Current Science

Open Access Open Access  Restricted Access Subscription Access

Evaluation of Superoxide Anion Level and Membrane Permeability in the Functionally Different Organs of Triticum aestivum L. Exposed to High Temperature and Antimycin A


Affiliations
1 Laboratory of Molecular Biology and Genetics, Department of Ecology, Institute of Life Sciences and Technology, Daugavpils University, Parades Str.1a, Daugavpils, Latvia, LV-5401, Latvia
 

The impact of antimycin A (AA) as an activator of the alternative respiratory pathway (AP) on the rate of superoxide anion (O•2¯) generation and membrane permeability was studied in the functionally different organs of wheat seedlings (Triticum aestivum L.) following short-term and long-term high temperature (HT). The results indicated a significant increase in the O•2¯ generating rate in etiolated wheat seedlings and seedlings grown under normal daylight regime following short-term (8%–37%) and long-term (13%– 65%) HT depending on the stage of development. The damages induced by HT were related to the permeability of membranes in the functionally different organs of wheat seedlings. However, our results demonstrated that increase in the O•2¯ generating rate in etiolated wheat seedlings was significantly lower following the combined effect of AA and HT, than under stressful conditions without AA. Taken together, our observations show that the induction of AP, provoked by AA, prevents over-reduction of the mitochondrial electron transport chain, alleviating reactive oxygen species formation and protecting the etiolated wheat seedlings against oxidative damage.

Keywords

Antimycin A, High Temperature, Membrane Permeability, Superoxide Anion, Triticum aestivum L.
User
Notifications
Font Size

  • Bita, C. E. and Gerats, T., Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front. Plant Sci., 2013, 4, 1–18.

  • Wahid, A., Gelani, S., Ashraf, M. and Foolad, M. R., Heat tolerance in plants: an overview. Environ. Exp. Bot., 2007, 61, 199– 223.

  • Hasanuzzaman, M., Nahar, K., Alam, M., Roychowdhury, R. and Fujita, M., Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci., 2013, 14, 9643– 9684.

  • Vanlerberghe, G. C., Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signalling homeostasis during abiotic and biotic stress in plants. Int. J. Mol. Sci., 2013, 14, 6805–6847.

  • Grabelnych, O. I. et al., 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.), 2014, 79, 506–519.

  • Slane, B., Antimycin: the big bad chain blocker. Free Radic. Biol. Med., 2003, 77, 1–10.

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

  • Vanlerberghe, G. C. and McIntosh, L., Coordinate regulation of cytochrome and alternative pathway respiration in tobacco. Plant Physiol., 1992, 100, 1846–1851.

  • Maxwell, D. P., Nickels, R. and McIntosh, L., Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J., 2002, 29, 269–279.

  • Strodtkötter, I. et al., 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, 284–297.

  • Batjuka, A., Škute, N. and Petjukevičs, A., The influence of antimycin A on pigment composition and functional activity of photosynthetic apparatus in Triticum aestivum L. under high temperature. Photosynthetica, 2017, 55(2), 251–263.

  • Shorning, B. Y., Smirnova, E. G., Yaguzhinsky, L. S. and Vanyushin, B. F., Necessity of superoxide production for development of etiolated wheat seedlings. Biochemistry (Moscow), 2000, 65, 1357–1361.

  • Guo, Z., Ou, W., Lu, S. and Zhong, Q., Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol. Biochem., 2006, 44, 828– 836.

  • Grabel’nykh, O. I., Pobezhimova, T. P., Pavlovskaya, N. S., Koroleva, N. A., Borovik, O. A., Lyubushkina, I. V. and Voinikov, V. K., Antioxidant function of alternative oxidase in mitochondria of winter wheat during cold hardening. Biochemistry (Moscow) Suppl. Ser. A, 2014, 5, 249–257.

  • Lyubushkina, I. V., Fedyaeva, A. V., Pobezhimova, T. P., Stepanov, A. V. and Rikhvanov, E. G., Activation of cell death in the sugar cane suspension culture by the exposure to high temperature. J. Stress Physiol. Biochem., 2014, 10, 13–24.

  • Sharma, P., Jha, A. B., Dubey, R. S. and Pessarakli, M., Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot., 2012, 1, 26.

  • Apel, K. and Hirt, H., Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol., 2004, 55, 373–399.

  • Gill, S. S. and Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem., 2010, 48, 909–930.

  • Fedyaeva, A. V., Stepanov, A. V., Lyubushkina, I. V., Pobezhimova, T. P. and Rikhvanov, E. G., Heat shock induces production of reactive oxygen species and increases inner mitochondrial membrane potential in winter wheat cells. Biochemistry (Moscow) Suppl. Ser. A, 2014, 79, 1202–1210.

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

  • Sairam, R. K. and Tyagi, A., Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci., 2004, 86, 407– 421.

  • Lee, R. H. and Chen, S. C. G., Programmed cell death during rice leaf senescence is nonapoptotic. New Phytol., 2002, 155, 25–32.

  • Roach, T. and Krieger-Liszkay, A., Regulation of photosynthetic electron transport and photoinhibition. Curr. Protein Pept. Sci., 2014, 15, 351–362.

  • Maxwell, D. P., Wang, Y. and McIntosh, L., The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA, 1999, 96, 8271–8276.

  • Dufour, E., Boulay, J., Rincheval, V. and Sainsard-Chanet, A., A causal link between respiration and senescence in Podospora anserina. Proc. Natl. Acad. Sci. USA, 2000, 97, 4138–4143.

  • Grabelnych, O. I. et al., 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., 2011, 7, 446–456.

  • Geisler, D. A., Johansson, F. I., Svensson, Å. S. and Rasmusson, A. G., Antimycin A treatment decreases respiratory internal rotenoneinsensitive NADH oxidation capacity in potato leaves. BMC Plant Biol., 2004, 4, 1–10.

  • Yoshida, K., Terashima, I. and Noguchi, K., Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol., 2007, 48, 606– 614.

  • Cvetkovska, M. and Vanlerberghe G. C., Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ., 2013, 36, 721–732.

  • Zentgraf, U., Zimmermann, P. and Smykowski A., Role of intracellular hydrogen peroxide as signalling molecule for plant senescence. In Senescence (ed. Nagata, T.), Intech Open, 2012, pp. 31–50.

  • Al-Jebory, E. I., Changes in cellular membrane tolerance due to heat stress during Triticum sativum L. seeds germination. Mag. Al-Kufa Univ. Biol., 2013, 5, 1–9.

  • Bertin, P., Bouharmont, J. and Kinet, J. M., Somaclonal variation and improvement in chilling tolerance in rice: changes in chillinginduced electrolyte leakage. Plant Breed, 1996, 115, 268–272.

  • Wise, R. R., Olson, A. J., Schrader, S. M. and Sharkey, T. D., Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant Cell Environ., 2004, 27, 717–724.

  • Ivanov, S., Konstantinova, T., Parvanova, D., Todorova, D., Djilianov, D. and Alexieva, V., Effect of high temperature on the growth, free proline content and some antioxidants in tobacco plants. CR Acad. Bulg. Sci., 2001, 54, 71–74.

  • Ali, M. K., Azhar, A. and Galani, S., Response of rice (Oryza sativa L.) under elevated temperature at early growth stage: physiological markers. RJOAS, 2013, 8, 11–19.

  • Batjuka, A. and 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, 743–752.

  • Cho, K. Y., Kim, J. S. and Hong, K. S., Physiological action characteristics of m-substituted diphenylethers, TOPE and KC6361. Weed Technol., 1997, 42, 307–317.

  • Joët, T., Cournac, L., Horvath, E. M., Medgyesy, P. and Peltier, G., 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, 1919–1929.

  • Kalbáčová, M., Vrbacký, M., Drahota, Z. and Mĕlková., Z., Comparison of the effect of mitochondrial inhibitors on mitochondrial membrane potential in two different cell lines using flow cytometry and spectrofluorometry. Cytometry A, 2003, 52, 110–116.


Abstract Views: 212

PDF Views: 77




  • Evaluation of Superoxide Anion Level and Membrane Permeability in the Functionally Different Organs of Triticum aestivum L. Exposed to High Temperature and Antimycin A

Abstract Views: 212  |  PDF Views: 77

Authors

A. Batjuka
Laboratory of Molecular Biology and Genetics, Department of Ecology, Institute of Life Sciences and Technology, Daugavpils University, Parades Str.1a, Daugavpils, Latvia, LV-5401, Latvia
N. Skute
Laboratory of Molecular Biology and Genetics, Department of Ecology, Institute of Life Sciences and Technology, Daugavpils University, Parades Str.1a, Daugavpils, Latvia, LV-5401, Latvia

Abstract


The impact of antimycin A (AA) as an activator of the alternative respiratory pathway (AP) on the rate of superoxide anion (O•2¯) generation and membrane permeability was studied in the functionally different organs of wheat seedlings (Triticum aestivum L.) following short-term and long-term high temperature (HT). The results indicated a significant increase in the O•2¯ generating rate in etiolated wheat seedlings and seedlings grown under normal daylight regime following short-term (8%–37%) and long-term (13%– 65%) HT depending on the stage of development. The damages induced by HT were related to the permeability of membranes in the functionally different organs of wheat seedlings. However, our results demonstrated that increase in the O•2¯ generating rate in etiolated wheat seedlings was significantly lower following the combined effect of AA and HT, than under stressful conditions without AA. Taken together, our observations show that the induction of AP, provoked by AA, prevents over-reduction of the mitochondrial electron transport chain, alleviating reactive oxygen species formation and protecting the etiolated wheat seedlings against oxidative damage.

Keywords


Antimycin A, High Temperature, Membrane Permeability, Superoxide Anion, Triticum aestivum L.

References





DOI: https://doi.org/10.18520/cs%2Fv117%2Fi3%2F440-447