Summary
In the chloroplasts of eukaryotic photosynthetic cells, ferredoxin and thioredoxin are linked in a redox cascade which activates several catalysts of the Calvin cycle by molecular reduction of selected disulfide bridges. These two redox constituents are also present in Chlamydomonas reinhardtii and their properties are described. Ferredoxin is a nucleus-encoded protein synthesized as a 126 amino-acid precursor which is processed to a 94 amino-acid mature protein. In contrast with the intronless genes of ferredoxin in land plants, the C. reinhardtii ferredoxin gene (Frx1) contains a single intron and is present in very few copies. In chloroplasts, ferredoxin is located at a metabolic branchpoint. Ferredoxin distributes electrons to many biochemical pathways involving reductive chemistry; e.g. reduced ferredoxin is a substrate of the enzymes ferredoxin NADP+ oxidoreductase (FNR) and ferredoxin-thioredoxin reductase (FTR). Several characteristics of electron transfer from ferredoxin to FNR and FTR will be described. Evidence will also be presented that FNR is subject to post-translational modification (methylation) in C. reinhardtii. As in land plants, C. reinhardtii cells contain several types of thioredoxin, with different subcellular localization. Thioredoxin h is nucleus-encoded, located in the cytosol and does not require a transit sequence. On the other hand, thioredoxin m (106 amino-acids in its mature form) is also nucleus-encoded, synthesized as a precursor of 140 amino-acids and located in the chloroplast. The genes coding for the two thioredoxins (Trx1 and Trx2) have been isolated and sequenced. In addition, the molecular 3D-structures of these two proteins will be presented as well as some of their biochemical characteristics.
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Abbreviations
- DTNB:
-
5-5′ dithiobis nitrobenzoic acid
- FNR:
-
ferredoxin NADP+ oxidoreductase
- FAD:
-
flavin adenine dinucleotide
- FTR:
-
ferredoxin-thioredoxin reductase
- NADP-MDH-NADP:
-
malate dehydrogenase
- NTR:
-
NADPH dependent thioredoxin reductase
- TRX:
-
thioredoxin
References
Aliverti A, Ermanno-Corrado M and Zanetti G (1994) Involvement of lysine-88 of spinach ferredoxin-NADP+ reductase in the interaction with ferredoxin. FEBS Lett 343: 247–250
Arnon DI (1988) The discovery of ferredoxin: The photosynthetic path. Trends Biochem Sci 13: 30–33
Babiychuk E, Kushnir S, Van Montagu M, and Inze D (1994) The Arabidopsis thaliana apurinic endonuclease Arp reduces human transcription factors Fos and Jun. Proc Natl Acad Sci USA 91: 3299–303
Beck CF and Haring MA (1996) Gametic differentiation of Chlamydomonas. Intern Rev Cytol 168: 259–302
Bodenstein-Lang J, Buch A and Follmann H (1989) Animal and plant mitochondria contain specific thioredoxins. FEBS Lett 258: 22–26
Bower MS, Matias DM, Femandes-Carvalho E, Mazzurco M, Gu T, Rothstein SJ and Goring DR (1996) Two Members of the thioredoxin-h family interact with the kinase domain of a Brassica S-locus receptor kinase. Plant Cell 8: 1641–1650
Breathnach R and Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50: 349–383
Buchanan BB (1991) Regulation of the CO2 assimilation in oxygenic photosynthesis: The ferredoxin/thioredoxin system. Arch Biochem Biophys 288: 1–9
Bringloe DH, Dyer TA and Gray JC (1995) Developmental, circadian and light regulation of wheat ferredoxin gene expression. Plant Mol Biol 27: 293–306
Buchanan BB, Schurmann P and Jacquot J-P (1994) Thioredoxin and metabolic regulation. Seminars in Cell Biology 5: 285–293
Campbell WH and Gowri G (1990) Codon usage in higher plants, green algae and cyanobacteria. Plant Physiol 92: 1–11
Danon A and Mayfield SP (1994) Light-regulated translation of chloroplast messenger RN As through redox potential. Science 266: 1717–1719
Decottignies P, Schmitter JM, Jacquot J-P, Dutka S, Picaud A and Gadal P (1990) Purification, characterization and complete amino-acid sequence of a thioredoxin from a green alga Chlamydomonas reinhardtii. Arch Biochem Biophys 280: 112–121
Decottignies P, Schmitter JM, Dutka S, Jacquot J-P and Miginiac-Maslow M (1991) Characterization and primary structure of a second thioredoxin from the green alga Chlamydomonas reinhardtii. Eur J Biochem 198: 505–512
Decottignies P, Le Maréchal P, Jacquot J-P, Schmitter JM and Gadal P (1995) Primary structure and post-translational modification of ferredoxin-NADP-reductase from Chlamydomonas reinhardtii. Arch Biochem Biophys 316: 249–259
de Pascalis AR, Schürmann P. and Bosshard HR (1994) Comparison of the binding sites of plant ferredoxin for two ferredoxin-dependent enzymes. FEBS Lett 337: 217–220
Eklund H, Cambillau C, Sjöberg BM, Holmgren A, Jörnvall H, Hoög JO and Bränden CI (1984) Conformational and functional similarities between glutaredoxin and thioredoxins. EMBO J 3: 1443–1449
Elliott RC, Pedersen TJ, Fristensky B, White MJ, Dickey LF and Thompson WF (1989) Characterization of a single copy gene encoding ferredoxin I from pea Plant Cell 1: 681–690
Farah J, Frank G, Zuber H and Rochaix JD (1995) Cloning and sequencing of a cDNA clone encoding the photosystem I PsaD subunit from Chlamydomonas reinhardtii. Plant Physiol 107: 1485–1486
Florencio FJ, Gadal P, and Buchanan BB (1993) Thioredoxin-linked activation of the chloroplast and cytosolic forms of Chlamydomonas reinhardtii glutamine synthetase. Plant Physiol Biochem 31: 649–655
Franzeii LG, Rochaix JD and von Heijne G (1990) Chloroplast transit peptides from the green alga Chlamydomonas reinhardtii share features with both mitochondrial and higher plant presequences. FEBS Lett 260: 165–168
Gleason FK (1994) Thioredoxins in cyanobacteria: structure and redox regulation of enzyme activity. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 715–729. Kluwer Academic Publishers, Dordrecht
Goldschmidt-Clermont M and Rahire M (1986) Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/ oxygenase in Chlamydomonas reinhardtii. J Mol Biol 191: 421–432
Halm D and Kück U (1994) Nucleotide sequence of a cDNA encoding the chloroplast sedoheptulose-1,7-bisphosphatase from Chlamydomonas reinhardtii. Plant Physiol 104: 1101–1102
Hill KL, Li HH, Singer J and Merchant S (1991) Isolation and structural characterization of the Chlamydomonas reinhardtii gene for cytochrome c6 J Biol Chem 266: 15060–15067
Huppe HC, de Lamotte-Guéry F, Jacquot J-P and Gadal P (1990) The ferredoxin-thioredoxin system of a green alga, Chlamydomonas reinhardtii. Planta 180: 341–351
Huppe HC, Picaud A, Buchanan BB and Miginiac-Maslow M (1991) Identification of an NADP/ thioredoxin system in Chlamydomonas reinhardtii. Planta 186: 115–121
Ishiwatari Y, Honda C, Kawashima I, Nakamura S, Hirano H, Mori S, Fujiwara T, Hayashi H and Chino M (1995) Thioredoxin h is one of the major proteins in rice phloem sap. Planta 195: 456–463
Jacquot J-P, Stein M, Hodges M, and Miginiac-Maslow M (1992) PCR cloning of a nucleotidic sequence coding for the mature part of Chlamydomonas reinhardtii thioredoxin. Nucl Ac Res 20: 617
Jacquot J-P, Rivera-Madrid R, Marinho P, Kollarova M, Le Maréchal P, Miginiac-Maslow M and Meyer Y (1994) Arabidopsis thaliana NADPH thioredoxin reductase. J Mol Biol 235: 1357–1363
Jacquot J-P, Lancelin J-M and Meyer Y (1997a) Thioredoxins: Structures and functions in plant cells. New Phytologist 136: 543–570
Jacquot J-P, Stein M, Suzuki A, Liottet S, Sandoz G and Miginiac-Maslow M (1997b) Residue Glu 91 of Chlamydomonas reinhardtii ferredoxin is essential for electron transfer to ferredoxin-thioredoxin reductase. FEBS Lett 400: 293–296
Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular Cyanobacteriuin Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136
Kitayama M, Kitayama K and Togasaki RK (1994) A cDNA clone encoding a ferredoxin-NADP+ reductase from Chlamydomonas reinhardtii. Plant Physiol. 106: 1715–1716
Kooijman R (1988) Signal transduction and the regulation by light of sexual agglutinability in the green alga Chlamydomonas eugametos. Thesis of Doctorate, University of Amsterdam
Koradi R, Billeter M and Wüthrich K (1996) MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graphics 14: 51–55
Lancelin J-M, Stein M and Jacquot J-P (1993) Secondary structure and protein folding of recombinant chloroplastic thioredoxin Ch2 from the green alga Chlamydomonas reinhardtii as determined by 1HNMR J Biochem 114: 421–431
Lancelin J-M, Bally I, Arlaud GJ, Blackledge M, Cans P, Stein M and Jacquot J-P (1994) NMR structures of ferredoxin chloroplastic transit peptide from Chlamydomonas reinhardtii promoted by trifluoroethanol in aqueous solution. FEBS Lett 343: 261–266
Lancelin J-M, Gans P, Bouchayer E, Bally I, Arlaud GJ and Jacquot J-P (1996) NMR structures of a mitochondrial transit peptide from the green alga Chlamydomonas reinhardtii. FEBS Lett 391: 203–208
Matsubara H and Hase T (1983) Phylogenetic considerations of ferredoxin sequencesin plants particularly algae. In: Jensen U and Fairbrother DE (eds) Proteins and Nucleic Acids in Plants, pp 168–181. Springer-Verlag, Berlin
Mittard V, Morelle N, Brutscher B, Simorre JP, Marion D, Stein M, Jacquot J-P, Lirsac PN and Lancelin J-M (1995) 1H, 13C, 15N-NMR resonance assignments of oxidized thioredoxin h from the eukaryotic green alga Chlamydomonas reinhardtii using new methods based on two-dimensional triple-resonance NMR spectroscopy and computer-assisted backbone assignment. Eur J Biochem 229: 473–485
Mittard V, Blackledge MJ, Stein M, Jacquot J-P, Marion D and Lancelin J-M (1997) NMR structure of oxidised thioredoxin h from the eukaryotic green alga Chlamydomonas reinhardtii. Eur J Biochem 243: 374–383
Patel-King RS, Benashaki SE, Harrison A, King SM. 1996. Two functional thioredoxins containing vicinal dithiols from the Chlamydomonas reinhardtii outer dynein arm. J Biol Chem 271: 6283–6291
Piubelli L, Aliverti A, Bellintani F and Zanetti G (1996) Mutations of Glu92 in ferredoxin 1 from spinach leaves produce proteins fully functional in electron transfer but less efficient in supporting NADP+ photoreduction. Eur J Biochem 236: 465–469
Qin J, Clore CM and Gronenborn AM (1994) The high-resolution three-dimensional solution structures of the oxidized and reduced states of human thioredoxin. Structure 2: 503–522
Rivera-Madrid R, Mestres D, Marinho P, Jacquot J-P, Decottignies P, Miginiac-Maslow M and Meyer Y (1995) Evidence for five divergent thioredoxin h sequences in Arabidopsis thaliana. Proc Natl Acad Sci USA 92: 5620–5624
Rogers WJ, Hodges M, Decottignies P, Schmitter JM, Gadal P and Jacquot J-P (1992) Isolation of a cDNA fragment coding for Chlamydomonas reinhardtii ferredoxin and expression of the recombinant protein in Escherichia coli. FEBS Lett 310: 240–245
Ross SA, Zhang MX and Selman BR (1995) Role of the Chlamydomonas reinhardtii coupling factor 1 gamma-subunit cysteine bridge in the regulation of ATP synthase. J Biol Chem 270: 9813–9318
Ross SA, Zhang MX and Selman BR (1996) A role for the disulfide bond spacer region of the Chlamydomonas reinhardtii coupling factor 1 gamma-subunit in redox regulation of ATP synthase. J Bioenerg Biomembr 28: 49–57
Saarinen M, Gleason FK and Eklund H. (1995) Crystal structure of thioredoxin-2 from Anabaena. Structure 3: 1097–1108
Sahrawy M, Hecht V, Lopez-Jaramillo J, Chueca A, Chattier Y and Meyer Y (1996) Intron position as an evolutionary marker of thioredoxins and thioredoxin domains. J Mol Evol 42: 422–431
Schenk H, Klein M, Erdbrugger W, Droge W, and Schulze-Osthoff K (1994) Distinct effects of thioredoxin and antioxidants on the activation of transcriptionfactors NF-kappa B and AP-1. Proc Natl Acad Sci USA 91: 1672–1676
Smart EJ and Selman BR (1991) Isolation and characterization of a Chlamydomonas reinhardtii mutant lacking the gammasubunit of chloroplast coupling factor 1 (CF1). Mol Cell Biol 11: 5053–5058
Smart EJ and Selman BR (1993) Complementation of a Chlamydomonas reinhardtii mutant defective in the nuclear gene encoding the chloroplast coupling factor 1 (CF1) gammasubunit (atpC). J Bioenerg Biomembr 25: 275–284
Stein M, Jacquot J-P and Miginiac-Maslow M (1993) A cDNA clon eencoding Chlamydomonas reinhardtii preferredoxin. Plant Physiol 102: 1349–1350
Stein M, Chedozeau B and Jacquot J-P (1995) Cloning and sequencing of a ferredoxin gene (Genbank U29516) from Chlamydomonas reinhardtii. Plant Physiol 109: 721
Stein M, Jacquot J-P, Jeannette E, Decottignies P, Hodges M, Lancelin J-M, Mittard V, Schmitter JM and Miginiac-Maslow M (1995) Chlamydomonas reinhardtii thioredoxins; structure of thegenescoding for the chloroplastic m and cytosolic h isoforms: Expression in Escherichia coli of the recombinant proteins, purification and biochemical properties. Plant Mol Biol 28: 487–503
Studier FW and Moffat BA (1986) Use of bacteriophage T7 RNA polymerase to direct selective high level expression of cloned genes. J Mol Biol 189: 113–130
Vorst O, van Dam F, Oosterhoff-Teertstra R, Smeekens S and Weisbeek P (1990) Tissue-specific expression directed by an Arabidopsis thaliana pre-ferredoxin promoter in transgenic tobacco plants. Plant Mol Biol 14: 491–499
Weichsel A, Gadaska JR, Powis G and Montfort W (1996) Crystal structures of reduced oxidized and mutated human thioredoxins: Evidence for a regulatory homodimer. Structure 4: 735–751
Wetterauer B, Jacquot J-P and Véron M (1992) Thioredoxins from Dictyostelium discoideum are a developmentally regulated multigene family. J Biol Chem 267: 9895–9904
Wollman EE, ďAuriol L, Rimsky L, Shaw A, Jacquot J-P, Wingfield P, Graber P, Dessarps F, Robin P, Galibert F, Bertoglio J and Fradelizi D (1988) Cloning and expression of a cDNA for human thioredoxin. J Biol Chem 263: 15506–15512
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Jacquot, JP., Stein, M., Lemaire, S., Decottignies, P., Le Maréchal, P., Lancelin, JM. (1998). Molecular Aspects of Components of the Ferredoxin/Thioredoxin Systems. In: Rochaix, J.D., Goldschmidt-Clermont, M., Merchant, S. (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Advances in Photosynthesis and Respiration, vol 7. Springer, Dordrecht. https://doi.org/10.1007/0-306-48204-5_26
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DOI: https://doi.org/10.1007/0-306-48204-5_26
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