The effect of antimycin A on the intensity of oxidative stress, the level of lipid peroxidation and antioxidant enzyme activities in different organs of wheat (Triticum aestivum L.) seedlings subjected to high temperature

Authors

  • Anna Batjuka Laboratory of Molecular Biology and Genetics, Ecology Department, Institute of Life Sciences and Technology, Daugavpils University
  • Natalja Škute Laboratory of Molecular Biology and Genetics, Ecology Department, Institute of Life Sciences and Technology, Daugavpils University

Keywords:

antimycin A, antioxidant enzymes, high temperature, lipid peroxidation, reactive oxygen species

Abstract

The objective of the present investigation was to identify the effect of antimycin A (AA) as an activator of the alternative pathway (AP) of respiration, on oxidative stress intensity, the level of lipid peroxidation (LPO) and activities of H2O2 scavenging enzymes in functionally different organs of Triticum aestivum L. subjected to short- and long-term exposure to high temperature (HT). The level of LPO was assessed in terms of malondialdehyde (MDA), an indicator of oxidative injury. The results demonstrated increases in the total content of reactive oxygen species (ROS) and MDA production in developing and senescent organs of wheat seedlings, and significant augmentation of the activities of the antioxidant enzymes, catalase and ascorbate peroxidase, in different organs in response to exposure to HT. The activation of the AP by AA restrained ROS production in the mitochondrial electron transport chain (mETC) under exposure to HT.

https://doi.org/10.2298/ABS160706134B

Received: July 6, 2016; Revised: October 31, 2016; Accepted: November 30, 2016; Published online: December 15, 2016

How to cite this article: Batjuka A, Škute N. The effect of antimycin A on the intensity of oxidative stress, the level of lipid peroxidation and antioxidant enzyme activities in different organs of wheat (Triticum aestivum L.) seedlings subjected to high temperature. Arch Biol Sci. 2017;69(4):743-52.

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Author Biographies

Anna Batjuka, Laboratory of Molecular Biology and Genetics, Ecology Department, Institute of Life Sciences and Technology, Daugavpils University

Ecology department

Natalja Škute, Laboratory of Molecular Biology and Genetics, Ecology Department, Institute of Life Sciences and Technology, Daugavpils University

Ecology department

References

Attri SD, Rathore LS. Simulation of impact of projected climate change on wheat in India. Int J Climatol. 2003;23:693-705.

Mittler R. Oxidative stress, antioxidant and stress tolerance. Trends Plant Sci. 2002;7:405-10.

Ibrahim MM, Alsahli AA, Ghamdi AL. Cumulative abiotic stresses and their effect on the antioxidant defense system in two species of wheat, Triticum durum Desf and Triticum aestivum L. Arch Biol Sci. 2013;65(4):1423-33.

Mavi HS, Tupper GT. Agrometeorology: principles and applications of climate studies in agriculture. 1st ed. New York, London, Oxford:Haworth Press; 2004. 43-68 p.

Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. 2012;1:1-26.

Miller G, Suzuki N, Ciftci-Yilmaz S, Mitler R. Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ. 2010;33:453-67.

Pérez-Pérez ME, Lemaire SD, Crespo JL. Reactive oxygen species and autophagy in plants and algae. Plant Physiol. 2012;160:156-64.

Stowe DF, Camara AKS. Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function. Antioxid Redox Sign. 2009;11(6):1373-1414.

Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance to crop plants. Plant Physiol Biochem. 2010;48:909-30.

Mittler R, Vanderauwera S, Gollery M, Breusegem FV. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490-98.

Laus MN, Soccio M, Trono D, Liberatore MT, Pastore D. Activation of the plant mitochondrial potassium channel by free fatty acids and acyl-CoA esters: a possible defence mechanism in the response to hyperosmotic stress. J Exp Bot. 2011;62(1):141-54.

Juszczuk IM, Rychter AM. Alternative oxidase in higher plants. Acta Biochim Pol. 2003;50(4):1257-71.

Jarmuszkiewicz W, Woyda-Ploszczyca A, Antos-Krzeminska N, Sluse FE. Mitochondrial uncoupling proteins in unicellular eukaryotes. Biochim Biophys Acta 2010;1797:792-99.

Kolesnichenko AV, Pobezhimova TP, Grabelnych OI, Tourchaninova VV, Korzun AM, Koroleva NA, Zykova VV, Voinikov V.K. Difference between the temperature of non-hardened and hardened winter wheat seedling shoots during cold stress. J Therm Biol. 2003;28:235-44.

Tripathy BC, Oelmüller R. Reactive oxygen species generation and signalling in plants. Plant Sign Behav. 2012;7(12):1621-33.

Scheibe R., Backhausen JE, Emmerlich V., Holtgrefe S. Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot. 2005;56(416):1481-89.

Batjuka A, Škute N, Petjukevičs A. The influence of antimycin A on pigment composition and functional activity of photosynthetic apparatus of Triticum aestivum L. under high temperature. Photosynthetica. 2016; 54:1-14.

Taira Y, Okegawa Y, Sugimoto K, Abe M, Miyoshi H, Shikanai T. Antimycin A-like molecules inhibit cyclic electron transport around photosystem I in ruptured chloroplasts. FEBS Open Bio. 2013;3:406‒410.

Slane B. Antimycin: the big chain blocker. Free Radical Bio Med. 2003;77:1-10.

Wagner AM. A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrid cells. FEBS Lett. 1995;368:339-42.

Maxwell DP, Wang Y, McIntosh L. The alternative oxidase lowers mitochondria reactive oxygen production in plant cells. P Natl Acad Sci USA. 1999;96:8271-76.

Zhu H, Bannenberg GL, Moldéus P, Shertzer HG. Oxidation pathways for the intracellular probe 2’,7’-dichlorofluorescein. Arch Toxicol. 1994;68(9):582-87.

Ali MB, Hahn EJ, Paek KY. Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. Environ Exp Bot. 2005;54:109-20.

Aebi H. Catalase in vitro. Meth Enzymol. 1984;105:121-26.

Johnson LB, Cunningham BA. Peroxidase activity in healthy and leaf-rust-infected wheat leaves. Phytochemistry. 1972;11:547-51.

Hasanuzzaman M, Nahar K, Alam M.M, Roychowdhury R, Fujita M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants Int J Mol Sci. 2013;14:9643-84.

Rhoads DM, Umbach AL, Subbaiah CC Siedow IN. Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signalling. Plant Physiol. 2006;141:357-66.

Lee RH, Chen SCG. Programmed cell death during rice leaf senescence is nonapoptotic. New Phytol. 2002;155:25-32.

Fedyaeva AV, Stepanov AV, Lyubushkina IV, Pobezhimova TP, Rikhvanov EG. Heat shock induces production of reactive oxygen species and increases inner mitochondrial membrane potential in winter wheat cells. Biochem (Mosc) Suppl Ser A Membr Cell Biol. 2014;79:1202-10.

Volkov RA, Panchuk II, Mullineaux PM, Schöffl F. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol. 2006;61:733-46.

Chen W, Cen W, Chen L, Di L, Li Y, Guo W. Differential sensitivity of four highbush blueberry (Vaccinium corymbosum L.) cultivars to heat stress. Pak J Bot. 2012;44:853-60.

Pastore D, Trono D, Laus MN, Fonzo ND, Flagella Z. Possible plant mitochondria involvement in cell adaptation to drought stress. A case study: durum wheat mitochondria. J Exp Bot. 2007;58(2):195-210.

Strodtkötter I, Padmasree K, Dinakar C, Speth B. Niazi PS, Wojtera J, Voss I, Do PT, Nunes-Nesi A, Fernie AR, Linke V, Raghavendra AS, Schreibe R. Induction of the AOX1D isoform of alternative oxidase in A. thaliana T-DNA insertion lines lacking isoform AOX1A is insufficient to optimize photosynthesis when treated with antimycin A. Mol Plant. 2009;2(2):284-97.

Umbach AL, Fiorani F, Siedow JN. Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol. 2005;139(4):1806-20.

Shorning BY, Smirnova EG, Yaguzhinsky LS, Vanyushin BF. Necessity of superoxide production for development of etiolated wheat seedlings. Biochem (Mosc) Suppl Ser A Membr Cell Biol. 2000;65:1357-61.

Zamyatnina VA, Bakeeva LE, Alekandrushkina NI, Vanyushin BF. Apoptosis in the initial leaf of etiolated wheat seedlings: influence of the antioxidant ionol (BHT) and peroxides. Biochem (Mosc) Suppl Ser A Membr Cell Biol. 2002;67(2):212-21.

Savicka M, Škute N. Effects of high temperature on malondialdehyde content, superoxide production and growth changes in wheat seedlings (Triticum aestivum L.). Ekol (Liet Moksl Akad (Spausd)). 2010;56:26-33.

Vanlerberghe GC. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci. 2013;14:6805-47.

Zentgraf U, Zimmermann P, Smykowski A. Role of intracellular hydrogen peroxide as signaling molecule for plant senescence. In: Nagata T, editor. Senescence. Rijeka, Croatia: In-Tech; 2012. p. 31-43.

Vanlerberghe GC, Robson CA, Yip JYH. Induction of mitochondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol. 2002;129:1829-42.

Carol RJ, Dolan L. The role of reactive oxygen species in cell growth: lessons from root hair. J Exp Bot. 2006;57(8):1829-34.

Kolupaev YY, Karpets YV, Kosakivska IV. The importance of reactive oxygen species in the induction of plant resistance to heat stress. Gen Appl Plant Physiol. 2008;34:251-66.

Dixit V, Pandey V, Shyam R. Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L., cv. Azad) root mitochondria. Plant Cell Environ. 2002;25:687-93.

Grabel’nykh OI, Pobezhimova TP, Pavlovskaya NS, Koroleva NA, Borovik OA, Lyubushkina IV, Voinikov VK. Antioxidant function of alternative oxidase in mitochondria of winter wheat during cold hardening. Biochem (Mosc) Suppl Ser A Membr Cell Biol. 2011;5:249-57.

Zhao X, Nishimura Y, Fukumoto Y, Li J. Effect of high temperature on active oxygen species, senescence and photosynthetic properties in cucumber leaves. Environ Exp Bot. 2011;70:212-16.

Song Y, Chen Q, Ci D, Shao X, Zhang D. Effects of high temperature on photosynthesis and related gene expression in poplar. BMC Plant Biol. 2014;14:1-20.

Liu X, Huang B. Changes in fatty acid composition and saturation in leaves and roots of creeping bentgrass exposed to high soil temperature. J Am Soc Hortic Sci. 2004;129(6):795-801.

Wang J, Rajakulendran N, Amirsadeghi S, Vanlerberghe GC. Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol Plantarum. 2011;142:339-51.

Sofo A, Scopa A, Nuzzaci M, Vitti A. Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 2015;16:13561-78.

Sairam RK, Saxena DC. Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. J Agron Crop Sci. 2000;184:55-61.

Navabpour S, Morris K, Allen R, Harrison E, Mackerness SAH, Buchanan-Wollaston V. Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot. 2003;54(391):2285-92.

Kang HM, Saltveit ME. Activity of enzymatic antioxidant defense systems in chilled and heat shocked cucumber seedling radicles. Physiol Plantarum. 2001;113:548-56.

Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP. Protective role of antioxidant enzymes under high temperature stress. Plant Sci. 2006;171:382-88.

Antal TK, Kukarskikh GP, Bulychev AA, Tyystjärvi E, Krendeleva T. Antimycin A effect on the electron transport in chloroplasts of two Chlamydomonas reinhardtii strains. Planta. 2013;273:1241-50.

Shikanai T. Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol. 2007;58:199-217.

Dertinger U, Schaz U, Schulze E.D. Age-dapendence of the antioxidative system in tobacco with enhanced glutathione reductase activity or senescence-induced production of cytokinins. Physiol Plantarum. 2003;119:19-23.

Veljovic-Jovanovic S, Kukavica B, Stevanovic B, Navari-Izzo F. Senescence- and drought-related changes in peroxidase and superoxide dismutase isoforms in leaves of Ramonda serbica. J Exp Bot. 2006;57(8):1759-68.

Scheller HV. In vitro cyclic electron transport in barley thylakoids follows two independent pathways. Plant Physiol. 1996;110:187-194.

Joët T, Cournac L, Horvath EM. Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol. 2001;125:1919-29.

Igamberdiev AU, Stoimenova M, Seregélyes C, Hill RD. Class-I hemoglobin and antioxidant metabolism in alfalfa roots. Planta 2005;223(5):1041-46.

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Published

2017-10-18

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Batjuka A, Škute N. The effect of antimycin A on the intensity of oxidative stress, the level of lipid peroxidation and antioxidant enzyme activities in different organs of wheat (Triticum aestivum L.) seedlings subjected to high temperature. Arch Biol Sci [Internet]. 2017Oct.18 [cited 2022Jul.1];69(4):743-52. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/808

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