival. Antioxid. Redox Signal. 19 : 998-1011.
105. Liu W., Yu K., He T., Li F., Zhang D., Liu J. 2013. The low temperature induced physiological responses of Avena nuda L., a cold-tolerant plant species. Sci. World J. 2013 : 658793.
106. Luo Y., Tang H. Zhang Y. 2011. Production of reactive oxygen species and antioxidant metabolism about strawberry leaves to low temperatures. J. Agr. Sci. 3 :. 89-96.
107. Marino D., Dunand C., Puppo A., Pauly N. 2012. A burst of plant NADPH oxidases. Trends Plant Sci. 17 : 9-15.
108. Matos A.R., Hourton-Cabassa C., Ciçek D., Rezé N., Arrabaça J.D., Zachowski A., Moreau F. 2007. Alternative oxidase involvement in cold stress response of Arabidopsis thaliana fad2 and FAD3+ cell suspensions altered in membrane lipid composition. Plant Cell Physiol. 48 : 856-865.
109. Matsumura T., Tabayashi N., Kamagata Y., Souma C., Saruyama H. 2002. Wheat catalase expressed in transgenic rice can improve tolerance against low temperature stress. Physiol. Plant. 116 : 317-327.
110. McKersie B.D., Senaratna T., Walker M.A., Kendall E.J. Hetherington P.R. 1988. Deterioration of membranes during aging in plants: evidence for free radical mediation. In: Senescence and Aging in Plants. Eds Nooden L.D., Leopold A.C. Academic Press : 441-464.
111. Mehla N., Sindhi V., Josula D., Bisht P., Wani S.H. 2017. An introduction to antioxidants and their roles in plant stress tolerance. In: Reactive Oxygen Species and Antioxidant Systems in Plants: Role and Regulation under Abiotic Stress. Eds. Khan M.I.R., Khan N.A. Springer Nature Singapore Pte Ltd., : 1-24.
112. Mei Y., Song S. 2010. Response to temperature stress of reactive oxygen species scavenging enzymes in the cross-tolerance of barley seed germination. J. Zhejiang Univ. Sci. B. 11 : 965-972.
113. Mishra S., Dubey R.S. 2006. Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant. J. Plant Physiol. 163 : 927-936.
114. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7 : 405-410.
115. Miura K., Furumoto T. 2013. Cold signaling and cold response in plants. Int. J. Mol. Sci. 14 : 5312-5337.
116. Mizuno N., Sugie A., Kobayashi F., Takumi S. 2008. Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat. Plant Physiol. 165 : 462-467.
117. Molinari H.B.C., Marura C.J., Daros E., De Campos M.K.F., De Carvalho J.F.R.P., Filho J.C.B., Pereira L.F.P., Vieira L.G.E. 2007. Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol. Plant. 130 : 218-229.
118. Moller I.M., Sweetlove L.J. 2010. ROS signaling-specificity is required. Trends Plant Sci. 15 : 370-374.
119. Monroy A.F., Sarhan F., Dhindsa R.S. 1993. Cold-Induced changes in freezing tolerance, protein phosphorylation, and gene expression (evidence for a role of calcium). Plant Physiol. 102 : 1227-1235.
120. Morelli R., Russo-Volpe S., Bruno N., Lo Scalzo R. 2003. Fenton-dependent damage to carbohydrates: free radical scavenging activity of some simple sugars. J. Agric. Food Chem. 51 : 7418-7425.
121. 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 : 691-703.
122. Ogasawara Y., Kaya H., Hiraoka G., Yumoto F., Kimura S., Kadota Y., Hishinuma H., Senzaki E., Yamagoe S., Nagata K., Nara M., Suzuki K., Tanokura M., Kuchitsu K. 2008. Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. Biol. Chem. 283 : 8885-8892.
123. Orvar B.L., Sangwan V., Omann, F., Dhindsa R.S. 2000. Early steps in cold sensing by plant cells: The role of actin cytoskeleton and membrane fluidity. Plant J. 23 : 785-794.
124. Ozden M., Demirel U., Kahraman A. 2009. Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Sci. Horticult. 119 : 163-168.
125. Paciolla C., Paradiso A., de Pinto M.C. 2016. Cellular redox homeostasis as central modulator in plant stress response. In: Redox State as a Central Regulator of Plant-Cell Stress Responses. Eds. Gupta D.K. et al. Springer International Publishing Switzerland : 1-23.
126. Petrov V., Hille J., Mueller-Roeber B., Gechev T.S. 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 6 : 69.
127. Pietrini F., Massacci A. 1998. Leaf anthocyanin content changes in Zea mays L. grown at low temperature: Significance for the relationship between the quantum yield of PS II and the apparent quantum yield of CO2 Photosynthesis Res. 58 : 213-219.
128. Ramel F., Sulmon C., Bogard M., Couée I., Gouesbet G. 2009. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol. 9 : 28.
129. Rhoads D.M., Umbach A.L., Subbaiah C.C., Siedow J.N. 2006. Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141. : 357-366.
130. Ribas-Carbo M., Aroca R., Conzalez-Meler M.A., Irigoyen J.J., Sanchezdiaz M. 2000. The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize different in chilling sensitivity. Plant Physiol. 122 : 199-204.
131. , Zachowski A. 2010. How plants sense temperature. Envir. Exp. Bot. 69 : 225-232.
132. Sangwan V., Foulds I., Singh J., Dhindsa R.S. 2001. Cold-Activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ Plant J. 27 : 1-12.
133. Scandalios J.G. 2002. The rise of ROS. Trends Biochem. Sci. 27 : 483-486.
134. Searle S.Y., Thomas S., Griffin K.L., Horton T., Kornfeld A., Yakir D., Hurry V., Turnbull M. H. 2011. Leaf respiration and alternative oxidase in field-grown alpine grasses respond to natural changes in temperature and light. New Phytol. 189 : 1027-1039.
135. Shen B., Jensen R.G., Bohnert H.J. 1997. Mannitol protexts against oxidation by hydroxyl radicals. Plant Physiol. 115 : 527-532.
136. Shi K., Fu L.J., Zhang S., Li X., Liao Y.W.K., Xia X.J., Zhou Y.H., Wang R.Q., Chen Z.X., Yu, J.Q. 2013. Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants. Planta. 237 : 589-601.
137. Streb P., Shang W, Feierabend J. 1999. Resistance of cold-hardened winter rye leaves (Secale cereale L.) to photo-oxidative stress. Plant Cell Environ. 22 : 1211-1223.
138. Sugie A., Naydenov N., Mizuno N., Nakamura C., Takumi S. 2006. Overexpression of wheat alternative oxidase gene Waoxla alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet. Syst. 81 : 349-354.
139. Svenning M.M., Røsnes K., Junttila O. 1997. Frost tolerance and biochemical changes during hardening and dehardening in contrasting white clover populations. Physiol. Plant. 101 : 31-37.
140. Szollosi R. 2014. Superoxide dismutase (SOD) and abiotic stress tolerance in plants: an overview. oxidative damage to plants. In: Antioxidant Networks and Signaling. Ed Ahmad P. Elsevier Inc. : 89-129.
141. Takumi S., Tomioka M., Eto K., Naydenov N., Nakamura C. 2002. Characterization of two non-homoeologous nuclear genes encoding mitochondrial alternative oxidase in common wheat. Gen. Cenet. Syst. 77 : 81-88.
142. 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.
143. Teige M., Scheikl E., Eulgem T., Doczi R., Ichimura K., Shinozaki K., Dangl J.L., Hirt H. 2004. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell. 15 : 141-152.
144. Theocharis A., Clement C., Barka E.A. 2012. Physiological and molecular changes in plants grown at low temperatures. Planta. 235 : 1091-1105.
145. Testerink C., Munnik T. 2005. Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10 : 368-375.
146. Thakur P., Nayyar H. 2013. Chapter 2. Facing the cold stress by plants in the changing environment: sensing, signaling, and defending mechanisms. In: Plant Acclimation to Environmental Stress. Eds. Tuteja N., Singh Gill S. New York : Springer Science+Business Media :29-69.
147. Tognolli M., Penel C., Greppin H., Simon P. 2003. Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene. 288 : 129-138.
148. Trchounian A., Petrosyan M., Sahakyan N. 2016. Plant cell redox homeostasis and reactive oxygen species. In: Redox State as a Central Regulator of Plant-Cell Stress Responses. Eds. Gupta D.K. et al. Springer International Publishing Switzerland : 25-50.
149. Trischuk R.G., Schilling B.S., Wisniewski M., Gusta L.V. 2006. Freezing stress: systems biology to study cold tolerance. In: Physiology and Molecular Biology of Stress Tolerance in Plants. Eds. Madhava Rao K. et al. Dordrecht : Springer : 131-155.
150. Vagujfalvi A., Kerepesi I., Galiba G., Tischner T., Sutka J. 1999. Frost hardiness depending on carbohydrate changes during cold acclimation in wheat . Plant Sci. 144 : 85-92.
151. Wang J., Rajakulendran N., Amirsadeghi S., Vanlerberghe G.C. 2011.Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol. Plant. 142 : 339-351.
152. Wanner L.A., Junttila O. 1999. Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120 : 391-399.
153. Wlngsle G., Karpinski S., Hällgren J.E. 1999. Low Temperature, high light stress and antioxidant defence mechanisms in higher plants. Phyton (Austria). 39 : 253-268.
154. Wong C.E., Li Y., Whitty B.R., Diaz-Camino C., Akhter S.R., Brandle J.E., Golding G.B., Weretilnyk E.A., Moffatt B.A., Griffith M. 2005. Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol. Biol. 58 : 561-574.
155. Xu J., Yin H., Li X. 2009. Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep. 28 : 325-333.
156. Yoshida M., Kawakami A. 2013. Molecular analysis of fructan metabolism associated with freezing tolerance and snow mold resistance of winter wheat. In: Plant and Microbe Adaptations to Cold in a Changing World. Eds. Imai R. et al. New York: Springer Science+Business Media : 231-243.
157. Zhang X., Wang K., Ervin E.H., Waltz C., Murphy T. 2011. Metabolic changes during cold acclimation and deacclimation in five bermudagrass varieties. I. Proline, total amino acid, protein, and dehydrin expression. Crop Sci. 51 : 838-846.
158. Zhong-Guang L., Ming G. 2011. Mechanical stimulation-induced cross-adaptation in plants: An overview. J. Plant Biol. 54 : 358-364.
159. Zhou J., Wang, J., Shi, K., Xia, X.J., Zhou, Y.H., Yu, J.Q. 2012. Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol. Biochem. 60 : 141-149.
160. Zuther E., Buchel K., Hundertmark M., Stitt M., Hinch D.K., Heyer A.G. 2004. The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett. 576 : 169-173.