Visn. Hark. nac. agrar. univ., Ser. Biol., 2017, Issue 3 (42), с. 52-61


Yu. V. Karpets

V.V. Dokuchaev Kharkiv National Agrarian University
(Kharkiv, Ukraine)

The participation of calcium ions and reactive oxygen species (ROS) in the induction of enzymatic antioxidative system of wheat (Triticum aestivum L.) coleoptiles and their resistances to the damaging heating by nitric oxide donor sodium nitroprusside (SNP) with the use of inhibitory method have been investigated. Treatment of coleoptiles with SNP in concentration of 0,1 and 0,2 mM in the greatest measure induced their resistance to the damaging heating. Under the influence of SNP there was the increase in activity of superoxide dismutase, catalase, guaiacol peroxidase and ascorbate peroxidase in coleoptiles. Antioxidant butylhydroxytoluene, inhibitor of NADPH-oxidase imidazole, chelator of external calcium EGTA, inhibitor of phospholipase C neomycin and inhibitor of ADP-ribosyl cyclase nicotinamide partially eliminated the SNP influence on the activity of antioxidant enzymes. Also these compounds levelled the effect of increase in heat resistance of wheat coleoptiles caused by SNP. The conclusion about the influence of exogenous nitric oxide, mediated by calcium and ROS, on the antioxidative system and heat resistance of wheat coleoptiles is made.

Key words: Triticum aestivum, nitric oxide, antioxidant enzymes, reactive oxygen species, calcium, NADPH-oxidase, heat resistance



1. Glyan'ko A. K., Ischenko O. O., Mitanova N. B., Vasil'eva G. G. 2009. Plants NADPH-oxidase. Visn. Hark. nac. agrar. univ., Ser. Biol. 2(17) : 6-18.
2. Karpets Yu.V., Kolupaev Yu.E., Lugovaya A.A., Oboznyi A.I. 2014. Effect of jasmonic acid on the pro-/antioxidant system of wheat coleoptiles as related to hyperthermia tolerance. Russ. J. Plant Physiol. 61(3) : 339-346.
3. Karpets Yu.V., Kolupaev Yu.E., Oboznyi O.I., Yastreb T.O. 2015. Influence of calcium antagonists on generation of reactive oxygen species induced by NO donor and development of heat resistance of wheat coleoptiles. Fiziol. rast. genet. 47(4) : 338-346.
4. Karpets Yu.V., Kolupaev Yu.E. 2017. Functional interaction of nitric oxide with reactive oxygen species and calcium ions at development of plants adaptive responses. Visn. Hark. nac. agrar. univ., Ser. Biol. 2(41) : 6-31.
5. Karpets Yu.V., Kolupaev Yu.E., Yastreb T.O. 2011. Effect of sodium nitroprusside on heat resistance of wheat coleoptiles: Dependence on the formation and scavenging of reactive oxygen species. Russ. J. Plant Physiol. : 58(6) : 127.
6. Karpets Yu.V., Kolupaev Yu.E., Shvidenko M.V., Dmitriev O.P. 2011. Effects of exogenous nitric oxide (NO) on the generation of superoxide anion-radical and heat resistance of wheat coleoptiles. Rep. Natl. Acad. Sci. Ukraine. 9 : 147-152.
7. Kolupaev Yu.Ye., Karpets Yu.V., Musatenko L.I. 2009. Calcium-dependent influence of salicylic acid and hydrogen peroxide on the superoxide dismutase activity of wheat coleoptiles. Rep. Natl. Acad. Sci. Ukraine. 9 : 165-169.
8. Kolupaev Yu.E. 2016. Plant cell antioxidants and their role in ros signaling and plant resistance. Uspekhi Sovrem. Biologii. 136(2) : 181-198.
9. Minibaeva F.V., Gordon L.Kh. 2003. Superoxide production and the activity of extracellular peroxidase in plant tissues under stress conditions. Russ. J. Plant Physiol. : 50(3) 411-416.
10. Shorning B.Yu., Smirnova E.G., Yaguzhinsky L.S., Vanyushin B.F. 2000. Necessity of Superoxide Production for Development of Etiolated Wheat Seedlings. Biochemistry (Mosc.). 65(12) : 1357-1361.
11. Allen G.J., Muir S.R., Sanders D. 1995. Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose. Science. 268 : 735-737.
12. 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.
13. Bajguz A. 2014. Nitric Oxide: role in plants under abiotic stress. In: Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment (Eds. Ahmad P., Wani M.R.). New York : Springer Science+Business Media, vol. 2, pp. 137-159.
14. Begara-Morales J.C., Chaki M., Sanchez-Calvo B., Ma-ta-Pérez C., Leterrier M., Palma J.M., Barroso J.B., Corpas F.J. 2013. Protein tyrosine nitration in pea roots during development and senescence. J. Exp. Bot. 64 : 1121-1142.
15. Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein uti-lizing the principle of protein-dye binding. Anal. Biochem. 72 : 248-254.
16. Chaki M., Valderrama R., Fernandez-Ocana A.M., Carreras A., Lopez-Jaramillo J., Luque F., Palma J.M., Pedrajas J.R., Begara-Morales J.C., Sanchez-Calvo B., Gomez-Rodriguez M.V., Corpas F.J., Barroso J.B. 2009. Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J. Exp. Bot. 60 : 4221-4236.
17. Corpas F.J., Leterrier M., Valderrama R., Airaki M., Chaki M., Palma J.M., Barroso J.B. 2011. Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci. 181 : 604-611.
18. Fares A., Rossignol M., Peltier J.B. 2011. Proteomics investi-gation of endogenous S-nitrosylation in Arabidopsis. Biochem. Biophys. Res. Commun. 416 : 331-338.
19. Gaber A., Yoshimura K., Yamamoto T., Yabuta Y., Takeda T., Miyasaka H., Nakano Y., Shigeoka S. 2006. Glutathione peroxidase-like protein of Synechocyst-is PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis. Physiol Plant. 128 : 251-262.
20. Gill S.S., Tuteja N. 2010. Reactive oxygen species and antiox-idant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48 : 909-930.
21. Hamed S.M., Zinta G., Klöck G., Asard H., Selim S., AbdElgawad H. 2017. Zinc-induced differential oxidative stress and antioxidant responses in Chlorella soro-kiniana and Scenedesmus acuminatus. Ecotoxic. Environ. Saf. 140 : 256-263.
22. Hu X., Jiang M., Zhang J., Zhang A., Lin F., Tan M. 2007. Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both up-stream and downstream of of H2O2 production in leaves of maize (Zea mays) plants. New Phytol. 173 : 27-38.
23. Hung K.T., Hsu Y.T., Kao C.H. 2006. Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol. Plant. 127 : 293-303.
24. Jeandroz S., Lamotte O., Astier J., Rasul S., Trapet P., Besson-Bard A., Bourque S. Nicolas-Frances V., Berkowitz G.A., Wendehenne D. 2013. There's more to the picture than meets the eye: nitric oxide cross talk with Ca2+ Plant Physiol. 163 : 459-470.
25. Khan M.N., Mobin M., Abbas Z.K. 2015. Nitric oxide and high temperature stress: a physiological perspective. In: Nitric oxide action in abiotic stress responses in plants (Eds. Khan M.N., Mobin M., Mohammad F., Corpas F.J.). Heidelberg, New York, Dordrecht, London, pp. 77-94.
26. Leckie C.P., Mcainsh M.R., Allen G.J., Sanders D., Hetherington A.M. 1998. Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc Natl Acad Sci USA 95: 15837-15842.
27. Lecourieux D., Mazars C., Pauly N., Ranjeva R., Pugin A. 2002. Analysis and effects of cytosolic free calcium in-creases in response to elicitors in Nicotiana plum-baginifolia cells. Plant Cell. 14 : 2627-2641
28. Lee Y., Lee Y. 2008. Roles of phosphoinositides in regulation of stomatal movements. Plant Signal. Behav. 3 : 211-213.
29. Lin C.C., Jih P.J., Lin H.H., Lin J.S., Chang L.L., Shen Y.H., Jeng S.T. 2011.Nitric oxide activates superox-ide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol. Biol. 77 : 235-249.
30. Liu H.T., Huang W.D., Pan Q.H., Weng F.H., Zhan J.C., Liu Y., Wan S.B., Liu Y.Y. 2006.Contributions of PIP2-specific-phospholipase C and free salicylic acid to heat acclimation induced thermotolerance in pea leaves. J. Plant. Physiol. 163 :405-416.
31. Lozano-Juste J., Leon J. 2011. Nitric oxide regulates DELLA content and PIF expression to promote photomor-phogenesis in Arabidopsis. Plant Physiol. 156 : 1410-1423.
32. Mur L.A.J., Mandon J., Persijn S., Cristescu S.M., Moshkov I.E., Novikova G.V., Hall M.A., Harren F.J.M., Hebelstrup K.H., Gupta K.J. 2013. Nitric oxide in plants: an assessment of the current state of knowledge . AoB Plants. 5. Pls052.
33. Oz M.T., Eyidogan F., Yucel M., Oktem H.A. 2015. Functional role of nitric oxide under abiotic stress conditions. In: Nitric oxide action in abiotic stress responses in plants (Eds. M.N. Khan, M. Mobin, F. Mohammad, F.J. Corpas). Heidelberg, New York, Dordrecht, London, pp. 21-42.
34. Song L., Ding W., Zhao M., Sun B., Zhang L. 2006. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci. 171 : 449-458.
35. Tewari R.K., Hahn E.J., Paek K.Y. 2008. Function of nitric oxide and superoxide anion in the adventitious root development and antioxidant defence in Panax ginseng. Plant Cell Rep. 27 : 563-573.
36. Vital S.A., Fowler R.W., Virgen A., Gossett D.R., Banks S.W., Rodriguez J. 2008.Opposing roles for super-oxide and nitric oxide in the NaCl stress-induced up-regulation of antioxidant enzyme activity in cotton callus tissue. Environ. Exp. Bot. 62 : 60-68.
37. Zhang A., Jiang M., Zhang J., Ding H., Xu S., Hu X., Tan M. 2007. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mi-togen-activated protein kinase cascade involved in antioxidant defense in maize leave. New Phytol. 175 : 36-50.
38. Zhang L., Zhou S., Xuan Y., Sun M., Zhao L. 2009. Protective effect of nitric oxide against oxidative damage in Arabidopsis leaves under ultraviolet-B irradiation. J. Plant Biol. 52 : 135-140.