Abstract
The ability of thioredoxin f to form an electrostatic (non-covalent) complex, earlier found with fructose-1,6-bisphosphatase, was extended to include 27 previously unrecognized proteins functional in 11 processes of chloroplasts. The proteins were identified by combining thioredoxin f affinity chromatography with proteomic analysis using tandem mass spectrometry. The results provide evidence that an association with thioredoxin enables the interacting protein to achieve an optimal conformation, so as to facilitate: (i) the transfer of reducing equivalents from the ferredoxin/ferredoxin—thioredoxin reductase complex to a target protein; (ii) in some cases, to enable the channeling of metabolite substrates; (iii) to function as a subunit in the formation of multienzyme complexes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adler S and Modrich P (1983) T7-induced DNA polymerase. Requirement for thioredoxin sulfhydryl groups. J Biol Chem 258: 6956-6962
Akashi T, Matsumura T, Ideguchi T, Iwakiri K, Kawakatsu T, Taniguchi I and Hase T (1999) Comparison of the electrostatic binding sites on the surface of ferredoxin for two ferredoxindependent enzymes, ferredoxin-NADP(+) reductase and sulfite reductase. J Biol Chem 274: 29399-29405
Arner ESJ and Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267: 6102-6109
Balmer Y, Koller A, del Val G, Manieri W, Schürmann P and Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100: 370-375
Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31: 341-374
Buchanan BB, Schürmann P, Wolosiuk RA and Jacquot JP (2002) The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth Res 73: 215-222
Crawford NA, Yee BC, Hutcheson SW, Wolosiuk RA and Buchanan BB (1986) Enzyme regulation in C4 photosynthesis: purification, properties, and activities of thioredoxins from C4 and C3 plants.Arch Biochem Biophys 244: 1-15
Dai S, Schwendtmayer C, Schürmann, Ramaswamy S and Eklund H (2000) Redox signaling in chloroplasts: cleavage of disulfides by an iron-sulfur cluster. Science 287: 655-658
Dose MM, Hirasawa M, Kleis-SanFrancisco S, Lew EL and Knaff DB (1997) The ferredoxin-binding site of ferredoxin: nitrite oxidoreductase. Differential chemical modification of the free enzyme and its complex with ferredoxin. Plant Physiol 114: 1047-1053
Droux M, Jacquot JP, Miginiac-Maslow M, Gadal P, Huet JC, Crawford NA, Yee BC and Buchanan BB (1987) Ferredoxin- thioredoxin reductase, an iron-sulfur enzyme linking light to enzyme regulation in oxygenic photosynthesis: purification and properties of the enzyme from C3, C4 and cyanobacterial species.Arch Biochem Biophys 252: 426-439
Garcia-Sanchez MI, Gotor C, Jacquot JP, Stein M, Suzuki A and Vega JM (1997) Critical residues of Chlamydomonas reinhardtii ferredoxin for interaction with nitrite reductase and glutamate synthase revealed by site-directed mutagenesis. Eur J Biochem 250: 364-368
Goyer A, Haslekas C, Miginiac-Maslow M, Klein U, LeMarechal P, Jacquot JP, Decottignies P (2002) Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem 269: 272-282
-end processing by a high molecular weight protein complex is regulated by nuclear encoded RNA binding protein. EMBO J 15: 1132-1141
Hirasawa M, Droux M, Gray KA, Boyer JM, Davis DJ, Buchanan BB and Knaff DB (1988) Ferredoxin-thioredoxin reductase: properties of its complex with ferredoxin. Biochim Biophys Acta 935: 1-8
Huber HE, Russel M, Model P and Richardson CC (1986) Interaction of mutant thioredoxins of Escherichia coli with the gene 5protein of phage T7. The redox capacity of thioredoxin is not required for stimulation of DNA polymerase activity. J Biol Chem 261: 15006-15012
Knaff DB and Hirasawa M (1991) Ferredoxin-dependent chloroplast enzymes. Biochim Biophys Acta 1056: 93-125
Lemaire SD, Collin V, Keryer E, Quesada A and Miginiac-Maslow M (2003) Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii.FEBS Lett 543: 87-92
Lim CJ, Haller B and Fuchs JA (1985) Thioredoxin is the bacterial protein encoded by fip that is required for filamentous bacteriophage f1 assembly. J Bacteriol 161: 799-802
Mark DF and Richardson CC (1976) Escherichia coli thioredoxin: a subunit of bacteriophage T7 DNA polymerase. Proc Natl Acad Sci USA 73: 780-784
Marx C, Wong JH and Buchanan BB (2003) Thioredoxin and germinating barley: targets and protein redox changes. Planta 216: 454-460
Mestres-Ortega D and Meyer Y (1999) The Arabidopsis thaliana genome encodes at least four thioredoxins m and a new prokaryotic-like thioredoxin. Gene 240: 307-316
Modrich P and Richardson CC (1975) Bacteriophage T7 deoxyribonucleic acid replication in vitro. Bacteriophage T7 DNA polymerase: an enzyme composed of phage-and host-specific subunits. J Biol Chem 250: 5515-5522
Mora-Garcia S, Rodriguez-Suarez R and Wolosiuk RA (1998) Role of electrostatic interactions on the affinity of thioredoxin for target proteins. Recognition of chloroplast fructose-1,6-bisphosphatase by mutant Escherichia coli thioredoxins. J Biol Chem 273: 16273-16280
Motohashi K, Kondoh A, Stumpp MT and Hisabori T (2001) Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 98: 11224-11229
Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K and Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17: 2596-2606
Schürmann P (2003) Redox signaling in the chloroplast: the ferredoxin/thioredoxin system. Antioxid Redox Signal 5: 69-78
Schürmann P and Jacquot JP (2000) Plant thioredoxin system revisited. Annu Rev Plant Physiol Plant Mol Biol 51: 371-400
Soulié JM, Buc J, Rivière M and Ricard J (1985) Equilibrium binding of thioredoxin fB to chloroplastic fructose bisphosphatase.Evidence for a thioredoxin site distinct from the active site. Eur J Biochem 152: 565-568
Truong K and Ikura M(2001) The use of FRET imaging microscopy to detect protein-protein interactions and protein conformational changes in vivo. Curr Opin Struct Biol 5: 573-578
Verdoucq L, Vignols F, Jacquot JP, Chartier Y and Meyer Y (1999) In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family. J Biol Chem 274: 19714-19722
Wang X, Tang X and Anderson LE (1996) Enzyme-enzyme interaction in the chloroplast: physical evidence for association between phosphoglycerate kinase and glyceraldehydes-3-phosphate dehydrogenase in vitro. Plant Sci 117: 45-53
Yamaguchi K, von Knoblauch K and Subramanian AP (2000) The plastid ribosomal proteins. J Biol Chem 275: 28455-28465
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Balmer, Y., Koller, A., Val, G.d. et al. Proteomics Uncovers Proteins Interacting Electrostatically with Thioredoxin in Chloroplasts. Photosynthesis Research 79, 275–280 (2004). https://doi.org/10.1023/B:PRES.0000017207.88257.d4
Issue Date:
DOI: https://doi.org/10.1023/B:PRES.0000017207.88257.d4