Comparison of Cold-hardiness Levels of Wheat Cultivars Based on Alterations in Alternative Oxidase Protein Level

Abstract

Plant mitochondrial electron transport chain consists of two terminal oxidases: the cytochrome oxidase (COX) and alternative oxidase (AOX). AOX pathway is known to be alternative respiration or cyanide-resistant respiration and linked to stress tolerance of plants. This study aimed to assess cold-hardening levels of four different cultivars of wheat by comparing alterations in protein levels of alternative oxidase, which is responsible for alternative respiration. The AOX protein levels of Yıldırım and Dogu-88 cultivars were markedly higher than those of Ayyıldız and Alpaslan cultivars in control conditions, which indicate that alternative respirations of Yıldırım and Dogu-88 cultivars are more active than those of the other cultivars. Cold stress resulted significant increases AOX protein levels of all cultivars in comparison to their controls. The increases rates were 47, 34, 31, and 70% in Yıldırım, Doğu-88, Ayyıldız, and Alpaslan cultivars, respectively. These findings revealed that although all cultivars tried to resist to cold stress by improving their alternative respirations, Yıldırım and Dogu-88 cultivars are more tolerant to cold stress than the other cultivars.

Keywords

• Alternative oxidase,cold stress,wheat,immuno-blot analysis

Supporting Institution

Atatürk Üniversitesi

Project Number

2012-1326

Thanks

This work was supported by a grant from the research funds appropriated to Ataturk University, Erzurum, Turkey (2012-1326).

References

1. ANDERSSON, M.E., & NORDLUND, P. 1999, A revised model of the active site of alternative oxidase. Febs Lett., 449(1): 17-22.
2. BENDALL, D.S., & BONNER, W.D. 1971, Cyanide-insensitive respiration in plant mitochondria. Plant Physiol., 47(2): 236-245.
3. BRADFORD, M.M. 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem., 72: 248-254. CAKMAK, T., DUMLUPINAR, R., ERDAL, S. 2010, Chilling resistance of Phaseolus vulgaris and Brassica oleracea under a high-intensity electric field. Zeitschrift Fur Naturforschung Section C-a Journal of Biosciences., 65(5-6): 380-386.
4. CHIEN, L.F., WU, Y.C., CHEN, H.P. 2011, Mitochondrial energy metabolism in young bamboo rhizomes from Bambusa oldhamii and Phyllostachys edulis during shooting stage. Plant Physiology and Biochemistry., 49(4): 449-457.
5. CVETKOVSKA, M., & VANLERBERGHE, G.C. 2012, Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol., 195(1): 32-39.
6. ELTHON, T.E., NICKELS, R.L., MCINTOSH, L. 1989, Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol., 89:1311-1317.
7. ERDAL, S. 2012, Androsterone-induced molecular and physiological changes in maize seedlings in response to chilling stress. Plant Physiology and Biochemistry., 57: 1-7.
8. ERDAL, S., & GENISEL M. 2016, The property of progesterone to mitigate cold stress in maize is linked to a modulation of the mitochondrial respiratory pathway. Theoretical and Experimental Plant Physiology., 28(4): 385-393.

9. ERDAL, S., GENISEL, M., TURK, H., DUMLUPINAR, R., DEMIR, Y. 2015, Modulation of alternative oxidase to enhance tolerance against cold stress of chickpea by chemical treatments. J Plant Physiol., 175: 95-101.
10. FOWLER, D.B., LIMIN, A.E., WANGS, Y., WARD, R.W., 1995. Relationship between low temperature tolerance and vernalization response in wheat and rye. Can J. Plant Sci., 76: 37-42.
11. GENISEL, M., TURK, H., ERDAL, S. 2013, Exogenous progesterone application protects chickpea seedlings against chilling-induced oxidative stress. Acta Physiol Plant., 35(1): 241-251.
12. KOBAYASHI, F., TAKUMI, S., NAKATA, M., OHNO, R., NAKAMURA, T., NAKAMURA, C., 2004. Comparative study of the expression profiles of the Cor/Lea gene family in two wheat cultivars with contrasting levels of freezing tolerance. Physiol. Plantarum., 120(4):585-594.
13. LAEMMLI, U..K 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature., 227(5259): 680-685.
14. LAMBOWITZ, A.M., SABOURIN, J.R., BERTRAND, H., NICKELS, R., MCINTOSH, L. 1989, Immunological identification of the alternative oxidase of Neurospora crassa mitochondria. Mol Cell Biol., 9(3): 1362-1364.
15. MAXWELL, D.P., WANG, Y., MCINTOSH, L. 1999, The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences of the United States of America., 96(14): 8271-8276.
16. MAY, B.G., YOUNG, L.E., MOORE, A.L. 2017, Structural insights into the alternative oxidases: are all oxidases made equal? Biochemical Society transactions. 45(3): 731-740.
17. MEEUSE, B.J.D. 1975, Thermogenic respiration in aroids. Annual Reviews in Plant Physiology., 26: 117-126.
18. NOBUYUKI, M., ATSUSHI, S., FUMINORI, K., SHIGEO, T. 2008, Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat. Journal of Plant Physiology., 165:462-467
19. PLUMMER, D.T. 1980, Assay methods., In Plummer DT ed, An introduction to practical biochemistry, Ed, Vol British Library, London pp 119-159.
20. PURVIS, A.C., & SHEWFELT, R.L. 1993, Does the alternative pathway ameliorate chilling injury in sensitive plant-tissues. Physiol Plantarum., 88(4): 712-718.
21. SCHONBAUM, G.S., BONNET, W.D.J., STOREY, B.T., BAHR, J.T., 1971, Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiol., 47: 124-128.
22. SIEDOW, J.N., & MOORE, A.L. 1993, A kinetic model for the regulation of electron transfer through the cyanide-resistant pathway in plant mitochondria. Biochim. Biophys. Acta., 1142:165-174.
23. SIEDOW, J.N., UMBACH, A.L., MOORE, A.L. 1995, The active site of the cyanide-resistant oxidase from plant mitochondria contains a coupled binuclear iron center. FEBS Lett., 362: 10-14.
24. SIEDOW, J.N., & UMBACH, A.L. 1995, Plant mitochondrial electron transfer and molecular biology. The Plant Cell., 7:821-831.
25. THOMASHOW, M.F. 1999, Plant cold acclimation. Ann. Rev. Plant Physiol.,50:571-599.
26. TOWBIN, H., STAEHELIN, T., GORDON, J. 1979, Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci., 76(9):4350-4354.
27. TURK, H. 2019, Chitosan-induced enhanced expression and activation of alternative oxidase confer tolerance to salt stress in maize seedlings. Plant Physiol Biochem., 141: 415-422.
28. TURK, H., & ERDAL, S. 2015, Melatonin alleviates cold-induced oxidative damage in maize seedlings by up-regulating mineral elements and enhancing antioxidant activity. Journal of Plant Nutrition and Soil Science., 178(3): 433-439.
29. TURK, H., ERDAL, S., DUMLUPINAR, R. 2019, Carnitine-induced physio-biochemical and molecular alterations in maize seedlings in response to cold stress. Archives of Agronomy and Soil Science, https://doi.org/10.1080/03650340.2019.1647336.
30. TURK, H., ERDAL, S., GENISEL, M., ATICI, O., DEMIR, Y., YANMIS, D. 2014, The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regulation., 74(2): 139-152.
31. WANG, J., RAJAKULENDRANA, N., AMIRSADEGHIA, S., VANLERBERGHEA, G.C., 2011, Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiologia Plantarum., 142:339-351.
32. WATLING, J.R., ROBINSON, S.A., SEYMOUR, R.S. 2006, Contribution of the alternative pathway to respiration during thermogenesis in flowers of the sacred lotus. Plant Physiology., 140: 1367-1373.
33. VANLERBERGHE, G.C., & MCINTOSH, L. 1992, Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol., 100(1): 115-119.
34. VAN HERK, A.W.H. 1937, Die chemischen vorgange im Sauromatum-Kolben. II. Mitteilung, Proc. Kon. Ned. Akad. Wet., 34(1):69-156.