Abstract
The post-translational modification consisting in the formation/reduction of disulfide bonds has been the subject of intense research in plants since the discovery in the 1970s that many chloroplastic enzymes are regulated by light through dithiol–disulfide exchange reactions catalyzed by oxidoreductases called thioredoxins (Trxs). Further biochemical and proteomic studies have considerably increased the number of target enzymes and processes regulated by these mechanisms in many sub-cellular compartments. Recently, glutathionylation, a modification consisting in the reversible formation of a glutathione adduct on cysteine residues, was proposed as an alternative redox regulation mechanism. Glutaredoxins (Grxs), proteins related to Trxs, are efficient catalysts for deglutathionylation, the opposite reaction. Hence, the Trxs- and Grxs-dependent pathways might constitute complementary and not only redundant regulatory processes. This article focuses on these two multigenic families and associated protein partners in poplar and on their involvement in the regulation of some major chloroplastic processes such as stress response, carbohydrate and heme/chlorophyll metabolism.
Similar content being viewed by others
References
Alkhalfioui F, Renard M, Vensel WH, Wong J, Tanaka CK, Hurkman WJ, Buchanan BB, Montrichard F (2007) Thioredoxin-linked proteins are reduced during germination of Medicago truncatula seeds. Plant Physiol 144:1559–1579
Alkhalfioui F, Renard M, Frendo P, Keichinger C, Meyer Y, Gelhaye E, Hirasawa M, Knaff DB, Ritzenthaler C, Montrichard F (2008) A novel type of thioredoxin dedicated to symbiosis in legumes. Plant Physiol 148:424–435
Baier M, Dietz KJ (1999) Alkyl hydroperoxide reductases: the way out of the oxidative breakdown of lipids in chloroplasts. Trends Plant Sci 4:166–168
Ballicora MA, Frueauf JB, Fu Y, Schürmann P, Preiss J (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 275:1315–1320
Balmer Y, Stritt-Etter AL, Hirasawa M, Jacquot JP, Keryer E, Knaff DB, Schürmann P (2001) Oxidation-reduction and activation properties of chloroplast fructose 1,6-bisphosphatase with mutated regulatory site. Biochemistry 40:15444–15450
Balmer Y, Koller A, del Val G, Manieri W, Schürmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100:370–375
Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schürmann P, Droux M, Buchanan BB (2004a) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101:2642–2647
Balmer Y, Koller A, Val GD, Schürmann P, Buchanan BB (2004b) Proteomics uncovers proteins interacting electrostatically with thioredoxin in chloroplasts. Photosynth Res 79:275–280
Balmer Y, Vensel WH, Hurkman WJ, Buchanan BB (2006a) Thioredoxin target proteins in chloroplast thylakoid membranes. Antioxid Redox Signal 8:1829–1834
Balmer Y, Vensel WH, DuPont FM, Buchanan BB, Hurkman WJ (2006b) Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J Exp Bot 57:1591–1602
Balsera M, Goetze TA, Kovács-Bogdán E, Schürmann P, Wagner R, Buchanan BB, Soll J, Bölter B (2009) Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca(2+) and a stromal regulatory disulfide bridge. J Biol Chem 284:2603–2616
Bandyopadhyay S, Gama F, Molina-Navarro MM, Gualberto JM, Claxton R, Naik SG, Huynh BH, Herrero E, Jacquot JP, Johnson MK, Rouhier N (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe–2S] clusters. EMBO J 27:1122–1133
Bartsch S, Monnet J, Selbach K, Quigley F, Gray J, von Wettstein D, Reinbothe S, Reinbothe C (2008) Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc Natl Acad Sci USA 105:4933–4938
Bick JA, Aslund F, Chen Y, Leustek T (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 95:8404–8409
Binda C, Coda A, Aliverti A, Zanetti G, Mattevi A (1998) Structure of the mutant E92K of [2Fe–2S] ferredoxin I from Spinacia oleracea at 1.7 A resolution. Acta Crystallographica D 54:1353–1358
Brandes HK, Larimer FW, Hartman FC (1996) The molecular pathway for the regulation of phosphoribulokinase by thioredoxin f. J Biol Chem 271:3333–3335
Bréhélin C, Meyer EH, de Souris JP, Bonnard G, 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
Broin M, Rey P (2003) Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-cysteine peroxiredoxin and increased lipid Peroxidation in thylakoids under photooxidative stress. Plant Physiol 132:1335–1343
Broin M, Cuine S, Eymery F, 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
Buchanan BB, Schürmann P, Wolosiuk RA, Jacquot JP (2002) The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth Res 73:215–222
Caporaletti D, D’Alessio AC, Rodriguez-Suarez RJ, Senn AM, Duek PD, Wolosiuk RA (2007) Non-reductive modulation of chloroplast fructose-1,6-bisphosphatase by 2-Cys peroxiredoxin. Biochem Biophys Res Commun 355:722–727
Carroll MC, Outten CE, Proescher JB, Rosenfeld L, Watson WH, Whitson LJ, Hart PJ, Jensen LT, Cizewski Culotta V (2006) The effects of glutaredoxin and copper activation pathways on the disulfide and stability of Cu, Zn superoxide dismutase. J Biol Chem 281:28648–28656
Chang CC, Slesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150:670–683
Chiadmi M, Navaza A, Miginiac-Maslow M, Jacquot JP, Cherfils J (1999) Redox signaling in the chloroplast: structure of the oxidized pea fructose 1,6 biphosphatase. EMBO J 18:6809–6815
Chibani K, Wingsle G, Jacquot JP, Gelhaye E, Rouhier N (2009) Comparative genomic study of the thioredoxin family in photosynthetic organisms with emphasis on Populus trichocarpa. Mol Plant 2:308–322
Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278:23747–23752
Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz KJ, Issakidis-Bourguet E (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136:4088–4095
Collin VC, Eymery F, Genty B, Rey P, Havaux M (2007) Vitamin E is essential for the tolerance of Arabidopsis thaliana to metal-induced oxidative stress. Plant Cell Environ 31:244–257
Couturier J, Jacquot JP, Rouhier N (2009a) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cell Mol Life Sci 66:2539–2557
Couturier J, Koh CS, Zaffagnini M, Winger A, Gualberto JM, Corbier C, Decottignies P, Jacquot JP, Lemaire SD, Didierjean C, Rouhier N (2009b) Structure-function relationship of the chloroplastic GrxS12 with an atypical WCSYS active site. J Biol Chem 284:9299–9310
Dai S, Johansson K, Miginiac-Maslow M, Schürmann P, Eklund H (2004) Structural basis of redox signaling in photosynthesis: structure and function of ferredoxin: thioredoxin reductase and target enzymes. Photosynth Res 79:233–248
Dai S, Friemann R, Glauser DA, Bourquin F, Manieri W, Schürmann P, Eklund H (2007) Structural snapshots along the reaction pathway of ferredoxin-thioredoxin reductase. Nature 448:92–96
Dangoor I, Peled-Zehavi H, Levitan A, Pasand O, Danon A (2009) A small family of chloroplast atypical thioredoxins. Plant Physiol 149:1240–1250
Dayer R, Fischer BB, Eggen RI, Lemaire SD (2008) The peroxiredoxin and glutathione peroxidase families in Chlamydomonas reinhardtii. Genetics 179:41–57
Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107
Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709
Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244
Entus R, Poling M, Herrmann KM (2002) Redox regulation of Arabidopsis 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase. Plant Physiol 129:1866–1871
Erales J, Lignon S, Gontero B (2009) CP12 from Chlamydomonas reinhardtii, a permanent specific “chaperone-like” protein of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 284:12735–12744
Fermani S, Sparla F, Falini G, Martelli PL, Casadio R, Pupillo P, Ripamonti A, Trost P (2007) Molecular mechanism of thioredoxin regulation in photosynthetic A2B2-glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci USA 104:11109–11114
Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and rootgrowth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180
Gama F, Keech O, Eymery F, Finkemeier I, Gelhaye E, Gardeström P, Dietz KJ, Rey P, Jacquot JP, Rouhier N (2007) The mitochondrial type II peroxiredoxin from poplar. Physiol Plant 129:196–206
Gama F, Bréhélin C, Gelhaye E, Meyer Y, Jacquot JP, Rey P, Rouhier N (2008) Functional analysis and expression characteristics of chloroplastic Prx IIE. Physiol Plant 133:599–610
Gao X-H, Bedhomme M, Veyel D, Zaffagnini M, Lemaire SD (2009) Methods for analysis of protein glutathionylation and their application to photosynthetic organisms. Mol Plant 2:218–235
Geck MK, Hartman FC (2000) Kinetic and mutational analyses of the regulation of phosphoribulokinase by thioredoxins. J Biol Chem 275:18034–18039
Geck MK, Larimer FW, Hartman FC (1996) Identification of residues of spinach thioredoxin f that influence interactions with target enzymes. J Biol Chem 279:24736–24740
Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35
Gelhaye E, Navrot N, Macdonald IK, Rouhier N, Raven EL, Jacquot JP (2006) Ascorbate peroxidase-thioredoxin interaction. Photosynth Res 89:193–200
Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Héroux A, Buchanan BB, Swaminathan K, Luan S (2004) Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101:13945–13950
Goyer A, Decottignies P, Issakidis-Bourguet E, Miginiac-Maslow M (2001) Sites of interaction of thioredoxin with sorghum NADP-malate dehydrogenase. FEBS Lett 505:405–408
Gustavsson N, Kokke BP, Härndahl U, Silow M, Bechtold U, Poghosyan Z, Murphy D, Boelens WC, Sundby C (2002) A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant J 29:545–553
Hanke GT, Kimata-Ariga Y, Taniguchi I, Hase T (2004) A post genomic characterization of Arabidopsis ferredoxins. Plant Physiol 134:255–264
Herbette S, Lenne C, Leblanc N, Julien JL, Drevet JR, Roeckel-Drevet P (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. Eur J Biochem 269:2414–2420
Hirasawa M, Schürmann P, Jacquot JP, Manieri W, Jacquot P, Keryer E, Hartman FC, Knaff DB (1999) Oxidation-reduction properties of chloroplast thioredoxins, ferredoxin:thioredoxin reductase, and thioredoxin f-regulated enzymes. Biochemistry 38:5200–5205
Hodges M, Miginiac-Maslow M, Decottignies P, Jacquot JP, Stein M, Lepiniec L, Crétin C, Gadal P (1994) Purification and characterization of pea thioredoxin f expressed in Escherichia coli. Plant Mol Biol 26:225–234
Horling F, König J, Dietz KJ (2002) Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 40:491–499
Horling F, Lamkemeyer P, König J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131:317–325
Howard TP, Metodiev M, Lloyd JC, Raines CA (2008) Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability. Proc Natl Acad Sci USA 105:4056–4061
Ikegami A, Yoshimura N, Motohashi K, Takahashi S, Romano PG, Hisabori T, Takamiya K, Masuda T (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 282:19282–19291
Ito H, Iwabuchi M, Ogawa K (2003) The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol 44:655–660
Jacquot JP, Vidal J, Gadal P, Schürmann P (1978) Evidence for the existence of several enzyme specific thioredoxins in plants. FEBS Lett 96:243–246
Jacquot JP, Lopez-Jaramillo J, Miginiac-Maslow M, Lemaire S, Cherfils J, Chueca A, Lopez-Gorge J (1997a) Cysteine 153 is required for redox regulation of pea chloroplast fructose-1,6-bisphosphatase. FEBS Lett 401:143–147
Jacquot JP, Lancelin JM, Meyer Y (1997b) Thioredoxins: structure and function in plant cells. New Phytol 136:543–570
Jacquot JP, Stein M, Suzuki A, Liottet S, Sandoz G, Miginiac-Maslow M (1997c) Residue Glu-91 of Chlamydomonas reinhardtii ferredoxin is essential for electron transfer to ferredoxin-thioredoxin reductase. FEBS Lett 400:293–296
Jacquot JP, Eklund H, Rouhier N, Schürmann P (2009) Structural and evolutionary aspects of thioredoxin reductases in photosynthetic organisms. Trends Plant Sci 14:336–343
Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW, Choi YO, Kim WY, Kang JS, Cheong GW, Yun DJ, Rhee SG, Cho MJ, Lee SY (2004) Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117:625–635
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458
Johansson K, Ramaswamy S, Saarinen M, Lemaire-Chamley M, Issakidis-Bourguet E, Miginiac-Maslow M, Eklund H (1999) Structural basis for light activation of a chloroplast enzyme: the structure of sorghum NADP-malate dehydrogenase in its oxidized form. Biochemistry 38:4319–4326
Jung BG, Lee KO, Lee SS, Chi YH, Jang HH, Kang SS, Lee K, Lim D, Yoon SC, Yun DJ, Inoue Y, Cho MJ, Lee SY (2002) A Chinese cabbage cDNA with high sequence identity to phospholipid hydroperoxide glutathione peroxidases encodes a novel isoform of thioredoxin-dependent peroxidase. J Biol Chem 277:12572–12578
Kiba A, Nishihara M, Tsukatani N, Nakatsuka T, Kato Y, Yamamura S (2005) A peroxiredoxin Q homolog from gentians is involved in both resistance against fungal disease and oxidative stress. Plant Cell Physiol 46:1007–1015
Knaff DB (1996) Ferredoxin and ferredoxin-dependent enzymes. In: Yocum CF, Ort DR (eds) Advances in photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 333–361
König J, Baier M, Horling F, Kahmann U, Harris G, Schürmann P, Dietz KJ (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
König J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz KJ (2003) Reaction mechanism of plant 2-Cys peroxiredoxin. Role of the C terminus and the quaternary structure. J Biol Chem 278:24409–24420
Kopriva S, Büchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schürmann P, Schünemann V, Trautwein AX, Kroneck PM, Brunold C (2001) Plant adenosine 5′-phosphosulfate reductase is a novel iron-sulfur protein. J Biol Chem 276:42881–42886
Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schöttler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A, Weis E, Miginiac-Maslow M, Dietz KJ (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981
Lee PY, Bae KH, Kho CW, Kang S, Lee do H, Cho S, Kang S, Lee SC, Park BC, Park SG (2008) Interactome analysis of yeast glutathione peroxidase 3. J Microbiol Biotechnol 18:1364–1367
Lemaire SD (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth Res 79:305–318
Lemaire SD, Guillon B, Le Maréchal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101:7475–7480
Lemaire SD, Quesada A, Merchan F, Corral JM, Igeno MI, Keryer E, Issakidis-Bourguet E, Hirasawa M, Knaff DB, Miginiac-Maslow M (2005) NADP-malate dehydrogenase from unicellular green alga Chlamydomonas reinhardtii. A first step toward redox regulation? Plant Physiol 137:514–521
Lemaire SD, Michelet L, Zaffagnini M, Massot V, Issakidis-Bourguet E (2007) Thioredoxins in chloroplasts. Curr Genet 51:343–365
Lepistö A, Kangasjärvi S, Luomala EM, Brader G, Sipari N, Keränen M, Keinänen M, Rintamäki E (2009) Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol 149:1261–1276
Levine RL, Mosoni L, Berlett BS, Stadtman ER (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 93:15036–15040
Li M, Yang Q, Zhang L, Li H, Cui Y, Wu Q (2007) Identification of novel targets of cyanobacterial glutaredoxin. Arch Biochem Biophys 458:220–228
Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Natl Acad Sci USA 103:12631–12636
Lindahl M, Florencio FJ (2003) Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci USA 100:16107–16112
Lindahl M, Kieselbach T (2009) Disulphide proteomes and interactions with thioredoxin on the track towards understanding redox regulation in chloroplasts and cyanobacteria. J Proteomics 72:416–438
López-Jaramillo J, Chueca A, Sahrawy M, Gorge JL (1998) Hybrids from pea chloroplast thioredoxins f and m: physicochemical and kinetic characteristics. Plant J 15:155–163
Maeda K, Finnie C, Svensson B (2004) Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms. Biochem J 378:497–507
Marchand C, Le Maréchal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P (2004) New targets of Arabidopsis thioredoxins revealed by proteomics analysis. Proteomics 4:2696–2706
Marchand C, Le Maréchal P, Meyer Y, Decottignies P (2006) Comparative proteomic approaches for the isolation of proteins interacting with thioredoxin. Proteomics 24:6528–6537
Marri L, Zaffagnini M, Collin V, Issakidis-Bourguet E, Lemaire SD, Pupillo P, Sparla F, Miginiac-Maslow M, Trost P (2009) Prompt and easy activation by specific thioredoxins of calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Mol Plant 2:259–269
Marx C, Wong JH, Buchanan BB (2003) Thioredoxin and germinating barley: targets and protein redox changes. Planta 21:454–460
Mata-Cabana A, Florencio FJ, Lindahl M (2007) Membrane proteins from the cyanobacterium Synechocystis sp. PCC 6803 interacting with thioredoxin. Proteomics 7:3953–3963
Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86:419–433
Meyer Y, Siala W, Bashandy T, Riondet C, Vignols F, Reichheld JP (2008) Glutaredoxins and thioredoxins in plants. Biochim Biophys Acta 1783:589–600
Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766
Michalska J, Zaubera H, Buchanana BB, Cejudoc FJ, Geigenberger P (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci USA 106:9908–9913
Michelet L, Zaffagnini M, Marchand C, Collin V, Decottignies P, Tsan P, Lancelin JM, Trost P, Miginiac-Maslow M, Noctor G, Lemaire SD (2005) Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc Natl Acad Sci USA 102:16478–16483
Michelet L, Zaffagnini M, Vanacker H, Le Maréchal P, Marchand C, Schroda M, Lemaire SD, Decottignies P (2008) In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J Biol Chem 283:21571–21578
Miginiac-Maslow M, Lancelin JM (2002) Intrasteric inhibition in redox signaling: light activation of NADP-malate dehydrogenase. Photosyn Res 72:1–12
Miginiac-Maslow M, Issakidis E, Lemaire M, Ruelland E, Jacquot JP, Decottignies P (1997) Light-dependent activation of NADP-malate dehydrogenase: a complex process. Aust J Plant Physiol 24:529–542
Mikkelsen R, Mutenda KE, Mant A, Schürmann P, Blennow A (2005) Alpha-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 102:1785–1790
Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in plants: the first 30 years. J Proteomics 72:452–474
Moon JC, Jang HH, Chae HB, Lee JR, Lee SY, Jung YJ, Shin MR, Lim HS, Chung WS, Yun DJ, Lee KO, Lee SY (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
Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281:35039–35047
Motohashi K, Kondoh A, Stumpp MT, Hisabori T (2001) Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 98:11224–11229
Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379
Née G, Zaffagnini M, Trost P, Issakidis-Bourguet E (2009) Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: a new role for f-type thioredoxin. FEBS Lett 583:2827–2832
Noguera-Mazon V, Lemoine J, Walker O, Rouhier N, Salvador A, Jacquot JP, Lancelin JM, Krimm I (2006) Glutathionylation induces the dissociation of 1-Cys d-peroxiredoxin non-covalent homodimer. J Biol Chem 281:31736–31742
Oster U, Tanaka R, Tanaka A, Rüdiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21:305–310
Pérez-Pérez ME, Florencio FJ, Lindahl M (2006) Selecting thioredoxins for disulphide proteomics: target proteomes of three thioredoxins from the cyanobacterium Synechocystis sp. PCC 6803. Proteomics 6:186–195
Pérez-Ruiz JM, Cejudo FJ (2009) A proposed reaction mechanism for rice NADPH thioredoxin reductase C, an enzyme with protein disulfide reductase activity. FEBS Lett 583:1399–1402
Pérez-Ruiz JM, Spinola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ (2006) Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18:2356–2368
Petersson UA, Kieselbach T, García-Cerdán JG, Schröder WP (2006) The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome. FEBS Lett 580:6055–6061
Pruzinská A, Tanner G, Anders I, Roca M, Hörtensteiner S (2003) Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci USA 100:15259–15264
Raux-Deery E, Leech HK, Nakrieko KA, McLean KJ, Munro AW, Heathcote P, Rigby SE, Smith AG, Warren MJ (2005) Identification and characterization of the terminal enzyme of siroheme biosynthesis from Arabidopsis thaliana: a plastid-located sirohydrochlorin ferrochelatase containing a 2Fe-2S center. J Biol Chem 280:4713–4721
Reichheld JP, Meyer E, Khafif M, Bonnard G, Meyer Y (2005) AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS Lett 17:337–342
Rey P, Cuiné S, Eymery F, Garin J, Court M, Jacquot JP, Rouhier N, Broin M (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41:31–42
Rey P, Bécuwe N, Barrault MB, Rumeau D, Havaux M, Biteau B, Toledano MB (2007) The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J 49:505–514
Rodriguez Milla MA, Maurer A, Rodriguez Huete A, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36:602–615
Romero HM, Berlett BS, Jensen PJ, Pell EJ, Tien M (2004) Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in Arabidopsis. Plant Physiol 136:3784–3794
Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130
Rouhier N, Jacquot JP (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74:93–107
Rouhier N, Jacquot JP (2005) The plant multigenic family of thiol peroxidases. Free Radic Biol Med 38:1413–1421
Rouhier N, Gelhaye E, Sautiere PE, Brun A, Laurent P, Tagu D, Gerard J, de Faÿ E, Meyer Y, Jacquot JP (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
Rouhier N, Gelhaye E, Jacquot JP (2002) Exploring the active site of plant glutaredoxin by site-directed mutagenesis. FEBS Lett 511:145–149
Rouhier N, Gelhaye E, Jacquot JP (2004a) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266–1277
Rouhier N, Gelhaye E, Gualberto JM, Jordy MN, De Fay E, Hirasawa M, Duplessis S, Lemaire SD, Frey P, Martin F, Manieri W, Knaff DB, Jacquot JP (2004b) Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense. Plant Physiol 134:1027–1038
Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot JP, Wingsle G (2005) Identification of plant glutaredoxin targets. Antioxid Redox Signal 7:919–929
Rouhier N, Couturier J, Jacquot JP (2006a) Genome-wide analysis of plant glutaredoxin systems. J Exp Bot 57:1685–1696
Rouhier N, Vieira Dos Santos C, Tarrago L, Rey P (2006b) Plant methionine sulfoxide reductase A and B multigenic families. Photosynth Res 89:247–262
Rouhier N, Kauffmann B, Tete-Favier F, Palladino P, Gans P, Branlant G, Jacquot JP, Boschi-Muller S (2007a) Functional and structural aspects of poplar cytosolic and plastidial type a methionine sulfoxide reductases. J Biol Chem 282:3367–3378
Rouhier N, Unno H, Bandyopadhyay S, Masip L, Kim SK, Hirasawa M, Gualberto JM, Lattard V, Kusunoki M, Knaff DB, Georgiou G, Hase T, Johnson MK, Jacquot JP (2007b) Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe–2S] cluster in poplar glutaredoxin C1. Proc Natl Acad Sci USA 104:7379–7384
Rouhier N, Lemaire SD, Jacquot JP (2008a) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166
Rouhier N, Koh CS, Gelhaye E, Corbier C, Favier F, Didierjean C, Jacquot JP (2008b) Redox based anti-oxidant systems in plants: biochemical and structural analyses. Biochim Biophys Acta 1780:1249–1260
Ruelland E, Miginiac-Maslow M (1999) Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition. Trends Plant Sci 4:136–141
Ruelland E, Lemaire-Chamley M, Le Maréchal P, Issakidis-Bourguet E, Djukic N, Miginiac-Maslow M (1997) An internal cysteine is involved in the thioredoxin-dependent activation of sorghum leaf NADP-malate dehydrogenase. J Biol Chem 272:19851–19857
Sakamoto A, Tsukamoto S, Yamamoto H, Ueda-Hashimoto M, Takahashi M, Suzuki H, Morikawa H (2003) Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J 33:841–851
Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signaling 10:1235–1274
Schürmann P, Jacquot JP (2000) Plant thioredoxin system revisited. Annu Rev Plant Physiol Plant Mol Biol 51:371–400
Serrato AJ, Pérez-Ruiz JM, Spínola MC, Cejudo FJ (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
Serrato AJ, Yubero-Serrano EM, Sandalio LM, Muñoz-Blanco J, Chueca A, Caballero JL, Sahrawy M (2009) cpFBPaseII, a novel redox-independent chloroplastic isoform of fructose-1,6-bisphosphatase. Plant Cell Environ 32:811–827
Sparla F, Pupillo P, Trost P (2002) The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. J Biol Chem 277:44946–44952
Stenbaek A, Hansson A, Wulff RP, Hansson M, Dietz KJ, Jensen PE (2008) NADPH-dependent thioredoxin reductase and 2-Cys peroxiredoxins are needed for the protection of Mg-protoporphyrin monomethyl ester cyclase. FEBS Lett 582:2773–2778
Ströher E, Dietz KJ (2008) The dynamic thiol-disulphide redox proteome of the Arabidopsis thaliana chloroplast as revealed by differential electrophoretic mobility. Physiol Plant 133:566–583
Sundby C, Härndahl U, Gustavsson N, Ahrman E, Murphy DJ (2005) Conserved methionines in chloroplasts. Biochim Biophys Acta 1703:191–202
Tarrago L, Laugier E, Rey P (2009a) Protein-repairing methionine sulfoxide reductases in photosynthetic organisms: gene organization, reduction mechanisms, and physiological roles. Mol Plant 2:202–217
Tarrago L, Laugier E, Zaffagnini M, Marchand C, Le Maréchal P, Rouhier N, Lemaire SD, Rey P (2009b) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284:18963–18971
Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314
Verdoucq L, Vignols F, Jacquot JP, Chartier Y, Meyer Y (1999) In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family. J Biol Chem 274:19714–19722
Vieira Dos Santos C, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11:329–334
Vieira Dos Santos C, Cuiné S, Rouhier N, Rey P (2005) The Arabidopsis plastidic methionine sulfoxide reductase 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
Vieira Dos Santos C, Laugier E, Tarrago L, Massot V, Issakidis-Bourguet E, Rouhier N, Rey P (2007) Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Lett 581:4371–4376
Villeret V, Huang S, Zhang Y, Xue Y, Lipscomb WN (1995) Crystal structure of spinach chloroplast fructose 1, 6 biphosphatase At 2.8 Å resolution. Biochemistry 34:4299–4306
Wakao S, Benning C (2005) Genome-wide analysis of glucose-6-phosphate dehydrogenases in Arabidopsis. Plant J 41:243–256
Wenderoth I, Scheibe R, von Schaewen A (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J Biol Chem 272:26985–26990
Wendt UK, Wenderoth I, Tegeler A, von Schaewen A (2000) Molecular characterization of a novel glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). Plant J 23:723–733
Wilcox KC, Zhou L, Jordon JK, Huang Y, Yu Y, Redler RL, Chen X, Caplow M, Dokholyan NV (2009) Modifications of superoxide dismutase (SOD1) in human erythrocytes: a possible role in amyotrophic lateral sclerosis. J Biol Chem 284:13940–13947
Wong JH, Cai N, Balmer Y, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB (2004) Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches. Photochemistry 65:1629–1640
Yamaryo Y, Motohashi K, Takamiya K, Hisabori T, Ohta H (2006) In vitro reconstitution of monogalactosyldiacylglycerol (MGDG) synthase regulation by thioredoxin. FEBS Lett 580:4086–4090
Yamazaki D, Motohashi K, Kasama T, Hara Y, Hisabori T (2004) Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol 45:18–27
Yano H, Wong JH, Lee YM, Cho MJ, Buchanan BB (2001) A strategy for the identification of proteins targeted by thioredoxin. Proc Natl Acad Sci USA 98:4794–4799
Zaffagnini M, Michelet L, Marchand C, Sparla F, Decottignies P, Le Maréchal P, Miginiac-Maslow M, Noctor G, Trost P, Lemaire SD (2007) The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS J 274:212–226
Zaffagnini M, Michelet L, Massot V, Trost P, Lemaire SD (2008) Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J Biol Chem 283:8868–8876
Acknowledgments
This research was supported by grants from the ANR programs (GNP05010G and JC07_204825) to J.C., N.R., and J.P.J, and from the INRA-FORMAS cooperation program to K.C.
Author information
Authors and Affiliations
Corresponding author
Additional information
Kamel Chibani, Jérémy Couturier, and Benjamin Selles have equally contributed to the writing of this review.
Rights and permissions
About this article
Cite this article
Chibani, K., Couturier, J., Selles, B. et al. The chloroplastic thiol reducing systems: dual functions in the regulation of carbohydrate metabolism and regeneration of antioxidant enzymes, emphasis on the poplar redoxin equipment. Photosynth Res 104, 75–99 (2010). https://doi.org/10.1007/s11120-009-9501-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-009-9501-8