Abstract
Sedoheptulose-1,7-bisphosphatase (SBPase) is a Calvin Cycle enzyme exclusive to chloroplasts and is involved in photosynthetic carbon fixation. The two cysteine residues involved in its redox regulation have been identified by site-directed mutagenesis. They are four residues apart in a predicted loop between two alpha helices and probably form a disulphide bond when oxidised. Three-dimensional modelling of SBPase has been performed using crystallographic data from the structurally homologous pig fructose-1,6-bisphosphatase (FBPase). The results suggest that formation of the disulphide bridge in SBPase is directly analogous to the allosteric regulation of pig FBPase by AMP in terms of the resulting structural changes. Similar changes are thought to occur in chloroplast FBPase, which like SBPase, is also redox regulated and involved in carbon fixation. From the results presented here it appears that the same basic mechanism for the allosteric regulation of enzymic activity operates in the FBPases and SBPase but that the sites at which the regulatory ligands (AMP or thioredoxin) exert their effects are different in each
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Anderson LE, Gibbons JT and Wang X (1996a) Distribution of ten enzymes of carbon metabolism in pea (Pisum sativum) chloroplasts. Int J Plant Sci 157: 525–538
Anderson LE, Huppe HC, Li AD and Stevens FJ (1996b) Identification of a potential redox-sensitive interdomain disulfide in the sedoheptulose bisphosphatase of Chlamydomonas reinhardtii. Plant J 10: 553–560
Anderson LE, Li D, Muslin EH, Stevens FJ and Schiffer M (1997) Predicting redox-sensitive cysteines in plant enzymes by homology modelling CR. Acad Sci Paris Life Sci 320: 767–781
Blackwell JR and Horgan R (1993) A novel strategy for production of highly expressed recombinant protein in an active form. FEBS Lett 295, 10–12
Breazeale VD, Buchanan BB and Wolosiuk R (1978) Chloroplast sedoheptulose 1,7-bisphosphatase: Evidence for regulation by the ferredoxin/thioredoxin system. Z Naturforsch 33c: 521–528
Buc J, Rivière M, Gontero B, Sauve P, Meunier J-C and Ricard J (1984) Affinity chromatography, on fructose-bisphosphatase-Sepharose, of two chloroplastic thioredoxins F. Eur J Biochem 140: 199–202
Cadet F and Meunier J-C (1988) Spinach (Spinacia oleracea) chloroplast sedoheptulose-1,7-bisphosphatase. Activation and deactivation, and immunological relationship to fructose-1,6-bisphosphatase. Biochem J 253: 243–248
Deng WP and Nickoloff JA (1992) Site-directed mutagenesis of virtually any plasmid by eliminating a unique site. Anal Biochem 200: 81–88
Dzugaj A, Chu DK, El-Dorry HA and Horecker BL (1976) Isolation of the S-peptide formedon digestion of fructose 1,6-bisphosphatase with subtilisin and its non-covalent association with the enzyme protein. Biochem Biophys Res Commun 70: 638–646
Gavel Y and von Heijne G (1990) A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett 261: 455–458
Harlow E and Lane D (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, NY
Harrison EP, Willingham NM, Lloyd JC and Raines CA (1998) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204: 27–36
Jacquot J-P, Lopez-Jaramillo J, Chueca A, Cherfils J, Lemaire S, Chedozeau B, Migniac-Maslow M, Decottignies P, Wolosiuk R and Lopez-Gorge J (1995) High-level expression of recombinant pea chloroplast fructose-1,6-bisphosphatase and mutagenesis of its regulatory site. Eur J Biochem 229: 675–681
Jacquot J-P, Lopez-Jaramillo J, Miginiac-Maslow M, Lemaire S, Cherfils J, Chueca A and Lopez-Gorge J (1997) Cysteine-153 is required for redox regulation of pea chloroplast fructose-1,6-bisphosphatase. FEBS Lett 401: 143–147
Lanzetta PA, Alvarez LJ, Reinach PS and Candia OA (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100: 95–97
Leyton JF, Chinelatto AM, El-Dorry HA and Bacila M (1980) Correlation of inhibition of fructose 1,6-bisphosphatase by AMP and presence of nucleotide-binding domain. Arch Biochem Biophys 202: 168–171
Li D, Stevens FJ, Schiffer M and Anderson LE (1994) Mechanism of light modulation: Identification of potential redox-sensitive cysteines distal to catalytic site in light-activated chloroplast enzymes. Biophys J 67: 29–35
Liang J-Y, Zhang Y, Huang S and Lipscomb WN (1993) Allosteric transition of fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 90: 2132–2136
Marcus F and Harrsch PB (1990) Amino acid sequence of spinach chloroplast fructose-1,6-bisphosphatase. Arch Biochem Biophys 279: 151–157
Marcus F, Edelstein I, Nishizawa AN and Buchanan BB (1980) Limited proteolysis of chloroplast fructose 1,6-bisphosphatase by subtilisin. Biochem Biophys Res Commun 97: 1304–1310
Marcus F, Edelstein I, Saidel LJ, Keim PS and Heinrikson RL (1981) The covalent structure of pig kidney fructose 1,6-bisphosphatase: sequence of the 60-residue NH2-terminal peptide produced by digestion with subtilisin. Arch Biochem Biophys 209: 687–696
Marcus F, Harrsch PB, Moberly L, Edelstein I and Latshaw SP (1987) Spinach chloroplast fructose-1,6-bisphosphatase: Identi-fication of the subtilisin-sensitive region of conserved histidines. Biochem 26: 7029–7035
Marcus F, Moberly L and Latshaw SP (1988) Comparative amino acid sequence of fructose-1,6-bisphosphatases: Identification of a region unique to the light-regulated enzyme. Proc Natl Acad Sci USA 85: 5379–5383
Martin W, Mustafa A-Z, Henze K and Schnarrenberger C (1996) Higher-plant chloroplast and cytosolic fructose-1,6-bisphosphatase isoenzymes: Origins via duplication rather than prokaryote-eukaryote divergence. Plant Mol Biol 32: 485–491
Pogell BM and McGilvery PW (1952) The proteolytic activation of fructose 1,6-diphosphatase. J Biol Chem 197: 293–302
Pontremoli S, Melloni E, De Flor A and Horecker BL (1973) Conversion of neutral to alkaline liver fructose-1,6-bisphosphatase: changes in molecular properties of the enzyme. Proc Natl Acad Sci USA 70: 661–664
Raines CA, Lloyd JC, Longstaff M, Bradley D and Dyer T (1988) Chloroplast fructose-1,6-bisphosphatase: the product of a mosaic gene. Nucleic Acids Res 16: 7931–7942
Raines CA, Lloyd JC, Willingham NM, Potts S and Dyer TA (1992) cDNA and gene sequences of wheat chloroplast sedoheptulose-1,7-bisphosphatase reveal homology with fructose-1,6-bisphosphatases. Eur J Biochem 205: 1053–1059
Sambrook J, Fritsch EF and Maniatis, T (1990) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
Sayle R (1994) Ras Win molecular graphics, Windows version 2.4
Süss K-H, Arkona C, Manteuffel R and Adler K (1993) Calvin cycle multienzyme complexes are bound to chloroplast thylakoid membranes of higher plants in situ. Proc Natl Acad Sci USA 90: 5514–5518
Traniello S, Melloni E, Sia CL and Horecker RL (1972) Rabbit liver fructose-1,6-diaphorase. Properties of the native enzyme and their modification by subtilisin. Arch Biochem Biophys 149: 222–231
Villeret V, Huang S, Zhang Y, Xue Y and Lipscomb WN (1995) Crystal structure of spinach chloroplast fructose-1,6-bisphosphatase at 2.9Å resolution. Biochem 34: 4299–4306
Zhang Y, Liang J-Y, Huang S and Lipscomb WN (1994) Toward a mechanism for the allosteric transition of pig kidney fructose-1,6-bisphosphatase. J Mol Biol 244: 609–624
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Dunford, R.P., Durrant, M.C., Catley, M.A. et al. Location of the redox-active cysteines in chloroplast sedoheptulose-1,7-bisphosphatase indicates that its allosteric regulation is similar but not identical to that of fructose-1,6-bisphosphatase. Photosynthesis Research 58, 221–230 (1998). https://doi.org/10.1023/A:1006178826976
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DOI: https://doi.org/10.1023/A:1006178826976