The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response

Plant Journal

Volumn 49, Issue 3, 2007, Pages 505-514

  Rey, Pascal ^a   Bécuwe, Noëlle ^a   Barrault, Marie Bénédicte ^b   Rumeau, Dominique ^a   Havaux, Michel ^a   Biteau, Benoît ^b   Toledano, Michel B ^b  

^a IRFM   (France)

^b DIF   (France)

Author keywords

Arabidopsis thaliana; Chloroplast; Cysteine sulfinic acid; Peroxiredoxin; Photooxidative stress; Sulfiredoxin

Indexed keywords

ARABIDOPSIS THALIANA; CYSTEINE SULFINIC ACID; PEROXIREDOXIN; PHOTOOXIDATIVE STRESS; SULFIREDOXIN;

AMINO ACIDS; ENZYME KINETICS; GENES; PHOTOCHEMICAL REACTIONS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; OXIDOREDUCTASE; PEROXIDASE; PEROXIREDOXIN; SULFIREDOXIN PROTEIN, ARABIDOPSIS; UNCLASSIFIED DRUG;

ADAPTATION; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHLOROPLAST; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOMOZYGOTE; LIGHT; METABOLISM; MOLECULAR GENETICS; MUTATION; OXIDATION REDUCTION REACTION; PHENOTYPE; SEQUENCE HOMOLOGY; TEMPERATURE;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; GENE EXPRESSION; HOMOZYGOTE; LIGHT; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PEROXIDASES; PHENOTYPE; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE;

CYSTEINE; ENZYMATIC ACTIVITY; GENES; PHOTOSYNTHESIS; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 33846427352     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02969.x     Document Type: Article

References (44)

1. Asada, K. (1996) Radical production and scavenging in the chloroplast. In Advances in Photosynthesis. Vol. 5, Photosynthesis and the Environment (Baker, N.R., ed.). Dordrecht: Kluwer Academic Publishers, pp. 123-150.
2. Baier, M. and Dietz, K.J. (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol. 119, 1407-1414.
3. Baier, M., Noctor, G., Foyer, C. and Dietz, K.J. (2000) Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol. 124, 823-832.
4. Biteau, B., Labarre, J. and Toledano, M.B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature, 425, 980-984.
5. Bozonet, S.M., Findlay, V.J., Day, A.M., Cameron, J., Veals, E.A. and Morgan, B.M. (2005) Oxidation of a eukaryotic 2-Cys peroxiredoxin is a molecular switch controlling the transcriptional responses to increasing levels of hydrogen peroxide. J. Biol. Chem. 280, 23319-23327.
6. Bréhelin, C., Meyer, E.H., de Souris, J.P., Bonnard, G. and Meyer, Y. (2003) Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: similar sequences for divergent gene expression, protein localization and activity. Plant Physiol. 132, 2045-2057.
7. Broin, M. and Rey, P. (2003) Potato plants lacking the CDSP32 plastidic thioredoxin exhibit over-oxidation of the BAS1 2-cys peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol. 132, 1335-1343.
8. Broin, M., Cuiné, S., Eymery, F. and Rey, P. (2002) The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell, 14, 1417-1432.
9. Budanov, A.V., Sablina, A.A., Feinstein, E., Koonin, E.V. and Chumakov, P.M. (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science, 304, 596-600.
10. Chang, T.S., Jeong, W., Woo, H.A., Lee, S.M., Park, S. and Rhee, S.G. (2004) Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J. Biol. Chem. 279, 50994-51001.
11. Collin, V., Issakidis-Bourguet, E., Marchand, C., Hirasawa, M., Lancelin, J.M., Knaff, D.B. and Miginiac-Maslow, M. (2003) The Arabidopsis plastidial thioredoxins. New functions and new insights into specificity. J. Biol. Chem. 278, 23747-23752.
12. Davis, S.J. and Vierstra, R.D. (1998) Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol. Biol. 36, 521-528.
13. Dietz, K.J. (2003) Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107.
14. Havaux, M. (2003) Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants. Trends Plant Sci. 8, 409-413.
15. Havaux, M. and Niyogi, K.K. (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl Acad. Sci. USA, 96, 8762-8767.
16. Heazlewood, J.L., Howell, K.A. and Millar, A.H. (2003) Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim. Biophys. Acta, 1604, 159-169.
17. Jeong, W., Park, S.J., Chang, T.-S., Lee, D.-Y. and Rhee, S.G. (2006) Molecular mechanisms of the reduction of cysteine sulfinic acid of peroxiredoxin to cysteine by mammalian sulfiredoxin. J. Biol. Chem. 281, 14400-14407.
18. Jönsson, T.J., Murray, M.S., Johnson, L.C., Poole, L.B. and Lowther, W.T. (2005) Structural basis for the retroreduction of inactivated peroxiredoxins by human sulfiredoxin. Biochemistry, 44, 8634-8642.
19. Karimi, M., De Meyer, B. and Hilson, P. (2005) Modular cloning in plant cells. Trends Plant Sci. 10, 103-105.
20. König, J., Baier, M., Horling, F., Kahmann, U., Harris, G., Schürmann, P. and Dietz, K.J. (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc. Natl Acad. Sci. USA, 99, 5738-5743.
21. König, J., Lotte, K., Plessow, R., Brockhinke, A., Baier, M. and Dietz, K.J. (2003) Reaction mechanisms of plant 2-Cys peroxiredoxin. Role of the C-terminus and the quaternary structure. J. Biol. Chem. 278, 24409-24420.
22. Lamkemeyer, P., Laxa, M., Collin, V. et al. (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J. 45, 968-981.
23. Liu, X.P., Liu, X.Y., Zhang, J., Xia, Z.L., Liu, X., Qin, H.J. and Wang, D.W. (2006) Molecular and functional characterization of sulfiredoxin homologs from higher plants. Cell Res. 16, 287-296.
24. Maxwell, K. and Johnson, G.N. (2000) Chlorophyll fluorescence-a practical guide. J. Exp. Bot. 51, 659-668.
25. Meyer, Y., Reichheld, J.P. and Vignols, F. (2005) Thioredoxins in Arabidopsis and other plants. Photosynth. Res. 86, 419-433.
26. Mittler, R., Vanderauwera, R.S., Gollery, M. and van Breusegem, F. (2004) Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498.
27. Müller-Moule, P., Havaux, M. and Niyogi, K.K. (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol. 133, 748-760.
28. Pruvot, G., Cuiné, S., Peltier, G. and Rey, P. (1996) Characterization of a novel drought-induced 34-kDa protein located in the thylakoids of Solanum tuberosum L. plants. Planta, 198, 471-479.
29. Rey, P., Eymery, F. and Peltier, G. (1990) Atrazine and diuron resistant plants from photoautotrophic protoplast-derived cultures of Nicotiana plumbaginifolia. Plant Cell Rep. 9, 241-244.
30. Rey, P., Pruvot, G., Becuwe, N., Eymery, F., Rumeau, D. and Peltier, G. (1998) A novel thioredoxin-like protein located in the chloroplast is induced by water deficit in Solanum tuberosum L. plants. Plant J. 13, 97-107.
31. Rey, P., Cuiné, S., Eymery, F., Garin, J., Court, M., Jacquot, J.-P., Rouhier, N. and Broin, M. (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J. 41, 31-42.
32. Rouhier, N., Gelhaye, E., Sautiere, P.E., Brun, A., Laurent, P., Tagu, D., Gerard, J., de Fay, E., Meyer, Y. and Jacquot, J.-P. (2001) Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol. 127, 1299-1309.
33. Rouhier, N., Gelhaye, E. and Jacquot, J.-P. (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol. Life Sci. 61, 1266-1277.
34. Ruelland, E. and Miginiac-Maslow, M. (1999) Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition? Trends Plant. Sci. 4, 136-141.
35. Vavilin, D.V. and Ducruet, J.M. (1998) The origin of the 115-130°C thermoluminescence bands in chlorophyll-containing material. Photochem. Photobiol. 68, 191-198.
36. Vieira Dos Santos, C. and Rey, P. (2006) Plant thioredoxins are key actors in oxidative stress response. Trends Plant Sci. 11, 329-334.
37. Vieira Dos Santos, C., Cuiné, S., Rouhier, N. and Rey, P. (2005) The Arabidopsis plastidic methionine sulfoxide reductases B proteins: sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A and induction by photooxidative stress. Plant Physiol. 138, 909-922.
38. 2-sensing by the antioxidant Pap1 patwway. Proc. Natl Acad. Sci. USA, 102, 8875-8880.
39. Woo, H.A., Kang, S.W., Kim, H.K., Yang, K.S., Chae, H.Z. and Rhee, S.G. (2003) Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid. Immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J. Biol. Chem. 278, 47361-47364.
40. Woo, H.A., Jeong, W., Chang, T.S., Park, K.J., Park, S.J., Yang, J.S. and Rhee, S.G. (2005) Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-Cys peroxiredoxins. J. Biol. Chem. 280, 3125-3128.
41. Wood, Z.A., Poole, L.B. and Karplus, P.A. (2003a) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science, 300, 650-653.
42. Wood, Z.A., Schröder, E., Harris, J.R. and Poole, L.B. (2003b) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40.
43. Yamada, K., Lim, J., Dale, J.M. et al. (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science, 302, 842-846.
44. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.