Вісн. Харків. нац. аграрн. ун-ту. Сер. Біологія, 2018, вип. 1 (43), с. 6-33


https://doi.org/10.35550/vbio2018.01.006




МЕХАНІЗМИ АДАПТАЦІЇ РОСЛИН ДО ГІПОТЕРМІЇ: РОЛЬ АНТИОКСИДАНТНОЇ СИСТЕМИ


Ю. Є. Колупаев1, 2, О. І. Горєлова1, Т. О. Ястреб1

1Харківський національний аграрний університет ім. В.В. Докучаєва
(Харків, Україна)
E-mail: plant_biology@ukr.net
2Харківський національний університет ім. В.Н. Каразіна
(Харків, Україна)


Окиснювальний стрес, пов'язаний в першу чергу з порушенням транспорту електронів в електрон-транспортних ланцюгах, зумовленим зміною стану ліпідів, розглядається як одна з важливих причин холодового ушкодження рослин. За дії на рослини негативних температур додатковою причиною посилення утворення активних форм кисню (АФК) може бути порушення функцій біомакромолекул і мембранних комплексів внаслідок зневоднення, зумовленого утворенням позаклітинного льоду. Антиоксидантна система, що забезпечує контроль вмісту АФК, є важливою протекторною системою, необхідною для виживання рослин за екстремальних низьких температур. Численними дослідженнями, виконаними на рослинах різної таксономічної приналежності, показана її активація при загартуванні і помірному холодовому стресі. Встановлено роль комплексу антиоксидантних ферментів і низькомолекулярних антиоксидантів у холодовій адаптації. Особливе значення для стійкості рослин до низьких температур мають пролин, цукри і деякі інші сполуки, що проявляють поряд з антиоксидантними осмопротекторний, мембранопротекторний і шаперонний ефекти. Як компоненти антиоксидантного захисту розглядаються також альтернативна оксидаза та інші роз'єднувальні білки, функціонування яких знижує ймовірність утворення АФК в мітохондріях за стресових умов. В огляді розглядаються питання функціональної взаємодії компонентів антиоксидантної та осмопротекторной систем при холодовому стресі. Підкреслюється необхідність врахування видових особливостей функціонування цих систем при скринінгу донорів стійкості для потреб селекції.Оцінюється роль холодоіндукованої активації антиоксидантної системи у прояві ефекту перехресної стійкості рослин до дії інших стресорів.


Ключові слова: активні форми кисню, антиоксидантана система, осмопротекторна система, холодостійкість, морозостійкість, крос-толерантність рослин

 


ЛІТЕРАТУРА


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.
https://doi.org/10.1134/S1021443710040084
 
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.
https://doi.org/10.1134/S1021443714030054
 
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.
https://doi.org/10.1023/B:BIRY.0000029857.05522.d5
 
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.
https://doi.org/10.1134/S0006297914060030
 
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.
https://doi.org/10.1134/S1021443708050075
 
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.
https://doi.org/10.1134/S1021443711040042
 
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.
https://doi.org/10.1134/S1021443710040126
 
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.
https://doi.org/10.17076/eb440
 
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.
https://doi.org/10.1134/S1021443708030035
 
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.
https://doi.org/10.15407/frg2017.06.463
 
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.
https://doi.org/10.1134/S102144371302012X
 
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.
https://doi.org/10.1134/S1021443715030115
 
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.
https://doi.org/10.1134/S1021443716030067
 
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.
https://doi.org/10.1016/B978-0-12-447650-9.50007-1
 
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.
https://doi.org/10.1134/S1021443710050067
 
31. Markovskaya E.F., Shibaeva T.G. 2017. Low temperature sensors in plants: Hypotheses and assumptions. Biology Bulletin. 44(2) : 150-158.
https://doi.org/10.1134/S1062359017020145
 
32. Medvedev S.S. 2005. Calcium signaling system in plants. Russ. J. Plant Physiol. 52(2) : 249-270.
https://doi.org/10.1007/s11183-005-0038-1
 
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.
https://doi.org/10.1134/S1021443706010055
 
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.
https://doi.org/10.1134/S0003683808050141
 
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.
https://doi.org/10.1134/S1021443711020154
 
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.
https://doi.org/10.1134/S1021443713060095
 
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.
https://doi.org/10.1134/S1021443709020058
 
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.
https://doi.org/10.1134/S1021443711010122
 
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.
https://doi.org/10.1134/S1021443712010165
 
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.
https://doi.org/10.17076/eb573
 
43. Rogov A.G., Zvyagilskaya R.A. 2015. Physiological role of alternative oxidase (from yeasts to plants) Biochemistry (Mosc.)., 80(4) : 400-407.
https://doi.org/10.1134/S0006297915040021
 
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.
https://doi.org/10.1134/S1021443709020046
 
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.
https://doi.org/10.1134/S0012496610050133
 
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.
https://doi.org/10.1134/S1021443709050203
 
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.
https://doi.org/10.1093/jxb/53.372.1331
 
54. Amtmann A. 2009. Learning from evolution: Thellungiella. Mol. Plant. 2 : 3-12.
https://doi.org/10.1093/mp/ssn094
 
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.
https://doi.org/10.1007/s11738-013-1381-z
 
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.
https://doi.org/10.1146/annurev.arplant.50.1.601
 
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.
https://doi.org/10.1134/S1021443715040056
 
59. Awasthi R., Bhandari K., Nayyar H. 2015. Temperature stress and redox homeostasis in agricultural crops. Front. Environ. Sci. 3 : 11.
https://doi.org/10.3389/fenvs.2015.00011
 
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.
https://doi.org/10.1016/S0168-9452(03)00329-7
 
61. Baxter A., Mittler R., Suzuki N. 2014. ROS as key players in plant stress signaling. J. Exp. Bot. 65(5) : 1229-1240.
https://doi.org/10.1093/jxb/ert375
 
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.
https://doi.org/10.1104/pp.104.2.725
 
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.
https://doi.org/10.1007/s11033-012-2402-5
 
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.
https://doi.org/10.1007/s11033-013-2921-8
 
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.
https://doi.org/10.1007/BF00714468
 
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.
https://doi.org/10.1093/aob/mct283
 
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.
https://doi.org/10.1016/j.jplph.2009.11.001
 
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.
https://doi.org/10.1093/jxb/erj027
 
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.
https://doi.org/10.1111/pce.12009
 
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.
https://doi.org/10.1016/S0168-1923(02)00253-8
 
73. Es-Safi N. E., Ghidouche S., Ducrot P.H. 2007. Flavonoids: hemisynthesis, reactivity, characterization and free radical scavenging activity. Molecules. 12 : 2228-2258.
https://doi.org/10.3390/12092228
 
74. Foyer C.H., Noctor G. 2009.Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Redox Signal. 11 : 861-906.
https://doi.org/10.1089/ars.2008.2177
 
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.
https://doi.org/10.1007/978-1-4614-8253-6_7
 
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.
https://doi.org/10.1016/j.plaphy.2010.08.016
 
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.
https://doi.org/10.1016/S0891-5849(00)00212-4
 
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.
https://doi.org/10.1016/j.plaphy.2006.10.024
 
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.
https://doi.org/10.1104/pp.103.4.1067
 
81. Gusta L.V., Wisniewski M. 2013. Understanding plant cold hardiness: an opinion. Physiol. Plant. 147 : 4-14.
https://doi.org/10.1111/j.1399-3054.2012.01611.x
 
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.
https://doi.org/10.1007/s004250100572
 
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.
https://doi.org/10.1104/pp.108.121384
 
87. Huang S., Millar A.H. 2013. Succinate dehydrogenase: the complex roles of a simple enzyme. Curr. Opin. Plant Biol. 16(3) : 344-349.
https://doi.org/10.1016/j.pbi.2013.02.007
 
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.
https://doi.org/10.1016/j.jplph.2009.04.002
 
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.
https://doi.org/10.1016/j.phytochem.2007.04.012
 
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.
https://doi.org/10.1016/S0168-9452(02)00414-4
 
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.
https://doi.org/10.1093/jxb/48.6.1195
 
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.
https://doi.org/10.1093/oxfordjournals.pcp.a029488
 
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.
https://doi.org/10.1016/B978-0-12-799963-0.00008-3
 
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.
https://doi.org/10.1007/s10535-012-0034-1
 
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.
https://doi.org/10.1038/352524a0
 
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.
https://doi.org/10.1016/S0168-9452(02)00090-0
 
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.
https://doi.org/10.1201/b10329-13
 
100. Koster K.L., Lynch D.V. 1992.Solute accumulation and compartmentation during the cold acclimation of puma rye. Plant Physiol. 98 : 108-113.
https://doi.org/10.1104/pp.98.1.108
 
101. Kozloff L.M., Turner M.A., Arellano F.J. 1991. Formation of bacterial membrane ice-nucleating lipoglycoprotein complexes. Bacteriol. 173 : 6528-6536.
https://doi.org/10.1128/jb.173.20.6528-6536.1991
 
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.
https://doi.org/10.1093/pcp/pch116
 
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.
https://doi.org/10.1089/ars.2012.5074
 
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.
https://doi.org/10.1155/2013/658793
 
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.
https://doi.org/10.5539/jas.v3n2p89
 
107. Marino D., Dunand C., Puppo A., Pauly N. 2012. A burst of plant NADPH oxidases. Trends Plant Sci. 17 : 9-15.
https://doi.org/10.1016/j.tplants.2011.10.001
 
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.
https://doi.org/10.1093/pcp/pcm061
 
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.
https://doi.org/10.1034/j.1399-3054.2002.1160306.x
 
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.
https://doi.org/10.1016/B978-0-12-520920-5.50019-5
 
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.
https://doi.org/10.1007/978-981-10-5254-5_1
 
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.
https://doi.org/10.1631/jzus.B1000147
 
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.
https://doi.org/10.1016/j.jplph.2005.08.003
 
114. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7 : 405-410.
https://doi.org/10.1016/S1360-1385(02)02312-9
 
115. Miura K., Furumoto T. 2013. Cold signaling and cold response in plants. Int. J. Mol. Sci. 14 : 5312-5337.
https://doi.org/10.3390/ijms14035312
 
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.
https://doi.org/10.1016/j.jplph.2007.04.004
 
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.
https://doi.org/10.1111/j.1399-3054.2007.00909.x
 
118. Moller I.M., Sweetlove L.J. 2010. ROS signaling-specificity is required. Trends Plant Sci. 15 : 370-374.
https://doi.org/10.1016/j.tplants.2010.04.008
 
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.
https://doi.org/10.1104/pp.102.4.1227
 
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.
https://doi.org/10.1021/jf030172q
 
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.
https://doi.org/10.1023/A:1010684719225
 
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.
https://doi.org/10.1074/jbc.M708106200
 
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.
https://doi.org/10.1046/j.1365-313x.2000.00845.x
 
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.
https://doi.org/10.1016/j.scienta.2008.07.031
 
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.
https://doi.org/10.1007/978-3-319-44081-1_1
 
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.
https://doi.org/10.3389/fpls.2015.00069
 
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.
https://doi.org/10.1023/A:1006152610137
 
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.
https://doi.org/10.1186/1471-2229-9-28
 
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.
https://doi.org/10.1104/pp.106.079129
 
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.
https://doi.org/10.1104/pp.122.1.199
 
131. , Zachowski A. 2010. How plants sense temperature. Envir. Exp. Bot. 69 : 225-232.
https://doi.org/10.1016/j.envexpbot.2010.05.011
 
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.
https://doi.org/10.1046/j.1365-313x.2001.01052.x
 
133. Scandalios J.G. 2002. The rise of ROS. Trends Biochem. Sci. 27 : 483-486.
https://doi.org/10.1016/S0968-0004(02)02170-9
 
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.
https://doi.org/10.1111/j.1469-8137.2010.03557.x
 
135. Shen B., Jensen R.G., Bohnert H.J. 1997. Mannitol protexts against oxidation by hydroxyl radicals. Plant Physiol. 115 : 527-532.
https://doi.org/10.1104/pp.115.2.527
 
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.
https://doi.org/10.1007/s00425-012-1799-3
 
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.
https://doi.org/10.1046/j.1365-3040.1999.00483.x
 
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.
https://doi.org/10.1266/ggs.81.349
 
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.
https://doi.org/10.1034/j.1399-3054.1997.1010105.x
 
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.
https://doi.org/10.1016/B978-0-12-799963-0.00003-4
 
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.
https://doi.org/10.1266/ggs.77.81
 
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.
https://doi.org/10.1007/s10681-004-2231-2
 
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.
https://doi.org/10.1016/j.molcel.2004.06.023
 
144. Theocharis A., Clement C., Barka E.A. 2012. Physiological and molecular changes in plants grown at low temperatures. Planta. 235 : 1091-1105.
https://doi.org/10.1007/s00425-012-1641-y
 
145. Testerink C., Munnik T. 2005. Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10 : 368-375.
https://doi.org/10.1016/j.tplants.2005.06.002
 
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.
https://doi.org/10.1007/978-1-4614-5001-6_2
 
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.
https://doi.org/10.1016/S0378-1119(02)00465-1
 
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.
https://doi.org/10.1007/978-3-319-44081-1_2
 
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.
https://doi.org/10.1007/1-4020-4225-6_5
 
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.
https://doi.org/10.1016/S0168-9452(99)00058-8
 
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.
https://doi.org/10.1111/j.1399-3054.2011.01471.x
 
152. Wanner L.A., Junttila O. 1999. Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 120 : 391-399.
https://doi.org/10.1104/pp.120.2.391
 
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.
https://doi.org/10.1007/s11103-005-6163-6
 
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.
https://doi.org/10.1007/s00299-008-0643-5
 
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.
https://doi.org/10.1007/978-1-4614-8253-6_20
 
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.
https://doi.org/10.2135/cropsci2010.06.0345
 
158. Zhong-Guang L., Ming G. 2011. Mechanical stimulation-induced cross-adaptation in plants: An overview. J. Plant Biol. 54 : 358-364.
https://doi.org/10.1007/s12374-011-9178-3
 
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.
https://doi.org/10.1016/j.plaphy.2012.07.010
 
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.
https://doi.org/10.1016/j.febslet.2004.09.006