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Questions about the complexity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase

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Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco; EC 4.1.1.39) has played a central role in our understanding of chloroplast biogenesis and photosynthesis. In particular, its catalysis of the rate-limiting step of CO2 fixation, and the mutual competition of CO2 and O2 at the active site, makes Rubisco a prime focus for genetically engineering an increase in photosynthetic productivity. Although it remains difficult to manipulate the chloroplast-encoded large subunit and nuclear-encoded small subunit of crop plants, much has been learned about the structure/function relationships of Rubisco by expressing prokaryotic genes in Escherichia coli or by exploiting classical genetics and chloroplast transformation of the green alga Chlamydomonas reinhardtii. However, the complexity of chloroplast Rubisco in land plants cannot be completely addressed with the existing model organisms. Two subunits encoded in different genetic compartments have coevolved in the formation of the Rubisco holoenzyme, but the function of the small subunit remains largely unknown. The subunits are posttranslationally modified, assembled via a complex process, and degraded in regulated ways. There is also a second chloroplast protein, Rubisco activase, that is responsible for removing inhibitory molecules from the large-subunit active site. Many of these complex interactions and processes display species specificity. This means that attempts to engineer or discover a better Rubisco may be futile if one cannot transfer the better enzyme to a compatible host. We must frame the questions that address this problem of chloroplast-Rubisco complexity. We must work harder to find the answers.

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References

  • Adam Z (1995) A mutation in the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase that reduces the rate of its incorporation into holoenzyme. Photosynth Res 43: 143–147

    Google Scholar 

  • Andersson I (1996) Large structures at high resolution: The 1.6 A crystal structure of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate. J Mol Biol 259: 160–174

    PubMed  Google Scholar 

  • Andersson I, Knight S, Schneider G, Lindqvist Y, Lundqvist T, Branden CI and Lorimer GH (1989) Crystal structure of the active site of ribulose-bisphosphate carboxylase. Nature 337: 229–234

    Article  Google Scholar 

  • Andrews TJ (1988) Catalysis by cyanobacterial ribulosebisphosphate carboxylase large subunits in the complete absence of small subunits. J Biol Chem 263: 12213–12219

    PubMed  Google Scholar 

  • Andrews TJ and Lorimer GH (1985) Catalytic properties of a hybrid between cyanobacterial large subunits and higher plant small subunits of ribulose bisphosphate carboxylase-oxygenase. J Biol Chem 260: 4632–4636

    PubMed  Google Scholar 

  • Baneyx F, Bertsch U, Kalbach CE, van der Vies SM, Soll J and Gatenby AA (1995) Spinach chloroplast cpn21 co-chaperonin possesses two functional domains fused together in a toroidal structure and exhibits nucleotide-dependent binding to plastid chaperonin 60. J Biol Chem 270: 10695–10702

    PubMed  Google Scholar 

  • Bar-Peled M, Bassham DC and Raikhel NV (1996) Transport of proteins in eukaryotic cells: More questions ahead. Plant Mol Biol 32: 223–249

    PubMed  Google Scholar 

  • Barraclough R and Ellis RJ (1980) Assembly of newly synthesized L subunits into ribulose bisphosphate carboxylase in isolated pea chloroplasts. Biochim Biophys Acta 608: 19–31

    PubMed  Google Scholar 

  • Berry JA, Lorimer GH, Pierce J, Seemann JR, Meek J and Freas S (1987) Isolation, identification, and synthesis of 2-carboxyarabinitol 1-phosphate, a diurnal regulator of ribulosebisphosphate carboxylase activity. Proc Natl Acad Sci USA 84: 734–738

    Google Scholar 

  • Bertsch U and Soll J (1995) Functional analysis of isolated cpn10 domains and conserved amino acid residues in spinach chloroplast co-chaperonin by site-directed mutagenesis. Plant Mol Biol 29: 1039–1055

    PubMed  Google Scholar 

  • Bertsch U, Soll J, Seetharam R and Viitanen PV (1992) Identification, characterization, and DNA sequence of a functional ‘double’ groES-like chaperonin from chloroplasts of higher plants. Proc Natl Acad Sci USA 89: 8696–8700

    PubMed  Google Scholar 

  • Bloom M, Milos P and Roy H (1983) Light-dependent assembly of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 80: 1013–1017

    Google Scholar 

  • Bowes G, Ogren WL and Hageman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45: 716–722

    PubMed  Google Scholar 

  • Bruggemann W (1995) Long-term chilling of young tomato plants under low light. VI. Differential chilling sensitivity of ribulose-1,5-bisphosphate carboxylase/oxygenase is linked to the oxidation of cysteine residues. Plant Cell Physiol 36: 733–736

    Google Scholar 

  • Bushnell TP, Bushnell D and Jagendorf AT (1993) A purified zinc protease of pea chloroplasts, EP1, degrades the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 103: 585–591

    PubMed  Google Scholar 

  • Charlet T, Moore BD and Seemann JR (1997) Carboxyarabinitol 1-phosphate phosphatase from leaves of Phaseolus vulgaris and other species. Plant Cell Physiol 38: 511–517

    Google Scholar 

  • Chen Z and Spreitzer RJ (1989) Chloroplast intragenic suppression enhances the low CO2/O2 specificity of mutant ribulosebisphosphate carboxylase/oxygenase. J Biol Chem 264: 3051–3053

    PubMed  Google Scholar 

  • Chen Z and Spreitzer RJ (1991) Proteolysis and transition-state analogue binding of mutant forms of ribulose-1,5-bisphosphate carboxylase/oxygenase from Chlamydomonas reinhardtii. Planta 83: 597–603

    Google Scholar 

  • Chen Z and Spreitzer RJ (1992) How various factors influence the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Photosynth Res 31: 157–164

    Google Scholar 

  • Chen Z, Green D, Westhoff C and Spreitzer RJ (1990) Nuclear mutation restores the reduced CO2/O2 specificity of ribulosebisphosphate carboxylase/oxygenase in a temperature-conditional chloroplast mutant of Chlamydomonas reinhardtii. Arch Biochem Biophys 283: 60–67

    PubMed  Google Scholar 

  • Chen Z, Hong S and Spreitzer RJ (1993) Thermal instability of ribulose-1,5-bisphosphate carboxylase/oxygenase from a temperature-conditional chloroplast mutant of Chlamydomonas reinhardtii. Plant Physiol 101: 1189–1194

    PubMed  Google Scholar 

  • Clegg MT (1993) Chloroplast gene sequences and the study of plant evolution. Proc Natl Acad Sci USA 90: 363–367

    PubMed  Google Scholar 

  • Clegg MT, Cummings MP and Durbin ML (1997) The evolution of plant nuclear genes. Proc Natl Acad Sci USA 94: 7791–7798

    PubMed  Google Scholar 

  • Cleland WW, Andrews TJ, Gutteridge S, Hartman FC and Lorimer GH (1998) Mechanism of Rubisco: The carbamate as general base. Chem Rev 98: 549–561

    PubMed  Google Scholar 

  • Cloney LP, Bekkaoui DR and Hemmingsen SM (1993) Coexpression of plastid chaperonin genes and a synthetic plant Rubisco operon in Escherichia coli. Plant Mol Biol 23: 1285–1290

    PubMed  Google Scholar 

  • Crafts-Brandner SJ, Klein RR, Klein P, Holzer R and Feller U (1996) Coordination of protein and mRNA abundance of stromal enzymes and mRNA abundances of the Clp protease subunits during senescence of Phaseolus vulgaris (L.) leaves. Planta 200: 312–318

    PubMed  Google Scholar 

  • Crafts-Brandner SJ, van de Loo FJ and Salvucci ME (1997) The two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol 114: 439–444

    PubMed  Google Scholar 

  • Day AG, Chene P and Fersht AR (1993) Role of phenylalanine-327 in the closure of loop 6 of ribulosebisphosphate carboxylase/oxygenase from Rhodospirillum rubrum. Biochemistry 32: 1940–1944

    PubMed  Google Scholar 

  • Dean C, Pichersky E and Dunsmuir P (1989) Structure, evolution, and regulation of rbcS genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40: 415–439

    Article  Google Scholar 

  • Dedonder A, Rethy R, Fredericq H, van Montagu M and Krebbers E (1993) Arabidopsis rbcS genes are differentially regulated by light. Plant Physiol 101: 801–808

    PubMed  Google Scholar 

  • Desimone M, Henke A and Wagner E (1996) Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 111: 789–796

    PubMed  Google Scholar 

  • Desimone M, Wagner E and Johanningmeier U (1998) Degradation of active-oxygen-modified ribulose-1,5-bisphosphate carboxylase/oxygenase by chloroplast proteases requires ATPhydrolysis. Planta 205: 459–466

    Google Scholar 

  • Dessauer CW and Bartlett SG (1994) Identification of a chaperonin binding site in a chloroplast precursor protein. J Biol Chem 269: 19766–19776

    PubMed  Google Scholar 

  • Eckardt NA and Portis Jr AR (1997) Heat denaturation profiles of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denatured Rubisco. Plant Physiol 113: 243–248

    PubMed  Google Scholar 

  • Eilenberg H, Beer S, Gepstein S, Geva N, Tadmor O and Zilberstein A (1991) Variability in ribulose-1,5-bisphosphate carboxylase/oxygenase small subunits and carboxylation activity in fern gametophytes grown under different light spectra. Plant Physiol 95: 298–304

    Google Scholar 

  • Esau BD, Snyder GW and Portis Jr AR (1996) Differential effects of N-and C-terminal deletions on the two activities of Rubisco activase. Arch Biochem Biophys 326: 100–105

    PubMed  Google Scholar 

  • Esquivel MG, Ferreira RB and Teixeira AR (1998) Protein degradation in C3 and C4 plants with particular reference to ribulose bisphosphate carboxylase and glycolate oxidase. J Exper Bot 49: 807–816

    Google Scholar 

  • Ewing RM, Jenkins GI and Langdale JA (1998) Transcripts of maize RbcS genes accumulate differentially in C3 and C4 tissues. Plant Mol Biol 36: 593–599

    PubMed  Google Scholar 

  • Fenton WA and Horwich AL (1997) GroEL-mediated protein folding. Protein Sci 6: 743–760

    PubMed  Google Scholar 

  • Ferreira RMB and Teixeira ARN (1992) Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. J Biol Chem 267: 7253–7257

    PubMed  Google Scholar 

  • Ferreira RMB, Franco E and Teixeira ARN (1996) Covalent dimerization of ribulose bisphosphate carboxylase subunits by UV radiation. Biochem J 318: 227–234

    PubMed  Google Scholar 

  • Fitchen JH, Knight S, Andersson I, Branden CI and McIntosh L (1990) Residues in three conserved regions of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase are required for quaternary structure. Proc Natl Acad Sci USA 87: 5768–5772

    PubMed  Google Scholar 

  • Flachmann R and Bohnert HJ (1992) Replacement of a conserved arginine in the assembly domain of ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit interferes with holoenzyme formation. J Biol Chem 267: 10576–10582

    PubMed  Google Scholar 

  • Flachmann R, Zhu G, Jensen RG and Bohnert HJ (1997) Mutations in the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase increase the formation of the misfire product xylulose-1,5-bisphosphate. Plant Physiol 114: 131–136

    PubMed  Google Scholar 

  • Furbank RT, Chitty JA, von Caemmerer S and Jenkins CLD (1996) Antisense RNA inhibition of RbcS gene expression reduces Rubisco level and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiol 111: 725–734

    PubMed  Google Scholar 

  • Garcia-Ferris C and Moreno J (1994) Oxidative modification and breakdown of ribulose-1,5-bisphosphate carboxylase/oxygenase induced in Euglena gracilis by nitrogen starvation. Planta 193: 208–215

    Google Scholar 

  • Gatenby AA, van der Vies SM and Rothstein SJ (1987) Coexpression of both the maize large and wheat small subunit genes of ribulosebisphosphate carboxylase in Escherichia coli. Eur J Biochem 168: 227–231

    PubMed  Google Scholar 

  • Gatenby AA, Lubben TH, Ahlquist P and Keegstra K (1988) Imported large subunits of ribulose bisphosphate carboxylase/oxygenase, but not imported β-ATP synthase subunits, are assembled into holoenzyme in isolated chloroplasts. EMBO J 7: 1307–1314

    Google Scholar 

  • Getzoff TP, Zhu G, Bohnert HJ and Jensen RG (1998) Chimeric Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase containing a pea small subunit protein is compromised in carbamylation. Plant Physiol 116: 695–702

    PubMed  Google Scholar 

  • Gotor C, Hong S and Spreitzer RJ (1994) Temperature-conditional nuclear mutation of Chlamydomonas reinhardtii decreases the CO2/O2 specificity of chloroplast ribulosebisphosphate carboxylase/oxygenase. Planta 193: 313–319

    Google Scholar 

  • Grimm R, Grimm M, Eckerskorn C, Pohlmeyer K, Rohl T and Soll J (1997) Postimport methylation of the small subunit of ribulose-1,5-bisphosphate carboxylase in chloroplasts. FEBS Lett 408: 350–354

    PubMed  Google Scholar 

  • Gutteridge S (1991) The relative catalytic specificities of the large subunit core of Synechococcus ribulosebisphosphate carboxylase/oxygenase. J Biol Chem 266: 7359–7362

    PubMed  Google Scholar 

  • Gutteridge S, Lorimer G and Pierce J (1988) Details of the reactions catalysed by mutant forms of rubisco. Plant Physiol Biochem 26: 675–682

    Google Scholar 

  • Harpel MR and Hartman FC (1992) Enhanced CO2/O2 specificity of a site-directed mutant of ribulosebisphosphate carboxylase/oxygenase. J Biol Chem 267: 6475–6478

    PubMed  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381: 571–580

    Article  PubMed  Google Scholar 

  • Hartman FC and Harpel MR (1994) Structure, function, regulation, and assembly of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Annu Rev Biochem 63: 197–234

    PubMed  Google Scholar 

  • Hayashi NR, Arai H, Kodama T and Igarashi Y (1997) The novel genes, cbbQ and cbbO, located downstream from the Rubisco genes of Pseudomonas hydrogenothermophila, affect the conformational states and activity of Rubisco. Biochem Biophys Res Commun 241: 565–569

    PubMed  Google Scholar 

  • He Z, von Caemmerer S, Hudson GS, Price GD, Badger MR and Andrews TJ (1997) Ribulose-1,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiol 115: 1569–1580

    PubMed  Google Scholar 

  • Hemmingsen SM, Woolford C, van der Vies SM, Tilly K, Dennis DT, Georgopoulos CP, Hendrix RW and Ellis RJ (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333: 330–334

    Article  PubMed  Google Scholar 

  • Hernandez JM, Baker SH, Lorbach SC, Shively JM and Tabita FR (1996) Deduced amino acid sequence, functional expression, and unique enzymatic properties of the form I and form II ribulose bisphosphate carboxylase/oxygenase from the chemoautotrophic bacterium Thiobacillus denitrificans. J Bacteriol 178: 347–356

    PubMed  Google Scholar 

  • Holbrook GP, Bowes G and Salvucci ME (1989) Degradation of 2-carboxyarabinitol 1-phosphate by a specific chloroplast phosphatase. Plant Physiol 90: 673–678

    Google Scholar 

  • Houtz RL, Stults JT, Mulligan RM and Tolbert NE (1989) Posttranslational modifications in the large subunit of ribulose bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 86: 1855–1859

    PubMed  Google Scholar 

  • Houtz RL, Royer M and Salvucci ME (1991) Partial purification and characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit ɛN-methyltransferase. Plant Physiol 97: 913–920

    Google Scholar 

  • Houtz RL, Poneleit L, Jones SB, Royer M and Stults JT (1992) Posttranslational modifications in the amino-terminal region of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from several plant species. Plant Physiol 98: 1170–1174

    Google Scholar 

  • Hubbs AE and Roy H (1993a) Assembly of in vitro-synthesized large subunits into ribulose bisphosphate carboxylase/oxygenase is sensitive to Cl-, requires ATP, and does not proceed when 40 large subunits are synthesized at temperatures >32 °C. Plant Physiol 101: 523–533

    PubMed  Google Scholar 

  • Hubbs AE and Roy H (1993b) Assembly of in vitro synthesized large subunits into ribulose-bisphosphate carboxylase/oxygenase: Formation and discharge of an L8-like species. J Biol Chem 268: 13519–13525

    PubMed  Google Scholar 

  • Ishida H, Nishimori Y, Sugisawa M, Makino A and Mae T (1997) The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented into 37-kDa and 16-kDa polypeptides by active oxygen in the lysates of chloroplasts from primary leaves of wheat. Plant Cell Physiol 38: 471–479

    PubMed  Google Scholar 

  • Ishida H, Shimizu S, Makino A and Mae T (1998) Light-dependent fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts isolated from wheat leaves. Planta 204: 305–309

    Article  PubMed  Google Scholar 

  • Jordan DB and Ogren WL (1981) Species variation in the specificity of ribulosebisphosphate carboxylase/oxygenase. Nature 291: 513–515

    Google Scholar 

  • Kane HJ, Viil J, Entsch B, Paul K, Morell MK and Andrews TJ (1994) An improved method for measuring the CO2/O2 specificity of ribulosebisphosphate carboxylase-oxygenase. Aust J Plant Physiol 21: 449–461

    Google Scholar 

  • Kanevski I and Maliga P (1994) Relocation of the plastid rbcL gene to the nucleus yields functional ribulose-1,5-bisphosphate carboxylase in tobacco chloroplasts. Proc Natl Acad Sci USA 91: 1969–1973

    PubMed  Google Scholar 

  • Kanevski I, Maliga P, Rhoades DF and Gutteridge S (1999) Plastome engineering of ribulose-1,5-bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119: 133–141

    PubMed  Google Scholar 

  • Kellogg EA and Juliano ND (1997) The structure and function of Rubisco and their implications for systematic studies. Amer J Bot 84: 413–428

    Google Scholar 

  • Kent SS and Tomany MJ (1995) The differential of the ribulose-1,5-bisphosphate carboxylase/oxygenase specificity factor among higher plants and the potential for biomass enhancement. Plant Physiol Biochem 33: 71–80

    Google Scholar 

  • Kettleborough CA, Parry MAJ, Burton S, Gutteridge S, Keys AJ and Phillips AL (1987) The role of the N-terminus of the large subunit of ribulosebisphosphate carboxylase investigated by construction and expression of chimaeric genes. Eur J Biochem 170: 335–342

    PubMed  Google Scholar 

  • Khrebtukova I and Spreitzer RJ (1996) Elimination of the Chlamydomonas gene family that encodes the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 93: 13689–13693

    PubMed  Google Scholar 

  • Klein RR and Houtz RL (1995) Cloning and developmental expression of pea ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit N-methyltransferase. Plant Mol Biol 27: 249–261

    PubMed  Google Scholar 

  • Kostov RV, Small CL and McFadden BA (1997) Mutations in a sequence near the N-terminus of the small subunit alter the CO2/O2 specificity factor for ribulose bisphosphate carboxylase/oxygenase. Photosynth Res 54: 127–134

    Google Scholar 

  • Laing WA, Ogren WL and Hageman RH (1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose 1,5-diphosphate carboxylase. Plant Physiol 54: 678–685

    Google Scholar 

  • Larson EM, O'Brien CM, Zhu G, Spreitzer RJ and Portis Jr AR (1997) Specificity for activase is changed by a Pro-89 to Arg substitution in the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 272: 17033–17037

    PubMed  Google Scholar 

  • Lee B, Berka RM and Tabita FR (1991) Mutations in the small subunit of cyanobacterial ribulosebisphosphate carboxylase/oxygenase that modulate interactions with large subunits. J Biol Chem 266: 7417–7422

    PubMed  Google Scholar 

  • Leegood RC, Lea PJ, Adcock MD and Hausler RE (1995) The regulation and control of photorespiration. J Exper Bot 46: 1397–1414

    Google Scholar 

  • Li LA and Tabita FR (1997) Maximum activity of recombinant ribulose 1,5-bisphosphate carboxylase/oxygenase of Anabaena sp. strain CA requires the product of the rbcX gene. J Bacteriol 179: 3793–3796

    PubMed  Google Scholar 

  • Li LA, Gibson JL and Tabita FR (1993) The Rubisco activase (rca) gene is located downstream from rbcS in Anabaena sp. strain CA and is detected in other Anabaena/Nostoc strains. Plant Mol Biol 21: 753–764

    PubMed  Google Scholar 

  • Lilley RM and Portis AR Jr (1997) ATP hydrolysis activity and polymerization state of ribulose-1,5-bisphosphate carboxylase oxygenase activase: Do the effects of Mg2+, K+, and activase concentrations indicate a functional similarity to actin? Plant Physiol 114: 605–613

    PubMed  Google Scholar 

  • Lorimer GH (1981) Ribulosebisphosphate carboxylase: Amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry 20: 1236–1240

    PubMed  Google Scholar 

  • Lubben TH, Donaldson GK, Viitanen PV and Gatenby AA (1989) Several proteins imported into chloroplasts form stable complexes with the GroEL-related chloroplast molecular chaperone. Plant Cell 1: 1223–1230

    Article  PubMed  Google Scholar 

  • Makino A, Shimada T, Takumi S, Kaneko K, Matsuoka M, Shimamoto K, Nakano H, Miyao-Tokutomi M, Mae T and Yamamoto N (1997) Does decrease in ribulose-1,5-bisphosphate carboxylase by antisense RbcS lead to a higher N-use efficiency of photosynthesis under condition of saturating CO2 and light in rice plants? Plant Physiol 114: 483–491

    PubMed  Google Scholar 

  • Martel R, Cloney LP, Pelcher LE and Hemmingsen SM (1990) Unique composition of plastid chaperonin-60: α and β polypeptide-encoding genes are highly divergent. Gene 94: 181–187

    Article  PubMed  Google Scholar 

  • Mate CJ, Hudson GS, von Caemmerer S, Evans JR and Andrews TJ (1993) Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiol 102: 1119–1128

    Article  PubMed  Google Scholar 

  • Mazarei M, Ying Z and Houtz RL (1998) Functional analysis of the Rubisco large subunit ɛN-methyltransferase promoter from tobacco and its regulation by light in soybean hairy roots. Plant Cell Reports 17: 907–912

    Google Scholar 

  • McFadden BA and Small CL (1988) Cloning, expression and directed mutagenesis of the genes for ribulosebisphosphate carboxylase/oxygenase. Photosynth Res 18: 245–260

    Google Scholar 

  • McIntosh L, Poulsen C and Bogorad L (1980) Chloroplast gene sequence for the large subunit of ribulosebisphosphate carboxylase of maize. Nature 288: 556–560

    Google Scholar 

  • Mehta RA, Fawcett TW, Porath D and Mattoo AK (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 267: 2810–2816

    Google Scholar 

  • Meier I, Callan KL, Fleming AJ and Gruissem W (1995) Organspecific differential regulation of a promoter subfamily for the ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit genes in tomato. Plant Physiol 107: 1105–1118

    PubMed  Google Scholar 

  • Moore BD, Kobza J and Seemann JR (1991) Measurement of 2-carboxyarabinitol 1-phosphate in plant leaves by isotope dilution. Plant Physiol 96: 208–213

    Google Scholar 

  • Moreno J, Penarrubia L and Garcia-Ferris C (1995) The mechanism of redox regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase turnover: A hypothesis. Plant Physiol Biochem 33: 121–127

    Google Scholar 

  • Newman J and Gutteridge S (1993) The X-ray structure of Synechococcus ribulose-bisphosphate carboxylase/oxygenaseactivated quaternary complex at 2.2 Å resolution. J Biol Chem 268: 25876–25886

    PubMed  Google Scholar 

  • Orozco BM, McClung CR, Werneke JM and Ogren WL (1993) Molecular basis of the ribulose-1,5-bisphosphate carboxylase/oxygenase activase mutation in Arabidopsis thaliana is a guanine-to-adenine transition at the 50-splice junction of intron 3. Plant Physiol 102: 227–232

    Article  PubMed  Google Scholar 

  • Parry MAJ, Schmidt CNG, Cornelius MJ, Millard BN, Burton S, Gutteridge S, Dyer TA and Keys AJ (1987) Variations in properties of ribulose-1,5-bisphosphate carboxylase from various species related to differences in amino acid sequences. J Exper Bot 38: 1260–1271

    Google Scholar 

  • Parry MAJ, Keys AJ and Gutteridge S (1989) Variation in the specificity factor of C3 higher plant Rubiscos determined by the total consumption of ribulose-P2. J Exper Bot 40: 317–320

    Google Scholar 

  • Parry MAJ, Madgwick P, Parmer S, Cornelius MJ and Keys AJ (1992) Mutations in loop six of the large subunit of ribulose-1,5-bisphosphate carboxylase affect substrate specificity. Planta 187: 109–112

    Google Scholar 

  • Parry MAJ, Andralojc PJ, Parmar S, Keys AJ, Habash D, Paul MJ, Alred R, Quick WP and Servaites JC (1997) Regulation of Rubisco by inhibitors in the light. Plant Cell Environ 20: 528–534

    Google Scholar 

  • Paul K, Morell MK and Andrews TJ (1991) Mutations in the small subunit of ribulosebisphosphate carboxylase affect subunit binding and catalysis. Biochemistry 30: 10019–10026

    PubMed  Google Scholar 

  • Pell EJ, Schlagnhaufer CD and Arteca RN (1997) Ozone induced oxidative stress: Mechanisms of action and reaction. Physiologia Plant 100: 264–273

    Google Scholar 

  • Portis AR Jr (1995) The regulation of Rubisco by Rubisco activase. J Exper Bot 46: 1285–1291

    Google Scholar 

  • Ramage RT, Read BA and Tabita FR (1998) Alteration of the α helix region of cyanobacterial ribulose 1,5-bisphosphate carboxylase/oxygenase to reflect sequences found in high substrate specificity enzymes. Arch Biochem Biophys 349: 81–88

    PubMed  Google Scholar 

  • Read BA and Tabita FR (1992a) Amino acid substitutions in the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase that influence catalytic activity of the holoenzyme. Biochemistry 31: 519–525

    PubMed  Google Scholar 

  • Read BA and Tabita FR (1992b) A hybrid ribulosebisphosphate carboxylase/oxygenase enzyme exhibiting a substantial increase in substrate specificity factor. Biochemistry 31: 5553–5559

    PubMed  Google Scholar 

  • Read BA and Tabita FR (1994) High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial Rubisco containing ‘algal’ residue modifications. Arch Biochem Biophys 312: 210–218

    Article  PubMed  Google Scholar 

  • Rochaix JD (1997) Chloroplast reverse genetics: New insights into the function of plastid genes. Trends Plant Sci 2: 419–425

    Google Scholar 

  • Rodermel SR, Abbott MS and Bogorad L (1988) Nuclear-organelle interactions: Nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55: 673–681

    Article  PubMed  Google Scholar 

  • Rodermel S, Haley J, Jiang C, Tsai C and Bogorad L (1996) A mechanism for intergenomic integration: Abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. Proc Natl Acad Sci USA 93: 3881–3885

    PubMed  Google Scholar 

  • Roesler KR and Ogren WL (1990) Primary structure of Chlamydomonas reinhardtii ribulose-1,5-bisphosphate carboxylase/oxygenase activase and evidence for a single polypeptide. Plant Physiol 94: 1837–1841

    Google Scholar 

  • Roulin S and Feller U (1998) Light-independent degradation of stromal proteins in intact chloroplasts isolated from Pisum sativum L. leaves: Requirement for divalent cations. Planta 205: 297–304

    Google Scholar 

  • Roy H, Hubbs A, Gilson M and Chaudhari P (1995) Rubisco and the chaperonins. In: Mathis (ed) Photosynthesis: From light to biosphere, Vol V, pp 53–58. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Rundle SJ and Zielinski RE (1991) Organization and expression of two tandemly oriented genes encoding ribulosebisphosphate carboxylase/oxygenase activase in barley. J Biol Chem 266: 4677–4685

    PubMed  Google Scholar 

  • Salvucci ME and Holbrook GP (1989) Purification and properties of 2-carboxy-D-arabinitol 1-phosphatase. Plant Physiol 90: 679–685

    Google Scholar 

  • Salvucci ME and Ogren WL (1996) The mechanism of Rubisco activase: Insights from studies of the properties and structure of the enzyme. Photosynth Res 47: 1–11

    Google Scholar 

  • Salvucci ME, Portis Jr AR and Ogren WL (1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res 7: 193–201

    Google Scholar 

  • Salvucci ME, Werneke JM, Ogren WL and Portis AR (1987) Purification and species distribution of Rubisco activase. Plant Physiol 84: 930–936

    Google Scholar 

  • Sanchez de Jimenez E, Medrano L and Martinez-Barajas E (1995) Rubisco activase, a possible new member of the molecular chaperone family. Biochemistry 34: 2826–2831

    PubMed  Google Scholar 

  • Schmidt GW, Devillers-Thiery A, Desruisseaux H, Blobel G and Chua NH (1979) NH2-terminal amino acid sequences of precursor and mature forms of the ribulose-1,5-bisphosphate carboxylase small subunit from Chlamydomonas reinhardtii. J Cell Biol 83: 615–622

    Article  PubMed  Google Scholar 

  • Schreuder HA, Knight S, Curmi PMG, Andersson I, Cascio D, Sweet RM, Branden CI and Eisenberg D (1993) Crystal structure of activated tobacco rubisco complexed with the reactionintermediate analogue 2-carboxyarabinitol 1,5-bisphosphate. Protein Sci 2: 1136–1146

    PubMed  Google Scholar 

  • Seemann JR, Badger MR and Berry JA (1984) Variations in the specific activity of ribulose-1,5-bisphosphate carboxylase between species utilizing differing photosynthetic pathways. Plant Physiol 74: 791–794

    Google Scholar 

  • Seemann JR, Berry JA, Freas SM and Krump MA(1985) Regulation of ribulose bisphosphate carboxylase activity in vivo by a lightmodulated inhibitor of catalysis. Proc Natl Acad Sci USA 82: 8024–8028

    Google Scholar 

  • Seemann JR, Kobza J and Moore BD (1990) Metabolism of 2-carboxyarabinitol 1-phosphate and regulation of ribulose-1,5-bisphosphate carboxylase activity. Photosynth Res 23: 119–130

    Google Scholar 

  • Servaites JC (1985) Binding of a phosphorylated inhibitor to ribulose bisphosphate carboxylase/oxygenase during the night. Plant Physiol 78: 839–843

    Google Scholar 

  • Shen JB and Ogren WL (1992) Alteration of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase activase activities by sitedirected mutagenesis. Plant Physiol 99: 1201–1207

    Google Scholar 

  • Shen JB, Orozco EM and Ogren WL (1991) Expression of the two isoforms of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase activase and essentiality of the conserved lysine in the consensus nucleotide-binding domain. J Biol Chem 266: 8963–8968

    PubMed  Google Scholar 

  • Shibata N, Inoue T, Fukuhara K, Nagara Y, Kitagawa R, Harada S, Kasai N, Uemura K, Kato K, Yokota A and Kai Y (1996) Orderly disposition of heterogeneous small subunits in D-ribulose-1,5-bisphosphate carboxylase/oxygenase from spinach. J Biol Chem 271: 26449–26452

    PubMed  Google Scholar 

  • Spreitzer RJ (1993) Genetic dissection of Rubisco structure and function. Annu Rev Plant Physiol Plant Mol Biol 44: 411–434

    Google Scholar 

  • Spreitzer RJ (1998) Genetic engineering of Rubisco. In: Rochaix JD, Goldschmidt-Clermont M and Merchant S (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, pp 515–527. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Spreitzer RJ, Thow G, Zhu G, Chen Z, Gotor C, Zhang D and Hong S (1992) Chloroplast and nuclear mutations that affect Rubisco structure and function in Chlamydomonas reinhardtii. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 593–600. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Tabita FR (1999) Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective. Photosynth Res 60: 1–28

    Google Scholar 

  • Terzaghi BE, Laing WA, Christeller JT, Petersen GB and Hill DF (1986) Ribulose-1,5-bisphosphate carboxylase: Effect on the catalytic properties of changing methionine-330 to leucine in the Rhodospirillum rubrum enzyme. Biochem J 235: 839–846

    PubMed  Google Scholar 

  • Thompson MD, Paavola CD, Lenvik TR and Gantt JS (1995) Chlamydomonas transcripts encoding three divergent plastid chaperonins are heat-inducible. Plant Mol Biol 27: 1031–1035

    PubMed  Google Scholar 

  • Uemura K, Suzuki Y, Shikanai T, Wadano A, Jensen RG, Chmara W and Yokota A (1996) A rapid and sensitive method for determination of relative specificity of RuBisCO from various species by anion-exchange chromatography. Plant Cell Physiol 37: 325–331

    Google Scholar 

  • van de Loo FJ and Salvucci ME (1998) Involvement of two aspartate residues of Rubisco activase in coordination of the ATP γ-phosphate and subunit cooperativity. Biochemistry 37: 4621–4625

    PubMed  Google Scholar 

  • van der Vies SM, Bradley D and Gatenby AA (1986) Assembly of cyanobacterial and higher plant ribulose bisphosphate carboxylase subunits into functional homologous and heterologous enzyme molecules in Escherichia coli. EMBO J 5: 2439–2444

    Google Scholar 

  • Viitanen PV, Schmidt M, Buchner J, Suzuki T, Vierling E, Dickson R, Lorimer GH, Gatenby A and Soll J (1995) Functional characterization of the higher plant chloroplast chaperonins. J Biol Chem 270: 18158–18164

    PubMed  Google Scholar 

  • Voordouw G, de Vries PA, van Den Berg WAM and de Clerck EPJ (1987) Site-directed mutagenesis of the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from Anacystis nidulans. Eur J Biochem 163: 591–598

    PubMed  Google Scholar 

  • Wang P, Royer M and Houtz RL (1995) Affinity purification of ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit ɛN-methyltransferase. Protein Expression Purification 6: 528–536

    PubMed  Google Scholar 

  • Wang X and Kolattukudy PE (1996) Isolation of a protein containing covalently linked large and small subunits of ribulose-1,5-bisphosphate carboxylase/oxygenase from Botryococcus braunii. Plant Physiol 111: 441–445

    PubMed  Google Scholar 

  • Wang ZY, Snyder GW, Esau BD, Portis Jr AR and Ogren WL (1992) Species-dependent variation in the interaction of substrate-bound ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase. Plant Physiol 100: 1858–1862

    Google Scholar 

  • Wang ZY, Ramage RT and Portis Jr AR (1993) Mg2+ and ATP or adenosine 50′-[γ-thio]-triphosphate (ATPγS) enhances intrinsic fluorescence and induces aggregation which increases the activity of spinach Rubisco activase. Biochim Biophys Acta 1202: 47–55

    PubMed  Google Scholar 

  • Wanner LA and Gruissem W (1991) Expression dynamics of the tomato rbcS gene family during development. Plant Cell 3: 1289–1303

    Article  PubMed  Google Scholar 

  • Wasmann CC, Ramage RT, Bohnert HJ and Ostrem JA (1989) Identification of an assembly domain in the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 86: 1198–1202

    PubMed  Google Scholar 

  • Werneke JM, Zielinski RE and Ogren WL (1988) Structure and expression of spinach leaf cDNA encoding ribulosebisphosphate carboxylase/oxygenase activase. Proc Natl Acad Sci USA 85: 787–791

    PubMed  Google Scholar 

  • Werneke JM, Chatfield JM and Ogren WL (1989) Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell 1: 815–825

    Article  PubMed  Google Scholar 

  • Whitney SP and Andrews TJ (1998) The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dino-flagellate, Amphidinium carterae. Aust J Plant Physiol 25: 131–138

    Google Scholar 

  • Wilson MI, Ghosh S, Gerhardt KE, Holland N, Babu TS, Edelman M, Dumbroff EB and Greenberg BM (1995) In vivo photomodification of ribulose-1,5-bisphosphate carboxylase/oxygenase holoenzyme by ultraviolet-B radiation: Formation of a 66-kilodalton variant of the large subunit. Plant Physiol 109: 221–229

    PubMed  Google Scholar 

  • Yeoh HH, Badger MR and Watson L (1981) Variations in kinetic properties of ribulose-1,5-bisphosphate carboxylases among plants. Plant Physiol 67: 1151–1155

    Google Scholar 

  • Ying Z, Janney N and Houtz RL (1996) Organization and characterization of the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit ɛ N-methyltransferase gene in tobacco. Plant Mol Biol 32: 663–671

    PubMed  Google Scholar 

  • Zabaleta E, Oropeza A, Jimenez B, Salerno G, Crespi M and Herrera-Estrella L (1992) Isolation and characterization of genes encoding chaperonin 60β from Arabidopsis thaliana. Gene 111: 175–181

    Google Scholar 

  • Zabaleta E, Oropeza A, Assad N, Mandel A, Salerno G and Herrera-Estrella L (1994) Antisense expression of chaperonin 60β in transgenic tobacco plants leads to abnormal phenotypes and altered distribution of photoassimilates. Plant J 6: 425–432

    Google Scholar 

  • Zhu G and Spreitzer RJ (1994) Directed mutagenesis of chloroplast ribulose-bisphosphate carboxylase/oxygenase: Substitutions at large-subunit asparagine 123 and serine 379 decrease CO2/O2 specificity. J Biol Chem 269: 3952–3956

    PubMed  Google Scholar 

  • Zhu G and Spreitzer RJ (1996) Directed mutagenesis of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase: Loop-6 substitutions complement for structural stability but decrease catalytic efficiency. J Biol Chem 271: 18494–18498

    PubMed  Google Scholar 

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    Robert J. Spreitzer

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Spreitzer, R.J. Questions about the complexity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase. Photosynthesis Research 60, 29–42 (1999). https://doi.org/10.1023/A:1006240202051

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