NADPH Thioredoxin reductase C controls the redox status of chloroplast 2-Cys peroxiredoxins in arabidopsis thaliana

Molecular Plant

Volumn 2, Issue 2, 2009, Pages 298-307

  Kirchsteiger, Kerstin ^a   Pulido, Pablo ^a   González, Maricruz ^a   Cejudo, Francisco Javier ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Arabidopsis; Chloroplast; NADPH thioredoxin reductase C; Overoxidation; Peroxiredoxin; Thioredoxin

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

PEROXIREDOXIN; PRIMER DNA; THIOREDOXIN REDUCTASE;

ARABIDOPSIS; CHLOROPLAST; ENZYMOLOGY; METABOLISM; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ARABIDOPSIS; BASE SEQUENCE; BLOTTING, WESTERN; CHLOROPLASTS; DNA PRIMERS; OXIDATION-REDUCTION; PEROXIREDOXINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIOREDOXIN-DISULFIDE REDUCTASE;

EID: 65249089101     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssn082     Document Type: Article

References (50)

1. Alkhalfioui, F., Renard, M.f and Montrichard, F. (2007). Unique properties of NADP-thioredoxin reductase C in legumes. J. Exp. Bot. 58, 969-978.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657.
3. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399.
4. Aran, M., Caporaletti, D., Senn, A.M., Tellez de Iñón, M.T., Girotti, M.R., Liera, A.S., and Wolosiuk, R.A. (2008). ATP-depen-dent modulation and autophosphorylation of a rapeseed 2-Cys peroxiredoxin. FEBS J. 275, 1450-1463.
5. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396.
6. Baier, M., and Dietz, K.-J. (1997). The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J. 12, 179-190.
7. 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.
8. Biteau, B., Labarre, J., and Toledano, M.B. (2003). ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature. 425, 980-984.
9. Broin, M., and Rey, P. (2003). Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BA51 2-Cysteine peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol. 132, 1335-1343.
10. Broin, M., Cuiné, S., Aymery, 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.
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. Collin, V., Lamkemeyer, P., Miginiac-Maslow, M., Hirasawa, M., Knaff, D.B., Dietz, K.J., and Issakidis-Bourguet, E. (2004). Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol. 136, 4088-4095.
13. Desikan, R., Mackerness, S.A.-H., Hancock, J.T., and Neil, S.J. (2001). Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159-172.
14. Dietz, K.-J. (2003). Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107.
15. Dietz, K.-J. (2008). Redox signal integration: from stimulus to networks and genes. Physiol. Plant. 133, 459-468.
16. Dietz, K.-J., Jacob, S., Oelze, M.L, Laxa, M., Tognetti, V., de Miranda, S.M., Baier, M., and Finkemeier, I. (2006). The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57, 1697-709.
17. Georgiou, G., and Masip, L. (2003). An overoxidation journey with a return ticket. Science. 300, 592-594.
18. Giacomelli, L., Masi, A., Ripoll, D.R., Lee, M.J., and van Wijk, K.J. (2007). Arabidopsis thaliana deficient in two chloroplast ascor-bate peroxidases shows accelerated light-induced necrosis when levels of cellular ascorbate are low. Plant Mol. Biol. 65, 627-644.
19. Kang, S.W., Baines, I.C., and Rhee, S.G. (1998). Characterization of mammalian peroxiredoxin that contains one conserved cysteine. J. Biol. Chem. 273, 6303-6311.
20. Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I., and Apel, K. (2007). Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA. 104, 672-677.
21. Lim, J.C., Choi, H.-l., Park, Y.S., Nam, H.W., Woo, H.A., Kwon, K.-S., Kim, Y.S., Rhee, S.G., Kim, K., and Chae, H.Z. (2008). Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem. 283, 28873-28880.
22. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410.
23. Moon, J.G., et al. (2006). The C-type Arabidopsis thioredoxin reductase ANTR-C acts as an electron donor to 2-Cys peroxiredoxins in chloroplasts. Biochem. Biophys. Res. Commun. 348, 478-484.
24. Nelson, N., and Ben-Shem, A. (2004). The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell Biol. 5, 1-12.
25. Neuhaus, H.E., and Ernes, M.J. (2000). Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 111-140.
26. Niyogi, K.K. (1999). Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359.
27. Nott, A., Jung, H.S., Koussevitzky, S., and Chory, J. (2006). Plastidto-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57, 739-759.
28. Op den Camp, R.G., et al. (2003). Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell. 15, 2320-2332.
29. Parmigiani, R.B., Xu, W.S., Venta-Pérez, G., Erdjument-Bromage, H., Yeneva, M., and Marks, P.A. (2008). HDAC6 is a specific deacety-lase of peroxiredoxins and is involved in redox regulation. Proc. Natl Acad. Sci. USA. 105, 9633-9638.
30. Perez-Ruiz, J.M., Spínola, M.C., Kirchsteiger, K., Moreno, J., Sahrawy, M., and Cejudo, F.J. (2006). Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell. 18, 2356-2368.
31. Pitzschke, A., Forzani, C., and Hirt, H. (2006). Reactive oxygen species signaling in plants. Antioxid. Redox Signal. 8, 1757-1764.
32. 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.
33. Rhee, S.G., Chae, H.Z., and Kim, K. (2005). Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signalling. Free Red. Biol. Med. 38, 1543-1552.
34. Rizhsky, L., Davletova, S., Liang, H., and Mittler, R. (2003). The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 278, 38921-38925.
35. Romero-Puertas, M.C., Laxa, M., Mattè, A., Zaninotto, F., Finkemeier, I., Jones, A.M., Perazzolli, M., Vandelle, E., Dietz, K.J., and Delledonne, M. (2007). S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell. 19, 4120-4130.
36. Rouhier, N., Couturier, J., and Jacquot, J.P. (2006). Genome-wide analysis of plant glutaredoxin systems. J. Exp. Bot. 57, 1685-1696.
37. Rouhier, N., Gelhaye, E., and Jacquot, J.P. (2002). Glutaredoxin-dependent peroxiredoxin from poplar. J. Biol. Chem. 277, 13609-13614.
38. Rouhier, N., Gelhaye, E., Sautiere, P.-E., Brun, A., Laurent, P., Tagu, D., Gerard, J., de Faÿ, 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.
39. Sanchez, R., and Cejudo, F.J. (2003). Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyr-uvate carboxylase from Arabidopsis and rice. Plant Physiol. 132, 949-957.
40. Schürmann, P., and Buchanan, B.B. (2008). The ferredoxin/thiore-doxin system of oxygenic photosynthesis. Antioxid. Redox Signal. 10, 1253-1273.
41. Serrato, A.J., Pérez-Ruiz, J.M., and Cejudo, F.J. (2002). Cloning of thioredoxin h reductase and characterization of the thioredoxin reductase-thioredoxin h system from wheat. Biochem. J. 217, 392-399.
42. Serrato, A.J., Pérez-Ruiz, J.M., Spínola, M.C., and Cejudo, F.J. (2004). A novel NADPH Thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J. Biol. Chem. 279, 43821-43827.
43. Spinola, M.C., Pérez-Ruiz, J.M., Pulido, P., Kirchsteiger, K., Guinea, M., González, M., and Cejudo, F.J. (2008). NTRC new ways of using NADPH in the chloroplast. Physiol. Plant. 133, 516-524.
44. Vandenabeele, S., et al. (2003). A comprehensive análisis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl Acad. Sci. USA. 100, 16113-16118.
45. Vanderauwera, S., Zimmermann, P., Rombauts, S., Vandenabeele, S., Langebartels, C., Gruissem, W., Inzé, D., and Van Breusegem, F. (2005). Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol. 139, 806-821.
46. Wagner, D., et al. (2004). The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science. 306, 1183-1185.
47. Woo, H.A., Chae, H.Z., Hwang, S.C., Yang, K.-S., Kang, S.W, Kim, K., and Rhee, S.G. (2003). Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science. 300, 653-656.
48. Wood, Z.A., Poole, LB., and Karplus, P.A. (2003a). Peroxiredoxin evolution and the regulation of hydrogen peroxide signalling. Science. 300, 650-653.
49. Wood, Z.A., Schröder, E., Harris, J.R., and Poole, LB. (2003b). Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40.
50. Yang, K.-S., Kang, S.W., Woo, H.A., Hwang, S.C., Chae, H.Z., Kim, K., and Rhee, S.G. (2002). Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277, 38029-38036.