Вісн. Харків. нац. аграрн. ун-ту. Сер. Біологія, 2017, вип. 1 (40), с. 21-34


https://doi.org/10.35550/vbio2017.01.021




АКТИВНІСТЬ СУПЕРОКСИДДИСМУТАЗИ В ОНТОГЕНЕЗІ РОСЛИН У НОРМІ І ЗА ДІЇ АБІОТИЧНИХ СТРЕСІВ


Л. О. Сахно

Державна установа «Інститут харчової біотехнології та геноміки»
Національної академії наук України
(Київ, Україна)


Узагальнено відомості щодо ролі ключового ферменту антиоксидантної системи рослин – супероксиддисмутази (СОД) – у процесах росту і розвитку та у забезпеченні толерантності до абіотичних стресів. Показано взаємозв’язок між активністю цього ферменту і особливостями відповіді рослинних тканин на умови культивування in vitro. Продемонстровано можливості трансгенезу у з’ясуванні ролі СОД в адаптації до абіотичних стресів і особливостей її регуляції. Запропоновано використовувати активність СОД для первинного скринінгу рослин на толерантність до сольового стресу та водного дефіциту.


Ключові слова: антиоксидантна система рослин, супероксиддисмутаза (СОД), засолення, водний дефіцит, трансгенез

 


ЛІТЕРАТУРА


1. Kolupaev Yu.E., Oboznyi A.I. 2013. Reactive oxygen species and antioxidative system at cross adaptation of plants to activity of abiotic stressors. Visn. Hark. nac. agrar. univ., Ser. Biol. 3 (30) : 18-31.
 
2. Arisi A.C.M., Cornic G., Jouanin L., Foyer C.H. 1998. Over-expression of Iron superoxide dismutase in trans-formed poplar modifies the regulation of photosyn-thesis at low CO2 partial pressures or following exposure to the prooxidant herbicide methyl viologen. Plant Physiol. 117 : 565-574.
https://doi.org/10.1104/pp.117.2.565
 
3. Bagnoli F., Capuana M., Racchi M.L. 1998. Developmental changes of catalase and superoxide dismutase isoenzymes in zygotic and somatic embryos of horse chestnut. Aust. J. Plant Physiol. 25 : 909-913.
https://doi.org/10.1071/PP98068
 
4. Bai X., Liu J., Tang L., Cai H., Chen M., Ji W., Liu Y., Zhu Y. 2013. Overexpression of GsCBRLK from Glycine soja enhances tolerance to salt stress in transgenic alfalfa (Medicago sativa). Funct. Plant Biol. 40 : 1048-1056.
https://doi.org/10.1071/FP12377
 
5. Bowler C., van Montagu M., Inzé D. 1992. Superoxide dis-mutase and stress tolerance. Ann. Rev. Plant Phys-iol. Plant Mol.Biol. 43 : 83-116.
https://doi.org/10.1146/annurev.pp.43.060192.000503
 
6. Bueno P., Varela J., Gimenez-Gallego G., del Rio L.A. 1995. Peroxisomal copper, zinc superoxide dismutase. Characterization of the isoenzyme from watermelon cotyledons. Plant Physiol. 108 : 1151-1160.
https://doi.org/10.1104/pp.108.3.1151
 
7. Chatzidimitriadou K., Nianiou-Obeidat I., Madesis P., Perl-Treves R. 2009. Expression of SOD transgene in pepper confers stress tolerance and improves shoot re-generation. Electron. J. Biotechnol. 12 (4).
https://doi.org/10.2225/vol12-issue4-fulltext-10
 
8. Cheng Y.J., Deng X.P., Kwak S.S. 2013. Enhanced tolerance of transgenic potato plants expressing choline oxi-dase in chloroplasts against water stress. Bot. Stud. 54 : 30.
https://doi.org/10.1186/1999-3110-54-30
 
9. Choi S.M., Jeong S.W., Jeong W.J., Kwon S., Chow W., Park Y.I. 2002. Chloroplast Cu/Zn-superoxide dismutase is a highly sensitive site in cucumber leaves chilled in the light. Planta. 216 : 315-324.
https://doi.org/10.1007/s00425-002-0852-z
 
10. Cohu C.M., Pilon M. 2007. Regulation of superoxide dis-mutase expression by copper availability. Physiol. Plant. 129 : 747-755.
https://doi.org/10.1111/j.1399-3054.2007.00879.x
 
11. Cui K., Xing G., Liu X., Gengmei X., Yafu W. 1999. Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L.. Plant Sci. 146 : 9-16.
https://doi.org/10.1016/S0168-9452(99)00087-4
 
12. Devi P.S., Satyanarayana B., Arundhati A., Rao T.R. 2013. Activity of antioxidant enzymes and secondary metabolites during in vitro regeneration of Sterculia urens. Biol. Plant. 57 : 778-782.
https://doi.org/10.1007/s10535-013-0337-x
 
13. Diaz-Vivancos P., Barba-Espin G., Clemente-Moreno M.J., Hernandez J.A. 2010.Characterization of the antioxidant system during the vegetative development of pea plants. Biol. Plant. 54 :76-82.
https://doi.org/10.1007/s10535-010-0011-5
 
14. Dong C., Zhang Z., Ren J., Qin Y., Huang J., Wang Y., Cai B., Wang B., Tao J. 2013. Stress-responsive gene ICE1 from Vitis amurensis increases cold tolerance in to-bacco. Plant Physiol.Biochem. 71 : 212-217.
https://doi.org/10.1016/j.plaphy.2013.07.012
 
15. Dugas D.V., Bartel B. 2008. Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol. Biol. 67 : 403-417.
https://doi.org/10.1007/s11103-008-9329-1
 
16. Erdal S., Dumlupinar R. 2011. Mammalian sex hormones stimulate antioxidant system and enhance growth of chickpea plants. Acta Physiol. Plant. 33 : 1011-1017.
https://doi.org/10.1007/s11738-010-0634-3
 
17. Faize M., Faize L., Petri C., Barba-Espin G., Diaz-Vivancos P., Clemente-Moreno M.J., Koussa T., Rifai L.A., Burgos L., Hernandez J.A. 2013. Cu/Zn superoxide dismutase and ascorbate peroxidase enhance in vitro shoot multiplication in transgenic plum. J. Plant Physiol. 170 : 625-632.
https://doi.org/10.1016/j.jplph.2012.12.016
 
18. Farooq M., Basra S.M.A., Wahid A., Cheema Z. A., Cheema M. A., Khaliq A. 2008. Physiological role of ex-ogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). J. Agronomy Crop Sci. 194 : 325-333.
https://doi.org/10.1111/j.1439-037X.2008.00323.x
 
19. Feng W., Hongbin W., Bing L., Jinfa W. 2006. Cloning and characterization of a novel splicing isoform of the iron-superoxide dismutase gene in rice (Oryza sativa L.). Plant Cell Rep. 24 : 734-742.
https://doi.org/10.1007/s00299-005-0030-4
 
20. Fridovich I. 1989.Superoxide dismutases. An adaptation to a paramagnetic gas. J. Biol.Chem. 264 : 7761-7764.
 
21. Giannopolitis C.N., Ries S.K. 1977. Superoxide dismutases. II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol. 59. 315-318.
https://doi.org/10.1104/pp.59.2.315
 
22. Gupta S.A., Webb R.P., Holaday A.S., Allen R.D. 1993. Over-expression 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
 
23. Hasanuzzaman M., Hossain A.M., Teixeira da Silva J.A., Fujita M. 2012. Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. Crop stress and its management: perspectives and strategies (eds.Venkateswarlu B. et al.). Springer Netherlands : 261-315.
https://doi.org/10.1007/978-94-007-2220-0_8
 
24. He S., Han Y., Wang Y., Zhai H., Liu Q. 2009. In vitro selection and identification of sweetpotato (Ipomoea batatas (L.) Lam.) plants tolerant to NaCl. Plant Cell Tiss Organ Cult. 96 : 69-74.
https://doi.org/10.1007/s11240-008-9461-2
 
25. Hosseini M., Maali-Amiri R., Mahfoozi S., Fowler D.B., Mohammadi R. 2016. Developmental regulation of metab-olites and low temperature tolerance in lines of crosses between spring and winter wheat. Acta Physiol Plant. 38 : 87.
https://doi.org/10.1007/s11738-016-2103-0
 
26. Houmani H., Rodríguez-Ruiz M., Palma J.M., Abdelly C., Corpas F.J. 2016. Modulation of superoxide dis-mutase (SOD) isozymes by organ development and high long-term salinity in the halophyte Cakile mari-tima. Protoplasma. 253 : 885-894.
https://doi.org/10.1007/s00709-015-0850-1
 
27. Jackson C., Dench J., Moore A. L., Halliwell B., Foyer C.H., Hall D.O. 1978. Subcellular localisation and iden-tification of superoxide dismutase in the leaves of higher plants. Europ. J. Biochem. 91 : 339-344.
https://doi.org/10.1111/j.1432-1033.1978.tb12685.x
 
28. Jiang J., Su M., Chen Y., Gao N., Jiao C., Sun Z., Li F., Wang C. 2013. Correlation of drought resistance in grass pea (Lathyrus sativus) with reactive oxygen species scavenging and osmotic adjustment. Biologia. 68 : 231-240.
https://doi.org/10.2478/s11756-013-0003-y
 
29. Jung S. 2004. Variation in antioxidant metabolism of young and mature leaves of Arabidopsis thaliana subjected to drought. Plant Sci. 166 : 459-466.
https://doi.org/10.1016/j.plantsci.2003.10.012
 
30. Karimi R., Ershadi A., Nejad A.R., Khanizadeh S. 2016. Abscisic acid alleviates the deleterious effects of cold stress on 'Sultana' grapevine (Vitis vinifera L.) plants by improving the anti-oxidant activity and photosynthetic capacity of leaves. J. Horticult. Sci. Biotechnol. 91 : 386-395.
https://doi.org/10.1080/14620316.2016.1162027
 
31. Karuppanapandian T., Moon J.C., Kim C., Mano-haran K., Kim W. 2011. Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust. J. Crop Sci. 5 : 709-725.
 
32. Khan M.N., Siddiqui M.H., Mohammad F., Naeem M., Khan M.M.A. 2010. Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol. Plant. 32 : 121-132.
https://doi.org/10.1007/s11738-009-0387-z
 
33. Kim M.D., Kim Y.H., Kwon S.Y., Yun D.J., Kwak S.S., Lee H.S. 2010. Enhanced tolerance to methyl viologen-induced oxidative stress and high temperature in transgenic potato plants overexpressing the CuZ-nSOD, APX and NDPK2 genes. Physiol. Plant. 140 : 153-162.
https://doi.org/10.1111/j.1399-3054.2010.01392.x
 
34. Lee Y.P., Ahmad R., Lee H.S., Kwak S.-S., Shafqat M.N., Kwon S.Y. 2013. Improved tolerance of Cu/Zn superoxide dismutase and ascorbate peroxidase expressing transgenic tobacco seeds and seedlings against multiple abiotic stresses. Int. J. Agric. Biol. 15 : 725-730.
 
35. Li C., Han L.B., Zhang X. 2012. Enhanced drought tolerance of tobacco overexpressing OjERF gene is associated with alteration in proline and antioxidant metabolism. J. Amer. Soc. Hort. Sci. 137 : 107-113.
https://doi.org/10.21273/JASHS.137.2.107
 
36. Libik M., Konieczny R., Pater B., Ślesak I., Miszalski Z. 2005. Differences in the activities of some antioxidant enzymes and in H2O2 content during rhizogenesis and somatic embryogenesis in callus cultures of the ice plant. Plant Cell Rep. 23 : 834-841.
https://doi.org/10.1007/s00299-004-0886-8
 
37. Luo J.P., Jiang S.T., Pan L.J. 2001. Enhanced somatic embryogenesis by salicylic acid of Astragalus adsurgens Pall.: relationship with H2O2 production and H2O2-metabolizing enzyme activities. Plant Sci. 161 : 125-132.
https://doi.org/10.1016/S0168-9452(01)00401-0
 
38. Luo X., Wu J., Li Y., Nan Z., Guo X., Wang Y., Zhang A., Wang Z., Xia G., Tian Y. 2013. Synergistic effects of GhSOD1 and GhCAT1 overexpression in cotton chloroplasts on enhancing tolerance to methyl viologen and salt stresses. PLoS ONE. 8 : e54002.
https://doi.org/10.1371/journal.pone.0054002
 
39. Ma L., Xie L., Lin G., Jiang S., Chen H., Li H., Takáč T., Šamaj J., Xu C. 2012. Histological changes and differences in activities of some antioxidant enzymes and hydrogen peroxide content during somatic embryogenesis of Musa AAA cv. Yueyoukang 1. Sci. Hortic. 144 : 87-92.
https://doi.org/10.1016/j.scienta.2012.06.039
 
40. Martinez C.A., Loureiro M.E., Oliva M.A., Maestri M. 2001. Differential responses of superoxide dismutase in freezing resistant Solanum curtilobum and freezing sensitive Solanum tuberosum subjected to oxidative and water stress. Plant Sci. 160 : 505-515.
https://doi.org/10.1016/S0168-9452(00)00418-0
 
41. Martins L.L., Mourato M.P., Cardoso A.I., Pinto A.P., Mota A.M., Gonçalves M.L.S., de Varennes A. 2011. Oxidative stress induced by cadmium in Nicotiana tabacum L.: effects on growth parameters, oxidative damage and antioxidant responses in different plant parts. Acta Physiol. Plant. 33 : 1375-1383.
https://doi.org/10.1007/s11738-010-0671-y
 
42. Matamoros M.A., Loscos J., Dietz K.J., Aparicio-Tejo P.M., Becana M. 2010.Function of antioxidant enzymes and metabolites during maturation of pea fruits. J. Exp. Bot. 61 : 87-97.
https://doi.org/10.1093/jxb/erp285
 
43. McCord J.M., Fridovich I. 1969. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 : 6049-6055.
 
44. 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
 
45. Mittova V., Guy M., Tal M., Volokita M. 2002. Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: increased activities of antioxidant enzymes in root plastids. Free Radic. Res. 36 : 195-202.
https://doi.org/10.1080/10715760290006402
 
46. Mostofa M.G., Hossain M.A., Fujita M. 2015. Trehalose pre-treatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma. 252 : 461-475.
https://doi.org/10.1007/s00709-014-0691-3
 
47. Myouga F., Hosoda C., Umezawa T., Iizumi H., Ku-romori T., Motohashi R., Shono Y., Nagata N., Ikeuchi M., Shinozakia K. 2008. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell. 20 : 3148-3162.
https://doi.org/10.1105/tpc.108.061341
 
48. Nath K., Kumar S., Poudyal R.S., Yang Y.N., Timilsina R., Park Y.S., Nath J., Chauhan P.S., Pant B., Lee C.H. 2014. Developmental stage-dependent differential gene expression of superoxide dismutase isoenzymes and their localization and physical interaction network in rice (Oryza sativa L.). Genes Genomics. 36 : 45-55.
https://doi.org/10.1007/s13258-013-0138-9
 
49. Panda S.K., Khan M.H. 2004. Changes in growth and superoxide dismutase activity in Hydrilla verticillata L. under abiotic stress. Braz. J. Plant Physiol. 16 : 115-118.
https://doi.org/10.1590/S1677-04202004000200007
 
50. Pandey P., Srivastava R.K., Dubey R.S. 2014.Water deficit and aluminum tolerance are associated with a high antioxidative enzyme capacity in Indica rice seedlings. Protoplasma. 251 : 147-160.
https://doi.org/10.1007/s00709-013-0533-8
 
51. Petrić M., Jevremović S., Trifunović M., Tadić V., Mi-lošević S., Subotić A. 2014. Activity of antioxidant enzymes during induction of morphogenesis of Fritil-laria meleagris in bulb scale culture. Turk. J. Biol. 38 : 328-338.
https://doi.org/10.3906/biy-1309-45
 
52. Pilon M., Ravet K., Tapken W. 2011. The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim. Biophys. Acta. Bioenerg. 1807 : 989-998.
https://doi.org/10.1016/j.bbabio.2010.11.002
 
53. Pilon-Smits E.A.H., Ebskamp M.J.M., Paul M.J., Jeuken M.J.W., Weisbeek P.J., Smeekens S.C.M. 1995. Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol. 107 :125-130.
https://doi.org/10.1104/pp.107.1.125
 
54. Qiao G., Zhou J., Jiang J., Sun Y., Pan L., Song H., Jiang J., Zhuo R., Wang X., Sun Z. 2010. Transformation of Liquidambar formosana L. via Agrobacterium tumefaciens using a mannose selection system and recovery of salt tolerant lines. Plant Cell Tiss Organ Cult. 102 : 163-170.
https://doi.org/10.1007/s11240-010-9717-5
 
55. Racchi M.L., Bagnoli F., Balla I., Danti S. 2001. Differential activity of catalase and superoxide dismutase in seedlings and in vitro micropropagated oak (Quercus robur L.). Plant Cell Rep. 20 : 169-174.
https://doi.org/10.1007/s002990000300
 
56. Rasool S., Ahmad A., Siddiqi T.O., Ahmad P. 2013. Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiol Plant. 35 : 1039-1050.
https://doi.org/10.1007/s11738-012-1142-4
 
57. Ribera-Fonseca A., Inostroza-Blancheteau C., Cartes P., Rengel Z., Mora M.L. 2013. Early induction of Fe-SOD gene expression is involved in tolerance to Mn toxicity in perennial ryegrass. Plant Physiol. Biochem. 73 : 77-82.
https://doi.org/10.1016/j.plaphy.2013.08.012
 
58. Sakhno L. 2014. Interferon application causes сanola seedling biomass increase. J. Microbiol. Biotechnol. Food Sci. 3, № 6 : 436-439: http://www.jmbfs.org/wp-content/uploads/2014/05/jmbfs_0612_sakhno.pdf.
 
59. Sakhno L.O. 2015. Adaptive plasticity in osmotic stress of bio-tech canola (Brassica napus L.) possessing cyp11A1 or simultaneously desC and epsps transgenes. Naukovi dopovidi NUBiP. 5 (54) : http://nd.nubip.edu.ua/2015_5/9.pdf.
 
60. Sakhno L.O., Slyvets M.S. 2014. Superoxide dismutase activity in transgenic canola. Cytol. Genet. 48 : 145-149.
https://doi.org/10.3103/S0095452714030104
 
61. Scandalios J.G. 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101 : 7-12.
https://doi.org/10.1104/pp.101.1.7
 
62. Slyvets M., Sakhno L. 2014. Human interferon alpha 2b positively affects сanola growth in both aseptic non-stress and water deficit conditions. Int. J. Biosci. Nanosci. 1 (5) : 104-118. http://ijbsans.com/journal14/oct14/MS-09-14-01_3.pdf.
 
63. Srivastava V., Srivastava M.K., Chibani K., Nilsson R., Rouhier N., Melzer M., Wingsle G. 2009. Alternative splic-ing studies of the reactive oxygen species gene net-work in Populus reveal two isoforms of high-isoelectric-point superoxide dismutase. Plant Physiol. 149 : 1848-1859.
https://doi.org/10.1104/pp.108.133371
 
64. Sultana T., Deeba F., Naz F., Rose R.J., Naqvi S.M.S. 2016. Expression of a rice GLP in Medicago truncatula exerting pleiotropic effects on resistance against Fusarium oxysporum through enhancing FeSOD-like activity. Acta Physiol. Plant. 38 : 255.
https://doi.org/10.1007/s11738-016-2273-9
 
65. Sun W.H., Wang Y., He H.G., Li X., Song W., Du B., Meng Q.W. 2013. Reduction of methyl viologen-mediated oxidative stress tolerance in antisense transgenic to-bacco seedlings through restricted expression of StAPX. J. Zhejiang Univ. Sci. B (Biomed. Biotechnol.). 14 : 578-585.
https://doi.org/10.1631/jzus.B1200190
 
66. Sunkar R., Kapoor A., Zhu J. 2006. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell. 18 : 2051-2065.
https://doi.org/10.1105/tpc.106.041673
 
67. Susuki N., Miller G., Morales J., Shulaev V., Torres M.A., Mittler R. 2011. Respiratory burst oxidases: the engines of ROS signaling. Curr. Opin. Plant Biol. 14 : 691-699.
https://doi.org/10.1016/j.pbi.2011.07.014
 
68. Talukdar D., Talukdar T. 2013. Superoxide-dismutase deficient mutants in common beans (Phaseolus vulgaris L.): genetic control, differential expressions of isozymes, and sensitivity to Arsenic. BioMed Res. Int. Article ID 782450, 11 pages: http://dx.doi.org/10.1155/2013/782450.
https://doi.org/10.1155/2013/782450
 
69. Tewari R.K., Kumar P., Sharma P.N. 2013. Oxidative stress and antioxidant responses of mulberry (Morus alba) plants subjected to deficiency and excess of manganese. Acta Physiol. Plant. 35 : 3345-3356.
https://doi.org/10.1007/s11738-013-1367-x
 
70. Trindade I., Capitão C., Dalmay T., Fevereiro M.P., dos Santos D.M. 2010. miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta. 231 : 705-716.
https://doi.org/10.1007/s00425-009-1078-0
 
71. van Breusegem F., Slooten L., Stassart J.M., Botterman J., Moens T., van Montagu M., Inzé D. 1999. Effects of overproduction of tobacco MnSOD in maize chloroplasts on foliar tolerance to cold and oxidative stress. J. Exp. Bot. 50 : 71-78.
https://doi.org/10.1093/jxb/50.330.71
 
72. Vatankhah E., Niknam V., Ebrahimzadeh H. 2010. Activity of antioxidant enzyme during in vitro organogenesis in Crocus sativus. Biol. Plant. 54 : 509-514.
https://doi.org/10.1007/s10535-010-0089-9
 
73. Vyšniauskiene R., Ranceliene V. 2008. Changes in the activity of antioxidant enzyme superoxide dismutase in Crepis capillaris plants after the impact of UV-B and ozone. Sodininkyste ir Daržininkyste. 27 (2) : 209-214.
 
74. Wang W.B., Kim Y.H., Lee H.S., Deng X.P., Kwak S.S. 2009.Differential antioxidation activities in two alfalfa cultivars under chilling stress. Plant Biotechnol. Rep. 3 : 301-307.
https://doi.org/10.1007/s11816-009-0102-y
 
75. Wang X., Cai J., Liu F., Dai T., Cao W., Wollenweber B., Jiang D. 2014. Multiple heat priming enhances thermotolerance to a later high temperature stress via improving subcellular antioxidant activities in wheat seedlings. Plant Physiol Biochem. 74 : 185-192.
https://doi.org/10.1016/j.plaphy.2013.11.014
 
76. Xu L., Pan Y., Yu F. 2015. Effects of water-stress on growth and physiological changes in Pterocarya stenoptera seedlings. Sci. Hortic-Amsterdam. 190 : 11-23.
https://doi.org/10.1016/j.scienta.2015.03.041
 
77. Yang G., Wang Y., Xia D., Gao C., Wang C., Yang C. 2014. Overexpression of a GST gene (ThGSTZ1) from Tamarix hispida improves drought and salinity tolerance by enhancing the ability to scavenge reactive oxygen species. Plant Cell Tiss Organ Cult. 117 : 99-112.
https://doi.org/10.1007/s11240-014-0424-5
 
78. Yang L., Zhao X., Zhu H., Paul M., Zu Y., Tang Z. 2014. Exogenous trehalose largely alleviates ionic unbalance, ROS burst, and PCD occurrence induced by high salinity in Arabidopsis seedlings. Front. Plant Sci. 5 : 570.
https://doi.org/10.3389/fpls.2014.00570
 
79. Zaefyzadeh M., Quliyev R.A., Babayeva S.M., Abbasov M.A. 2009. The effect of the interaction between genotypes and drought stress on the superoxide dis-mutase and chlorophyll content in durum wheat landraces. Turk. J. Biol. 33 : 1-7.
 
80. Zakharchenko N.S., Buryanov Ya.I., Lebedeva A.A. 2013. Physiological features of rapeseed plants expressing the gene for an antimicrobial peptide cecropin P1. Russ. J. Plant Physiol. 60 : 411-419.
https://doi.org/10.1134/S1021443713030163
 
81. Zaoui S., Gautier H., Bancel D., Chaabani G., Wasli H., Lachaâl M., Karray-Bouraoui N. 2016. Antioxidant pool optimization in Carthamus tinctorius L. leaves under different NaCl levels and treatment durations. Acta Physiol. Plant. 38 : Article 187.
https://doi.org/10.1007/s11738-016-2204-9
 
82. Zhang J., Li D.M., Gao Y., B. Yu B., Xia C.X., Bai J.G. 2012. Pretreatment with 5-aminolevulinic acid mitigates heat stress of cucumber leaves. Biol. Plant. 56 : 780-784.
https://doi.org/10.1007/s10535-012-0136-9
 
83. Zhang L., Xi D., Luo L. Meng F., Li Y., Wu C., Guo X. 2011. Cotton GhMPK2 is involved in multiple signaling pathways and mediates defense responses to pathogen infection and oxidative stress. FEBS J. 278 : 1367-1378.
https://doi.org/10.1111/j.1742-4658.2011.08056.x
 
84. Zhang S., Hu J., Zhang Y., Xie X.J., Knapp A. 2007.Seed priming with brassinolide improves lucerne (Medicago sativa L.) seed germination and seedling growth in relation to physiological changes under sa-linity stress. Austr. J. Agricult. Res. 58 : 811-815.
https://doi.org/10.1071/AR06253
 
85. Zhang X., Wan Q., Liu F., Zhang K., Sun A., Luo B., Sun L., Wan Y. 2015. Molecular analysis of the chloroplast Cu/Zn-SOD gene (AhCSD2) in peanut. Crop J. 3 : 246-257.
https://doi.org/10.1016/j.cj.2015.03.006
 
86. Zhou B., Guo Z. 2009.Calcium is involved in the abscisic acid-induced ascorbate peroxidase, superoxide dismutase and chilling resistance in Stylosanthes guianensis. Biol. Plant. 53 : 63-68.
https://doi.org/10.1007/s10535-009-0009-z
 
87. Zhou L., Wang J., Bi Y., Wang L., Tang L., Yu X., Ohtani M., Demura T., Zhuge Q. 2014. Overexpression of PtSOS2 enhances salt tolerance in transgenic poplars. Plant Mol. Biol. Report. 32 : 185-197.
https://doi.org/10.1007/s11105-013-0640-x