Advertisement

Biochemistry (Moscow)

, Volume 81, Issue 4, pp 364–372 | Cite as

Glutathione reductase gene expression depends on chloroplast signals in Arabidopsis thaliana

  • E. Yu. GarnikEmail author
  • V. I. Belkov
  • V. I. Tarasenko
  • M. A. Korzun
  • Yu. M. Konstantinov
Article

Abstract

Glutathione reductase (EC 1.6.4.2) is one of the main antioxidant enzymes of the plant cell. In Arabidopsis thaliana, glutathione reductase is encoded by two genes: the gr1 gene encodes the cytosolic-peroxisomal form, and the gr2 gene encodes the chloroplast-mitochondrial form. Little is known about the regulation of expression of plant glutathione reductase genes. In the present work, we have demonstrated that gr2 (but not gr1) gene expression in Arabidopsis leaves changes depending on changes in redox state of the photosynthetic electron transport chain. Expression of both the gr1 and gr2 genes was induced by reactive oxygen species. In heterotrophic suspension cell culture of Arabidopsis, expression of both studied genes did not depend on H2O2 level or on changes in the redox state of the mitochondrial electron transport chain. Our data indicate that chloroplasts are involved in the regulation of the glutathione reductase gene expression in Arabidopsis.

Keywords

reactive oxygen species hydrogen peroxide glutathione reductase redox-regulation chloroplast-nuclear regulation of gene expression Arabidopsis thaliana 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Tahmasebi, A., Aram, F., Ebrahimi, M., Mohammadi Dehcheshmeh, M., and Ebrahimie, E. (2012) Genomewide analysis of cytosolic and chloroplastic isoforms of glutathione reductase in plant cells, Plant Omics J., 5, 94–102.Google Scholar
  2. 2.
    Noctor, G., Queval, G., Mhamdi, A., Chaouch, S., and Foyer, C. H. (2011) Glutathione, The Arabidopsis Book, doi: 10.1199/tab.0142.Google Scholar
  3. 3.
    Chalapathi-Rao, A. S. V., and Reddy, A. R. (2008) Glutathione reductase: a putative redox regulatory system in plant cells, in Sulfur Assimilation and Abiotic Stresses in Plants (Khan, N. A., Singh, S., and Umar, S., eds.) Springer, The Netherlands, pp. 111–147.Google Scholar
  4. 4.
    Creissen, G. P., Reynolds, H., Xue, Y., and Mullineaux, P. M. (1995) Cloning and characterization of glutathione reductase cDNAs and identification of two genes encoding the tobacco enzyme, Plant J., 8, 167–175.CrossRefPubMedGoogle Scholar
  5. 5.
    Stevens, R., Creissen, G. P., and Mullineaux, P. M. (1997) Cloning and characterization of a cytosolic glutathione reductase cDNA from pea (Pisum sativum L.) and its expression in response to stress, Plant Mol. Biol., 35, 641–654.CrossRefPubMedGoogle Scholar
  6. 6.
    Rouhier, N., Couturier, J., and Jacquot, J. (2006) Genome-wide analysis of plant glutaredoxins systems, J. Exp. Bot., 57, 1685–1696.CrossRefPubMedGoogle Scholar
  7. 7.
    Romero-Puertas, M. C., Corpas, F. J., Sandalio, L. M., Leterrier, M., Rodriguez-Serrano, M., Del Rio, L. A., and Palma, J. M. (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of peroxisomal isozyme, New Phytol., 170, 43–52.CrossRefPubMedGoogle Scholar
  8. 8.
    Lee, H., Won, S.-H., Lee, B.-H., Park, H.-D., Chung, W.I., and Jo, J. (2002) Genomic cloning and characterization of glutathione reductase gene from Brassica campestris var. Pekinensis, Mol. Cells, 13, 245–251.PubMedGoogle Scholar
  9. 9.
    Dghim, A. A., Mhamdi, A., Vaultier, M.-N., Hasenfratz Sauder, M.-P., Le Thiec, D., Dizengremel, P., Noctor, G., and Jolivet, Y. (2013) Analysis of cytosolic isocitrate dehydrogenase and glutathione reductase 1 in photoperiodinfluenced responses to ozone using Arabidopsis knockout mutants, Plant Cell Environ., 36, 1981–1991.PubMedGoogle Scholar
  10. 10.
    Kaminaka, H., Morita, S., Nakajima, M., Masumura, T., and Tanaka, K. (1998) Gene cloning and expression of cytosolic glutathione reductase in rice (Oryza sativa L.), Plant Cell Physiol., 39, 1269–1280.CrossRefPubMedGoogle Scholar
  11. 11.
    Contour-Ansel, D., Torres-Franklin, M. L., Cruz, D. E., Carvalho, M. H., D’Arcy-Lameta, A., and Zuily-Fodil, Y. (2006) Glutathione reductase in leaves of cowpea: cloning of two cDNAs, expression and enzymatic activity under progressive drought stress, desiccation and abscisic acid treatment, Ann. Bot., 98, 1278–1287.Google Scholar
  12. 12.
    Trivedi, D. P., Gill, S. S., Yadav, S., and Tuteja, N. (2013) Genome-wide analysis of glutathione reductase (GR) genes from rice and Arabidopsis, Plant Signal. Behav., 8, e23201.CrossRefGoogle Scholar
  13. 13.
    Belin, C., Bashandy, T., Cela, J., Delorme-Hinoux, V., Riondet, C., and Reichheld, J. P. (2015) A comprehensive study of thiol reduction gene expression under stress conditions in Arabidopsis thaliana, Plant Cell Environ., 38, 299–314.CrossRefPubMedGoogle Scholar
  14. 14.
    Murashige, T., and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures, Physiol. Plant., 15, 473–497.CrossRefGoogle Scholar
  15. 15.
    Meyer, E. H., Tomaz, T., Carroll, A. J., Estavillo, G., Delannoy, E., Tanz, S. K., Small, I. D., Pogson, B. J., and Millar, A. H. (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night, Plant Physiol., 151, 603–619.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Maxwell, D. P., Wang, Y., and McIntosh, L. (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells, Proc. Natl. Acad. Sci. USA, 96, 8271–8276.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Ivanov, B. N. (2014) Role of ascorbic acid in photosynthesis, Biochemistry (Moscow), 79, 282–269.CrossRefGoogle Scholar
  18. 18.
    Pfannschmidt, T., Shcutze, K., Brost, M., and Oelmuller, R. (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment, J. Biol. Chem., 276, 36125–36130.CrossRefPubMedGoogle Scholar
  19. 19.
    Ivanov, B. N., Khorobrykh, S. A., Kozuleva, M. A., and Borisova-Mubarakshina, M. M. (2013) The role of oxygen and its reactive species in photosynthesis, in Photosynthesis: Questions to Answer and What We Know Today (Allakhverdiev, S. I., Rubin, A. B., and Shuvalov, V. A., eds.) [in Russian], Institute of Computer-Aided Studies, Izhevsk, pp. 243–298.Google Scholar
  20. 20.
    Zubo, Y. O., Potapova, T. V., Yamburenko, M. V., Tarasenko, V. I., Konstantinov, Yu. M., and Borner, T. (2014) Inhibition of the electron transport strongly affects transcription and transcript levels in Arabidopsis mitochondria, Mitochondrion, 19, 222–230.CrossRefPubMedGoogle Scholar
  21. 21.
    Tarasenko, V. I., Garnik, E. Yu., Shmakov, V. N., and Konstantinov, Yu. M. (2009) Induction of Arabidopsis gene gdh2 expression during changes in redox state of the mitochondrial respiratory chain, Biochemistry (Moscow), 74, 47–53.CrossRefGoogle Scholar
  22. 22.
    Rasmusson, A. G., and Escobar, M. A. (2007) Light and diurnal regulation of plant respiratory gene expression, Physiol. Plant., 129, 57–67.CrossRefGoogle Scholar
  23. 23.
    Blasing, O. E., Gibon, Y., Gunter, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheibe, W.-R., and Stitt, M. (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis, Plant Cell Physiol., 17, 3257–3281.CrossRefGoogle Scholar
  24. 24.
    Glasser, C., Haberer, G., Finkemeier, I., Pfannschmidt, T., Kleine, T., Leister, D., Dietz, K. J., Hausler, R. E., Grimm, B., and Mayer, K. F. (2014) Meta-analysis of retrograde signaling in Arabidopsis thaliana reveals a core module of genes embedded in complex cellular signaling networks, Mol. Plant, 7, 1167–1190.CrossRefPubMedGoogle Scholar
  25. 25.
    Yoshida, K., Terashima, I., and Noguchi, K. (2011) How and why does the mitochondrial respiratory chain respond to light? Plant Signal. Behav., 6, 864–866.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Oelze, M. L., Vogel, M. O., Alsharafa, K., Kahmann, U., Viehhauser, A., Maurino, V. G., and Dietz, K. J. (2012) Efficient acclimation of the chloroplast antioxidant defense of Arabidopsis thaliana leaves in response to a 10or 100-fold light increment and the possible involvement of retrograde signals, J. Exp. Bot., 63, 1297–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Estavillo, G. M., Chan, K. X., Phua, S. Y., and Pogson, B. J. (2013) Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast, Front. Plant Sci., doi: 10.3389/fpls.2012.00300.Google Scholar
  28. 28.
    Yurina, N. P., Mokerova, D. V., and Odintsova, M. S. (2013) Light-induced stress proteins of phototrophs, Russ. J. Plant Physiol., 60, 577–589.CrossRefGoogle Scholar
  29. 29.
    Lee, C. P., Eubel, H., and Millar, A. H. (2010) Diurnal changes in mitochondrial function reveal daily optimization of light and dark respiratory metabolism in Arabidopsis, Mol. Cell. Proteom., 9, 2125–2139.CrossRefGoogle Scholar
  30. 30.
    Pogson, B. J., Woo, N. S., Forster, B., and Small, I. D. (2008) Plastid signaling to the nucleus and beyond, Trends Plant Sci., 13, 602–609.CrossRefPubMedGoogle Scholar
  31. 31.
    Chi, W., Sun, X., and Zhang, L. (2013) Intracellular signaling from plastid to nucleus, Annu. Rev. Plant Biol., 64, 559–582.CrossRefPubMedGoogle Scholar
  32. 32.
    Ogawa, K., Hatano-Iwasaki, A., Yanagida, M., and Iwabuchi, M. (2004) Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering, Plant Cell Physiol., 45, 1–8.CrossRefPubMedGoogle Scholar
  33. 33.
    Cottage, A., Mott, E. K., Kempster, J. A., and Gray, J. C. (2010) The Arabidopsis plastid-signaling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development, J. Exp. Bot., 61, 3773–3786.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Liu, R., Xu, Y.-H., Jiang, S.-C., Lu, K., Lu, Y.-F., Feng, X.-J., Wu, Z., Liang, S., Yu, Y.-T., Wang, X.-F., and Zhang, D.-P. (2013) Light-harvesting chlorophyll a/b-binding proteins, positively involved in abscisic acid signaling, require a transcription repressor, WRKY40, to balance their function, J. Exp. Bot., 64, 5443–5456.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Waters, M. T., and Langdale, J. A. (2009) The making of a chloroplast, EMBO J., 28, 2861–2873.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Borisova-Mubarakshina, M. M., Ivanov, B. N., Vetochkina, D. V., Lubimov, V. Y., Fedorchuk, T. P., Naydov, I. A., Kozuleva, M. A., Rudenko, N. N., Dall’Osto, L., Cazzaniga, S., and Bassi, R. (2015) Longterm acclimatory response to excess excitation energy: evidence for a role of hydrogen peroxide in the regulation of photosystem II antenna size, J. Exp. Bot., doi: 10.1093/jxb/erv410.Google Scholar
  37. 37.
    Xu, Y., and Johnson, C. H. (2001) A clockand light-regulated gene that links the circadian oscillator to LHCB gene expression, Plant Cell, 13, 1411–1425.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Estavillo, G. M., Crisp, P. A., Pornsiriwong, W., Wirtz, M., Collinge, D., Carrie, C., Giraud, E., Whelan, J., David, P., Javot, H., Brearley, C., Hell, R., Marin, E., and Pogson, B. J. (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis, Plant Cell, 23, 3992–4012.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Dal Bosco, C., Busconi, M., Govoni, C., Baldi, P., Stanca, A. M., Crosatti, C., Bassi, R., and Cattivelli, L. (2003) Cor gene expression in barley mutants affected in chloroplast development and photosynthetic electron transport, Plant Physiol., 131, 793–802.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Tarasenko, V. I., Garnik, E. Yu., Shmakov, V. N., and Konstantinov, Yu. M. (2012) Modified alternative oxidase expression results in different reactive oxygen species content in Arabidopsis cell culture but not in whole plants, Biol. Plant., 56, 635–640.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • E. Yu. Garnik
    • 1
    Email author
  • V. I. Belkov
    • 1
  • V. I. Tarasenko
    • 1
  • M. A. Korzun
    • 1
  • Yu. M. Konstantinov
    • 1
  1. 1.Siberian Institute of Plant Physiology and BiochemistrySiberian Branch of the Russian Academy of SciencesIrkutskRussia

Personalised recommendations