The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling

FEBS Letters

Volumn 586, Issue 18, 2012, Pages 2974-2980

  Cejudo, Francisco Javier ^a   Ferrández, Julia ^a   Cano, Beatriz ^a   Puerto Galán, Leonor ^a   Guinea, Manuel ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Chloroplast; Peroxiredoxin; Redox regulation; Thioredoxin; Thioredoxin reductase

Indexed keywords

2 CYSTEINE PEROXIREDOXIN; CHLOROPHYLL; OXIDOREDUCTASE; PEROXIREDOXIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEPENDENT THIOREDOXIN REDUCTASE; SULFIREDOXIN; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARABIDOPSIS; CHLOROPHYLL CONTENT; CHLOROPLAST; CONFERENCE PAPER; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENE SWITCHING; GENETIC REGULATION; MOLECULAR INTERACTION; NONHUMAN; NTRC GENE; OXIDATION; OXIDATION REDUCTION STATE; PHOTOSYNTHESIS; PLANT DEVELOPMENT; PLANT GENE; PLANT GENETICS; PLANT METABOLISM; PLASTID; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

HOMEOSTASIS; NADP; OXIDATION-REDUCTION; PEROXIREDOXINS; PLASTIDS; SIGNAL TRANSDUCTION; THIOREDOXIN-DISULFIDE REDUCTASE;

EID: 84864941653     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.07.003     Document Type: Conference Paper

References (58)

1. J.F. Collet, and J. Messens Structure, function, and mechanism of thioredoxin proteins Antioxid. Redox Sign. 13 2010 1205 1216
2. J.-P. Jacquot, H. Eklund, N. Rohuier, and P. Schürmann Structural and evolutionary aspects of thioredoxin reductase in photosynthetic organisms Trends Plant Sci. 14 2009 336 343
3. Y. Meyer, J.P. Reichheld, and F. Vignols Thioredoxins in Arabidopsis and other plants Photosynth. Res. 86 2005 419 433
4. S.D. Lemaire, L. Michelet, M. Zaffagnini, V. Massot, and E. Issakidis-Bourguet Thioredoxins in chloroplasts Curr. Genet. 51 2007 343 365
5. A. Serrato, J.M. Pérez-Ruiz, M.C. Spínola, and F.J. Cejudo A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana J. Biol. Chem. 279 2004 43821 43827
6. M.C. Spínola, J.M. Pérez-Ruiz, P. Pulido, K. Kirchsteiger, M. Guinea, M.C. González, and F.J. Cejudo NTRC: New ways of using NADPH in the chloroplast Physiol. Plant. 133 2008 516 524
7. H.E. Neuhaus, and M.J. Emes Non-photosynthetic metabolism in plastids Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 2000 111 140
8. J.M. Pérez-Ruiz, M.C. Spínola, K. Kirchsteiger, J. Moreno, M. Sahrawy, and F.J. Cejudo Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage Plant Cell 18 2006 2356 2368
9. A. Lepistö, S. Kangasjärvi, E.M. Luomala, G. Brader, N. Sipari, M. Keränen, M. Keinänen, and E. Rintamäki Choloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis Plant Physiol. 149 2009 1261 1276
10. K. Kirchsteiger, J. Ferrández, M.B. Pascual, M. González, and F.J. Cejudo NADPH thioredoxin reductase C is localized in plastids of photosynthetic and non-photosynthetic tissues and is involved in lateral root formation in Arabidopsis thaliana Plant Cell 24 2012 1534 1548
11. A.J. Serrato, J.M. Pérez-Ruiz, and F.J. Cejudo Cloning of thioredoxin h reductase and characterization of the thioredoxin reductase-thioredoxin h system from wheat Biochem. J. 217 2002 392 399
12. C.H. Williams, L.D. Arscott, S. Müller, B.W. Lennon, M.L. Ludwig, P.F. Wang, D.M. Veine, K. Becker, and R.H. Schirmer Thioredoxin reductase two modes of catalysis have evolved Eur. J. Biochem. 267 2000 6110 6117
13. J.P. Reichheld, E. Meyer, M. Khafif, G. Bonnard, and Y. Meyer AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana FEBS Lett. 579 2005 337 342
14. J.C. Moon, H.H. Jang, H.B. Chae, J.R. Lee, S.Y. Lee, Y.J. Jung, M.R. Shin, H.S. Lim, W.S. Chung, D.J. Yun, K.O. Lee, and S.Y. Lee The C-type Arabidopsis thioredoxin reductase ANTR-C acts as an electron donor to 2-Cys peroxiredoxins in chloroplasts Biochem. Biophys. Res. Commun. 348 2006 478 484
15. F. Alkhalfioui, M. Renard, and F. Montrichard Unique properties of NADP-thioredoxin reductase C in legumes J. Exp. Bot. 58 2007 969 978
16. M. Broin, S. Cuiné, F. Aymery, and P. Rey 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 2002 1417 1432
17. V. Collin, E. Issakidis-Bourguet, C. Marchand, M. Hirasawa, J.-M. Lancelin, D.B. Knaff, and M. Miginiac-Maslow The Arabidopsis plastidial thioredoxins. New functions and new insights into specificity J. Biol. Chem. 278 2003 23747 23752
18. P. Pulido, M.C. Spínola, K. Kirchsteiger, M. Guinea, M.B. Pascual, M. Sahrawy, L.M. Sandalio, K.J. Dietz, M. González, and F.J. Cejudo Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts J. Exp. Bot. 61 2010 4043 4054
19. J.M. Pérez-Ruiz, M. González, M.C. Spínola, L.M. Sandalio, and F.J. Cejudo The quaternary structure of NADPH thioredoxin reductase C is redox-sensitive Mol. Plant 2 2009 457 467
20. J.M. Pérez-Ruiz, and F.J. Cejudo A proposed reaction mechanism for rice NADPH thioredoxin reductase C, an enzyme with protein disulfide reductase activity FEBS Lett. 583 2009 1399 1402
21. R.P. Wulff, J. Lundqvist, G. Rutsdottir, A. Hansson, A. Stenbaek, D. Elmlund, H. Elmlund, P.E. Jensen, and M. Hansson The activity of barley NADPH-dependent thioredoxin reductase C is independent of the oligomeric state of the protein: tetrameric structure determined by cryo-electron microscopy Biochemistry 50 2011 3713 3723
22. M.B. Pascual, A. Mata-Cabana, F.J. Florencio, M. Lindahl, and F.J. Cejudo A comparative analysis of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system from plants and cyanobacteria Plant Physiol. 155 2011 1806 1816
23. P.D. Aart, R. Tanaka, and A. Tanaka Effects of oxidative stress on chlorophyll biosynthesis in cucumber (Cucumis sativus) cotyledons Physiol. Plant. 128 2006 186 197
24. A. Stenbaek, A. Hansson, R.P. Wulff, M. Hansson, K.-J. Dietz, and P.E. Jensen NADPH-dependent thioredoxin reductase and 2-Cys peroxiredoxins are needed for the protection of Mg-protoporphyrin monomethyl ester cyclase FEBS Lett. 582 2008 2773 2778
25. J. Peñuelas, and S. Munne-Bosch Isoprenoids: an evolutionary pool for photoprotection Trends Plant Sci. 10 2005 166 169
26. C.H. Foyer, and G. Noctor Redox regulation in photosynthetic organisms: signalling, acclimation, and practical implications Antiox. Redox Signal. 11 2009 861 905
27. M. Baier, and K.J. Dietz Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis Plant Physiol. 119 1999 1407 1414
28. M. Baier, G. Noctor, C.H. Foyer, and K.J. Dietz Antisense suppression of 2-peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism Plant Physiol. 124 2000 823 832
29. P. Geigenberger Regulation of starch biosynthesis in response to fluctuating environment Plant Physiol. 155 2011 1566 1577
30. J.H.M. Hendriks, A. Kolbe, Y. Gibon, M. Stitt, and P. Geigenberger ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species Plant Physiol. 133 2003 838 849
31. I. Thormählen, J. Ruber, E. von Roepenack-Lahaye, S.M. Ehrlich, V. Massot, C. Hümmer, J. Tezycka, E. Issakidis-Bourguet, and P. Geigenberger Inactivation of thioredoxin f1 leads to decreased light-activation of ADP-glucose pyrophosphorylase and altered diurnal starch turnover in leaves of Arabidopsis plants Plant Cell Environ. 2012 10.1111/j. 1365-3040, 2012.02549.x
32. J. Michalska, H. Zauber, B.B. Buchanan, F.J. Cejudo, and P. Geigenberger NTRC links built in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts Proc. Natl. Acad. Sci. U S A 106 2009 9908 9913
33. J. Li, I. Ezquer, A. Bahaji, M. Montero, M. Ovecka, E. Baroja-Fernández, F.J. Muñoz, A. Mérida, G. Almagro, M. Hidalgo, M.T. Sesma, and J. Pozueta-Romero Microbial volatile-induced accumulation of exceptionally high levels of starch in Arabidopsis leaves is a process involving NTRC and starch synthase classes III and IV Mol. Plant Microb. Interact. 24 2011 1165 1178
34. J. Li, G. Almagro, F.J. Muñoz, E. Baroja-Fernández, A. Bahaji, M. Montero, M. Hidalgo, A.M. Sánchez-López, I. Ezquer, M.T. Sesma, and J. Pozueta-Romero Post-translational redox modification of ADP-glucose pyrophosphorylase in response to light is not a major determinant of fine regulation of transitory starch accumulation in Arabidopsis leaves Plant Cell Physiol. 53 2012 433 444
35. C.J. Walker, and R.D. Willows Mechanism and regulation of Mg chelatase Biochem. J. 327 1997 321 333
36. P.E. Jensen, J.D. Reid, and C.N. Hunter Modification of cysteine residues in the ChlI and ChlH subunits of magnesium chelatase results in enzyme inactivation Biochem. J. 352 2000 435 441
37. A. Ikegami, N. Yoshimura, K. Motohashi, S. Takahashi, P.G.N. Romano, T. Hisabori, K. Takamiya, and T. Masuda The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin J. Biol. Chem. 282 2007 19282 19291
38. A. Stenbaek, and P.E. Jensen Redox regulation of chlorophyll biosynthesis Phytochemistry 71 2010 853 859
39. T. Luo, T. Fan, Y. Liu, M. Rothbart, J. Yu, S. Zhou, B. Grimm, and M. Luo Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants Plant Physiol. 159 2012 118 130
40. J.D. Woodson, and J. Chory Coordination of gene expression between organellar and nuclear genomes Nat. Rev. Genet. 9 2008 383 395
41. E. Rintamäki, A. Lepistö, and S. Kangasjärvi Implication of chlorophyll biosynthesis on chloroplast-to-nucleus retrograde signaling Plant Signal. Behav. 4 2009 545 547
42. A. Pitzschke, C. Forzani, and H. Hirt Reactive oxygen species signaling in plants Antiox. Redox Signal. 8 2006 1757 1764
43. F. Van Breusegem, J. Bailey-Serres, and R. Mittler Unraveling the tapestry of networks involving reactive oxygen species in plants Plant Physiol. 147 2008 978 984
44. Z.A. Wood, L.B. Poole, and P.A. Karplus Peroxiredoxin evolution and the regulation of hydrogen peroxide signalling Science 300 2003 650 653
45. K.-J. Dietz Plant peroxiredoxins Annu. Rev. Plant Biol. 54 2003 93 107
46. H.Z. Chae, S.J. Chung, and S.G. Rhee Thioredoxin-dependent peroxide reductase from yeast J. Biol. Chem. 269 1994 27670 27678
47. M.B. Pascual, A. Mata-Cabana, F.J. Florencio, M. Lindahl, and F.J. Cejudo Overoxidation of 2-Cys peroxiredoxin in prokaryotes: cyanobacterial 2-Cys peroxiredoxins sensitive to oxidative stress J. Biol. Chem. 285 2010 34485 34492
48. A. Hall, P.A. Karplus, and L.B. Poole Typical 2-Cys peroxiredoxins - structures, mechanisms and functions FEBS J. 276 2009 2469 2477
49. K. Kirchsteiger, P. Pulido, M.C. González, and F.J. Cejudo NADPH Thioredoxin reductase C controls the redox status of chloroplast 2-Cys peroxiredoxins in Arabidopsis thaliana Mol. Plant 2 2009 298 307
50. B. Biteau, J. Labarre, and M.B. Toledano ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin Nature 425 2003 980 984
51. H.A. Woo, H.Z. Chae, S.C. Hwang, K.-S. Yang, S.W. Kang, K. Kim, and S.G. Rhee Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation Science 300 2003 653 656
52. X.P. Liu, X.Y. Liu, J. Zhang, Z.L. Xia, X. Liu, H.J. Qin, and D.W. Wang Molecular and functional characterization of sulfiredoxin homologs from higher plants Cell Res. 16 2006 287 296
53. P. Rey, N. Becuwe, M.B. Barrault, D. Rumeau, M. Havaux, B. Biteau, and M.B. Toledano The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulphinic acid reductase involved in the photooxidative stress response Plant J. 49 2007 505 514
54. I. Iglesias-Baena, S. Barranco-Medina, A. Lázaro-Payo, F.J. López-Jaramillo, F. Sevilla, and J.J. Lázaro Characterization of plant sulfiredoxin and role of sulphinic form of 2-Cys peroxiredoxin J. Exp. Bot. 61 2010 1509 1521
55. H.H. Jang, K.O. Lee, Y.H. Chi, and B.G. Jung Two enzymes in one: two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function Cell 117 2004 625 635
56. M. Muthuramalingam, T. Seidel, M. Laxa, S.M. Nunes de Miranda, F. Gärtner, E. Ströher, A. Kandlbinder, and K.-J. Dietz Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast Mol. Plant 2 2009 1273 1288
57. J.S. O'Neill, G. van Ooijen, L.E. Dixon, C. Troein, F. Corellou, F.Y. Bouget, A.B. Reddy, and A.J. Millar Circadian rhythms persist without transcription in a eukaryote Nature 469 2011 554 558
58. Y. Balmer, W.H. Vensel, W. Manieri, P. Schürmann, W.J. Hurkman, and B.B. Buchanan A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts Proc. Natl. Acad. Sci. U S A 103 2006 2988 2993