Recent Developments in Rubisco Research: Structure, Assembly, Activation, and Genetic Engineering

  • Robert T. Ramage
  • Hans J. Bohnert
Part of the NATO ASI Series book series (NSSA, volume 168)


Ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco, E.C. catalyzes the rate limiting steps in the diverging pathways of photosynthetic carbon assimilation and photorespiration. Rubisco is most likely the most abundant protein in the biosphere and it is definitely the most extensively studied plant enzyme. Recent developments in research on Rubisco have resulted in new information about several aspects of the enzyme. These include the determination of the structure of two Rubisco enzymes with different subunit stoichiometry, the identification of auxiliary systems for enzyme assembly and activation, and the application of molecular biology techniques for genetic engineering and analysis of the reactions catalyzed by Rubisco. This survey covers such recent developments while we refer to several other reviews1,2,3 which deal with the intensively studied aspects of subunit biosynthesis, reaction chemistry and activity.


Small Subunit Transit Peptide Terminal Domain Rubisco Activase Bisphosphate Carboxylase 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    H. M. Miziorko and G. H. Lorimer, Ribulose-l,5-bisphosphate carboxylase oxygenase, Ann Rev Biochem 52:507–535 (1983).PubMedCrossRefGoogle Scholar
  2. 2.
    T. J. Andrews and G. H. Lorimer, Rubisco: Structure, mechanisms, and prospects for improvement, in: “The Biochemistry of Plants, Vol. 10,” M. D. Hatch and N. K. Boardman, eds., Academic Press, San Diego, CA (1987).Google Scholar
  3. 3.
    S. Gutteridge and A. A. Gatenby, The molecular analysis of the assembly, structure and function of rubisco, in: “Oxford Surveys of Plant Molecular Biology Vol. 4,” B. J. Miflin, ed., Oxford University Press, London (1987).Google Scholar
  4. 4.
    G. Schneider, Y. Lindqvist, C-I. Branden, and G. Lorimer, Three-dimensional structure of ribulose-l,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum at 2.9 Å resolution, EMBO J 5:3409–3415 (1986).PubMedGoogle Scholar
  5. 5.
    C. Chothia, The 14th barrel rolls out, Nature 333:598–599 (1988).PubMedCrossRefGoogle Scholar
  6. 6.
    C.-I. Branden, G. Schneider, Y. Lindqvist, I. Andersson, S. Knight, and G. Lorimer, Structural and evolutionary aspects of the key enzymes in photorespiration; RuBisCO and glycolate oxidase, in.: “Cold Spring Harbor Symposia on Quantitative Biology, Vol. LII,” Cold Spring Harbor Laboratory (1987).Google Scholar
  7. 7.
    R. J. Almassy, C. A. Janson, R. Hamlin, N-H. Xuong, and D. Eisenberg, Novel subunit-subunit interactions in the structure of glutamine synthetase, Nature 323:304–309 (1986).PubMedCrossRefGoogle Scholar
  8. 8.
    M. S. Chapman, S. W. Suh, P. M. G. Curmi, D. Cascio, W. W. Smith, and D. S. Eisenberg, Tertiary structure of plant RuBisCO: Domains and their contacts, Science 241:71–74 (1988).PubMedCrossRefGoogle Scholar
  9. 9.
    D. W. Banner, A. C. Bloomer, G. A. Petsko, D. C. Phillips, C. I. Pogson, I. A. Wilson, P.H. Priddle, A. J. Furth, J. D. MMilman, R. E. Offord, J. D. Priddle, and S. G. Waley, Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5Å resolution using amino acid sequence data, Nature 255:609–614 (1975).PubMedCrossRefGoogle Scholar
  10. 10.
    J. P. Priestle, M. G. Gruetter, J. L. White, M. G. Vincent, M. Kania, E. Wilson, T. S. Jardetzky, K. Kirschner, and J. N. Jansonius, Three-dimensional structure of the bifunctional enzyme N-(5’-phosphoribosyl) anthranilate isomerase-indole-3-glycerol-phosphate synthase from Escherichia coli, Proc Natl Acad Sci USA 84:5690–5694 (1987).PubMedCrossRefGoogle Scholar
  11. 11.
    L. Lebioda and B Stec, Crystal structure of enolase indicates that enolase and pyruvate kinase evolved from a common ancestor, Nature 333:683–686 (1988).PubMedCrossRefGoogle Scholar
  12. 12.
    S. A. Nierzwicki-Bauer, S. E. Curtis, and R. Haselkorn, Cotranscription of genes encoding the small and large subunits of ribulose-l,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120, Proc Natl Acad Sci USA 81:5961–5965 (1984).PubMedCrossRefGoogle Scholar
  13. 13.
    K. Shinozaki and M. Sugiura, Genes for the large and small subunits of ribuose- 1,5-bisphosphate carboxylase/ oxygenase constitute a single operon in a cyanobacterium Anacystis nidulans 6301, Mol Gen Genet 200:27–32 (1985).CrossRefGoogle Scholar
  14. 14.
    G. W. Schmidt and M. L. Mishkind, Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts, Proc Natl Acad Sci USA 80:2632–2636 (1983).PubMedCrossRefGoogle Scholar
  15. 15.
    T. J. Andrews and B. Bailment, The function of the small subunit of ribulose bisphosphate carboxylase-oxygenase, J Biol Chem 258:7514–7518 (1983).PubMedGoogle Scholar
  16. 16.
    S. Asami, T. Takabe, T. Akazawa, and G. A. Codd, Ribulose 1,5-bisphosphate carboxylase from the halophilic cyanobacterium Aphanothece halophytica. Arch Biocem Biophv 225:713–721 (1983).CrossRefGoogle Scholar
  17. 17.
    T. J. Andrews and B. Bailment, Active-site carbamate formation and reaction-intermediate-analog binding by ribulosebisphosphate carboxylase/ oxygenase in the absence of its small subunit, Proc Natl Acad Sci USA 81:3660–3664 (1984).PubMedCrossRefGoogle Scholar
  18. 18.
    T. Takabe, A. Incharoensakdi, and T. Akazawa, Essentiality of the small subunit (B) in the catalysis of RuBP carboxylase/oxygenase is not related to substrate-binding in the large subunit (A), Biochem and Biophv Res Com 122:763–769 (1984).CrossRefGoogle Scholar
  19. 19.
    T. J. Andrews, D. M. Greenwood, and D. Yellowlees, Catalytically active hybrids formed in vitro between large and small subunits of different procaryotic ribulose bisphosphate carboxylases, Arch Biochem Biophv 234:313–317 (1984).CrossRefGoogle Scholar
  20. 20.
    T. J. Andrews and G. H. Lorimer, 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 (1985).PubMedGoogle Scholar
  21. 21.
    D. B. Jordan and R. Chollet, Subunit dissociation and reconstitution of ribulose- 1,5-bisphosphate carboxylase from Chromatium vinosum, Arch Biochem Biophv 236:487–496 (1985).CrossRefGoogle Scholar
  22. 22.
    T. J. Andrews, Catalysis by cyanobacterial ribulose-bisphosphate carboxylase large subunits in the complete absence of small subunits, J Biol Chem 263:12213–12219 (1988).PubMedGoogle Scholar
  23. 23.
    R. Barraclough and R. J. Ellis, Protein synthesis in chloroplasts IX. Assembly of newly-synthesized large subunits into ribulose bisphosphate carboxylase in isolated intact pea chloroplasts, Biochim Biophvs Acta 608:19–31 (1980).Google Scholar
  24. 24.
    M. V. Bloom, P. Milos, and H. Roy, Light-dependent assembly of ribulose-1, 5-bisphosphate carboxylase, Proc Natl Acad Sci USA 80:1013–1017 (1983).PubMedCrossRefGoogle Scholar
  25. 25.
    S. M. Hemmingsen and R. J. Ellis, Purification and properties of ribulose bisphosphate carboxylase large subunit binding protein, Plant Physiol 80:269–276 (1986).PubMedCrossRefGoogle Scholar
  26. 26.
    R. J. Ellis and S. M. van der Vies, The rubisco subunit binding protein, Photosyn Res 16:101–115 (1988).CrossRefGoogle Scholar
  27. 27.
    J. E. Musgrove, R. A. Johnson, and R. J. Ellis, Dissociation of the ribulose bisphosphate-carboxylase large-subunit binding protein into dissimilar subunits, Eur J Biochem 163:529–534 (1987).PubMedCrossRefGoogle Scholar
  28. 28.
    S. M. Hemmingsen, C. Woolford, S. M. van der Vies, K. Tilly, D. T. Dennis, C. P. Georgopoulos, R. W. Hendrix, and R. J. Ellis, Homologous plant and bacterial proteins chaperone oligomeric protein assembly, Nature 333:330–334 (1988).PubMedCrossRefGoogle Scholar
  29. 29.
    S. Cannon, P. Wang, and H. Roy, Inhibition of ribulose bisphosphate carboxylase assembly by antibody to a binding protein, J Cell Biol 103:1327–1335 (1986).PubMedCrossRefGoogle Scholar
  30. 30.
    J. Ellis, Proteins as molecular chaperones, Nature 328:378–379 (1987).PubMedCrossRefGoogle Scholar
  31. 31.
    G. W. Schmidt and M. L. Mishkin, The transport of proteins into chloroplasts, Ann Rev Biochem 55:879–912 (1986).PubMedCrossRefGoogle Scholar
  32. 32.
    N-H. Chua and G. W. Schmidt, Post-translational transport into intact chloroplasts of a precursor to the small subunit of ribulose-l,5-bisphosphate carboxylase, Proc Natl Acad Sci USA 75:6110–6114 (1978).PubMedCrossRefGoogle Scholar
  33. 33.
    R. Broglie, G. Coruzzi, R. T. Fraley, S. G. Rogers, R. B. Horsch, J. G. Niedermeyer, C. L. Fink, J. S. Flick, and N-H. Chua, Light-regulated expression of a pea ribulose-l,5-bisphosphate carboxylase small subunit gene in transformed plant cells, Science 224:838–843 (1984).PubMedCrossRefGoogle Scholar
  34. 34.
    C. C. Wasmann, R. T. Ramage, H. J. Bohnert, and J. A. Ostrem, Identification of an assembly domain in the small subunit of ribulose-l,5-bisphosphate carboxylase, Proc Natl Acad Sci USA (in press).Google Scholar
  35. 35.
    F. P. Wolter, C. C. Fritz, L. Willmitzer, J. Schell, and P. H. Schreier, rbcS genes in Solanum tuberosum: Conservation of transit peptide and exon shuffling during evolution, Proc Natl Acad Sci USA 85:846–850 (1988).PubMedCrossRefGoogle Scholar
  36. 36.
    D. B. Jordan and R. Chollet, Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate, J Biol Chem 258:13752–13758 (1983).PubMedGoogle Scholar
  37. 37.
    A. Brooks and A. R. Portis Jr., Protein-bound ribulose bisphosphate correlates with deactivation of ribulose bisphosphate carboxylase in leaves, Plant Phvsiol 87:244–249 (1988).CrossRefGoogle Scholar
  38. 38.
    T. J. Andrews and K. M. Abel, Kinetics and subunit interactions of ribulose bisphosphate carboxylase-oxygenase from the cyanobacterium, Svnechococcus sp. J Biol Chem 256:8445–8451 (1981).PubMedGoogle Scholar
  39. 39.
    J. R. Seeman, J. A. Berry, S. Freas, and M. A. Krump, Regulation of ribulose bisphosphate carboxylase activity in vivo by a light-modulated inhibitor of catalysis, Proc Natl Acad Sci USA 82:8024–8028 (1985).CrossRefGoogle Scholar
  40. 40.
    J. C. Servaites, Binding of a phsyiological inhibitor to ribulose bisphosphate carboxylase/oxygenase during the night, Plant Physiol 78:839–843 (1985).PubMedCrossRefGoogle Scholar
  41. 41.
    S. Gutteridge, M. A. J. Parry, S. Burton, A. J. Keys, A. Mudd, J. Feeney, J. C. Servaites, and J. Pierce, A nocturnal inhibitor of carboxylation in leaves, Nature 324:274–276 (1986).CrossRefGoogle Scholar
  42. 42.
    J. A. Berry, G. H. Lorimer, J. Pierce, J. R. Seeman, J. Meek, and S. Freas, Isolation, identification and synthesis of 2’-carboxy arabinitol-1-phosphate, a diurnal regulator of ribulose bisphosphate carboxylase activity, Proc Natl Acad Sci USA 84:734–738 (1987).PubMedCrossRefGoogle Scholar
  43. 43.
    H-H. Yeoh, M. R. Badger, and L. Watson, Variations in kinetic properties ofribulose-l,5-bisphosphate carboxylases among plants, Plant Physiol 67:1151–1155 (1981).PubMedCrossRefGoogle Scholar
  44. 44.
    J. Pierce, N. E. Tolbert, and R. Barker, Interaction of ribulosebisphosphate carboxylase/oxygenase with transition-state analogues, Biochem 19:934–942 (1980).CrossRefGoogle Scholar
  45. 45.
    J. C. Servaites, M. A. J. Parry, S. Gutteridge, and A. J. Keys, Species variation in the predawn inhibition of ribulose-1,5-bisphosphate carboxylase/oxygenase, Plant Phsiol 79:1161–1163 (1986).CrossRefGoogle Scholar
  46. 46.
    J. Kobza and J. R. Seeman, Mechanisms for light-dependent regulation of ribulose-l,5-bisphosphate carboxylase activity and photosynthesis in intact leaves, Proc Natl Acad Sci USA 85:3815–3819 (1988).PubMedCrossRefGoogle Scholar
  47. 47.
    S. P. Robinson and A. R. Portis Jr, Release of the nocturnal inhibitor carboxy arabinitol-1-phosphate, from ribulose bisphosphate carboxylase/oxygenase by rubisco activase, FEB S Lett 233:413–416 (1988).CrossRefGoogle Scholar
  48. 48.
    C. R. Somerville, A. R. Portis, and W. L. Ogren, A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo, Plant Physiol 70:381–387 (1982).PubMedCrossRefGoogle Scholar
  49. 49.
    M. E. Salvucci, J. M. Werneke, W. L. Ogren and A. R. Portis Jr., Purification and species distribiution of rubisco activase, Plant Physiol 84:930–936 (1987).PubMedCrossRefGoogle Scholar
  50. 50.
    V. J. Streusand and A. R. Portis Jr., Rubisco activase mediates ATP-dependent activation of ribulose bisphosphate carboxylase, Plant Physiol 85:152–154 (1987).PubMedCrossRefGoogle Scholar
  51. 51.
    M. A. J. Parry, A. J. Keys, C. H. Foyer, R. T. Furbank, and D. A. Walker, Regulation of ribulose-1,5-bisphosphate carboxylase activity by the activase system in lysed spinach chloroplasts, Plant Phvsiol 87:558–561 (1988).CrossRefGoogle Scholar
  52. 52.
    J. M. Werneke, R. E. Zielinski, and W. L. Ogren, Structure and expression of spinach leaf cDNA encoding ribulosebisphosphate carboxylase/oxygenase activase, Proc Natl Acad Sci USA 85:787–791 (1988).PubMedCrossRefGoogle Scholar
  53. 53.
    J. M. Werneke, J. M. Chatfield, and W. L. Ogren, Catalysis of ribulose bisphosphate carboxylase/oxygenase activation by the product of a rubisco activase cDNA clone expressed in Escherichia coli, Plant Phvsiol 87:917–920 (1988).CrossRefGoogle Scholar
  54. 54.
    R. M. Mulligan, R. L. Houtz, and N. E. Tolbert, Reaction-intermediate analogue binding by ribulose bisphosphate carboxylase/ oxygenase causes specific changes in proteolytic sensitivity: The amino-terminal residue of the large subunit is acetylated proline, Proc Natl Acad Sci USA 85:1513–1517 (1988).PubMedCrossRefGoogle Scholar
  55. 55.
    C. R. Somerville and S. C. Somerville, Cloning and expression of the Rhodospirillum rubrum ribulosebisphosphate carboxylase gene in E. coli, Mol Gen Genet 193:214–219 (1984).CrossRefGoogle Scholar
  56. 56.
    R. G. Quivey Jr. and F. R. Tabita, Cloning and expression in Escherichia coli of the form II ribulose 1,5-bisphosphate carboxylase/oxygenase gene from Rhodopseudomonas sphaeroides. Gene 31:91–101 (1984).PubMedCrossRefGoogle Scholar
  57. 57.
    J. Chory, E. D. Muller, and S. Kaplan, DNA-directed in vitro synthesis and assembly of the form II D-ribulose-1,5-bisphosphate carboxylase/ oxygenase from Rhodopseudomonas sphaeroides. J Bacteriology 161:307–313 (1985).Google Scholar
  58. 58.
    J. L. Gibson and F. R. Tabita, Isolation of the Rhodopseudomonas sphaeroides form I ribulose 1,5-bisphosphate carboxylase/ oxygenase large and small subunits genes and expression of the active hexadecameric enzyme in Escherichia coli. Gene 44:271–278 (1986).PubMedCrossRefGoogle Scholar
  59. 59.
    A. M. Viale, J. Kobayashi, T. Takabe, and T. Akazawa, Expression of genes for subunits of plant-type RuBisCO from Chromatium and production of the enzymatically active molecule in Escherichia coli, FEBS Lett 192:283–288 (1985).PubMedCrossRefGoogle Scholar
  60. 60.
    A. A. Gatenby, S. M. van der Vies, and D. Bradley, Assembly in E. coli of a functional multi-subunit ribulose bisphosphate carboxylase from a blue-green alga, Nature 314:617–620 (1985).CrossRefGoogle Scholar
  61. 61.
    J. T. Christeller, B. E. Terzaghi, D. F. Hill, and W. A. Laing, Activity expressed from cloned Anacystis nidulans large and small subunit ribulose bisphosphate carboxylase genes, Plant Mol Biol 5:257–263 (1985).CrossRefGoogle Scholar
  62. 62.
    F. R. Tabita and C. L. Small, Expression and assembly of active cyanobacterial ribulose-1,5-bisphosphate carboxylase/oxygenase in Escherichia coli containing stoichiometric amounts of large and small subunits, Proc Natl Acad Sci USA 82:6100–6103 (1985).PubMedCrossRefGoogle Scholar
  63. 63.
    M Gurevitz, C. R. Somerville, and L. Mcintosh, Pathway of assembly ofribulosebisphosphate carboxylase/oxygenase from Anabaena 7120 expressed in Escherichia coli, Proc Natl Acad Sci USA 82:6546–6550 (1985).PubMedCrossRefGoogle Scholar
  64. 64.
    S. M. van der Vies, D. Bradley, and A. A. Gatenby, 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 (1986).PubMedGoogle Scholar
  65. 65.
    A. A. Gatenby, The properties of the large subunit of maize ribulose bisphosphate carboxylase/oxygenase synthesized in Escherichia coli, Eur J Biochem 144:361–366 (1984).PubMedCrossRefGoogle Scholar
  66. 66.
    A. A. Gatenby, S. M. van der Vies, S. J. Rothstein, Co-expression of both the maize large and wheat small subunit genes of ribulose-bisphosphate carboxylase in Escherichia coli. Eur J Biochem 168:227–231 (1987).PubMedCrossRefGoogle Scholar
  67. 67.
    G. Voordouw, P. A. de Vries, W. A. M. van den Berg, and E. P. J. de Clerck, Site-directed mutagenesis of the small subunit of ribulose-1,5-bisphosphate carboxylase/ oxygenase from Anacystis nidulans.Eur J Biochem 163:591–598 (1987).PubMedCrossRefGoogle Scholar
  68. 68.
    C. A. Kettleborough, M. A. J. Parry, S. Burton, S. Gutteridge, A. J. Keys, and A. L. Philips, 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 (1987).PubMedCrossRefGoogle Scholar
  69. 69.
    C. C. Wasmann, B. Reiss, S. G. Bartlett, and H. J. Bohnert, The importance of the transit peptide and the transported protein for protein import into chloroplasts, Mol Gen Genet 205:446–453 (1986).CrossRefGoogle Scholar
  70. 70.
    P. H. Schreier, E. A. Seftor, J. Schell, and H. J. Bohnert, The use of nuclear-encoded sequences to direct the light-regulated synthesis and transport of a foreign protein into plant chloroplasts, EMBO J 4:25–32 (1985).PubMedGoogle Scholar
  71. 71.
    G. van den Broeck, M. P. Timko, A. P. Kausch, A. R. Cashmore, M. van Montagu, and L. Herrera-Estrella, Targeting of a foreign protein to chlorplasts by fusion to the transit peptide from the small subunit of ribulose 1,5-bisphosphate carboxylase, Nature 313:358–363 (1985).PubMedCrossRefGoogle Scholar
  72. 72.
    Z. Chen, C. J. Chastain, S. R. Al-Abed, R. Chollet, and R. J. Spreitzer, Reduced CO2/O2 specificity of ribulose-bisphosphate carboxylase/ oxygenase in a temperature-sensitive chloroplast mutant of Chlamydomonas, Proc Natl Acad Sci USA 85:4696–4699 (1988).PubMedCrossRefGoogle Scholar
  73. 73.
    T. C. Tso and S. D. Kung, Soluble proteins in tobacco and their potential use, in: “Leaf Protein Concentrates,” L. Telek and H. D. Graham, eds., AVI Publishing Co., Inc, Westport, CN (1983).Google Scholar
  74. 74.
    B. Ranty, D. Roby, G. Cavelie, and M.-T. Esquerre-Tugaye, Ribulose-1,5 bisphosphate carboxylase/oxygenase expression in melon plants infected with Colletotrichum lagenarium, Planta 170:386–391 (1987).CrossRefGoogle Scholar
  75. 75.
    F. Nargang, L. Mcintosh, and C. Somerville, Nucleotide sequence of the ribulosebisphosphate carboxylase gene from Rhodospirillum rubrum, Mol Gen Genet 193:220–224 (1984).CrossRefGoogle Scholar
  76. 76.
    K. Shinozaki, C. Yamada, N. Takahata, and M. Sugiura, Molecular cloning and sequence analysis of the cyanobacterial gene for the large subunit of ribulose-l,5-bisphosphate carboxylase/ oxygenase, Proc Natl Acad Sci USA 80:4050–4054 (1983).PubMedCrossRefGoogle Scholar
  77. 77.
    K. Shinozaki and M. Sugiura, The nucleotide sequence of the tobacco chloroplast gene for the large subunit of ribulose- 1,5-bisphosphate carboxylase/ oxygenase, Gene 20:91–102 (1982).PubMedCrossRefGoogle Scholar
  78. 78.
    K. Andersen and J. Caton, Sequence analysis of the Alcaligenes eutrophus chromosomally encoded ribulose bisphosphate carboxylase large and small subunit genes and their gene products, J Bacteriol 169:4547–4558 (1987).PubMedGoogle Scholar
  79. 79.
    K Shinozaki and M Sugiura, The gene for the small subunit of ribulose-1,5 bisphosphate carboxylase/ oxygenase is located close to the gene for the large subunit in the cyanobacterium Anacystis nidulans 6301, Nucleic Acids Res 11:6957–6964 (1983).PubMedCrossRefGoogle Scholar
  80. 80.
    C. C. Wasmann, Ph D thesis, Michigan State University, East Lancing Michigan, (1985).Google Scholar
  81. 81.
    A. Sailland, I. Amiri, and G. Freyssinet, Amino acid sequence of the ribulose-1,5-bisphosphate carboxylase/ oxygenase small subunit from Euglena, Plant Mol Biol 7:213–218 (1986).CrossRefGoogle Scholar
  82. 82.
    M Goldschmidt-Clermont and M. Rahire, Sequence, evolution and differential expression of the two genes encoding varitant small subunits of ribulose bisphosphate carboxylase/ oxygenase in Chlamydomonas reinhardtii, J Mol Biol 191:421–432 (1986).PubMedCrossRefGoogle Scholar
  83. 83.
    C. L. Baszczynski, L. Fallis and G. Bellemare, Nucleotide sequence of a full length cDNA clone of a Brassica napus ribulose bisphosphate carboxylase-oxygenase small subunit gene, Nucleic Acids Res 16:4732 (1988).PubMedCrossRefGoogle Scholar
  84. 84.
    M. Matsuoka, Y. Kano-Murakami, Y. Tanaka, Y. Ozeki and N. Yamamoto, Nucleotide sequence of cDNA encoding the small subunit of ribulose-1,5 bisphosphate carboxylase from maize, J. Biochem 102:673–676 (1987).PubMedGoogle Scholar
  85. 85.
    G. Coruzzi, R. Broglie, A. Cashmore and N-H. Chua, Nucleotide sequences of two pea cDNA clones encoding the small subunit of ribulose-1,5-bisphosphate carboxylase and the major chlorophyll a/b-binding thylakoid polypeptide, J Biol Chem 258:1399–1402 (1983).PubMedGoogle Scholar
  86. 86.
    S. L. Berry-Lowe, T. D. McKnight, D. M. Shah and R. B. Meagher, The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean, J Mol Appl Gen 1:483–498 (1982).Google Scholar
  87. 87.
    G. Waksman and G. Freyssinet, Nucleotide sequence of a cDNA encoding the ribulose-1,5-bisphosphate carboxylase/ oxygenase from sunflower (Helianthus annuus). Nucleic Acids Res 15:1328 (1987).PubMedCrossRefGoogle Scholar
  88. 88.
    E. J. DeRocher, R. T. Ramage, C. B. Michalowski and H. J. Bohnert, Nucleotide sequence of a cDNA encoding rbcS from the desert plant Mesembryanthemum crystallinum, Nucleic Acids Res 15:6301 (1987).PubMedCrossRefGoogle Scholar
  89. 89.
    C. A. Adams, M. Babcock, F. Leung and S. M. Sun, Sequence of a ribulose 1,5-bisphosphate carboxylase/ oxygenase cDNA from the C4 dicot Flaveria rinervia. Nucleic Acids Res 15:1875 (1987).PubMedCrossRefGoogle Scholar
  90. 90.
    P. Dunsmuir, S. Smith and J. Bedbrook, A number of different nuclear genes for the small subunit of RuBPCase are transcribed in petunia, Nucleic Acids Res 11:4177–4183 (1983).PubMedCrossRefGoogle Scholar
  91. 91.
    B. J. Mazur and C-F. Chui, Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco, Nucleic Acids Res 13:2373–2386 (1985).PubMedCrossRefGoogle Scholar
  92. 92.
    S. Gutteridge, I. Sigal, B. Thomas, R. Arentzen, A. Cordova, and G. Lorimer, A site-specific mutation within the active site of ribulose-1,5-bisphosphate carboxylase of Rhodo spirillum rubrum, EMBQ J 3:2737–2743 (1984).Google Scholar
  93. 93.
    M. Estelle, J. Hanks, L. Mcintosh, and C. Somerville, Site-specific mutagenesis of ribulose-1,5-bisphosphate carboxylase/ oxygenase, J Biol Chem 260:9523–9526 (1985).PubMedGoogle Scholar
  94. 94.
    S. K. Niyogi, R. S. Foote, R. J. Mural, F. W. Larimer, S. Mitra, T. S. Soper, R. Machanoff, and F. C. Hartman, Nonessentiality of histidine 291 of Rhod spirillum rubrum ribulose-bisphosphate carboxylase/ oxygenase as determined by site-directed mutagenesis, J Biol Chem 261:10087–10092 (1986).PubMedGoogle Scholar
  95. 95.
    B. E. Terzaghi, W. A. Laing, J. T. Christeller, G. B. Petersen, and D. F. Hill, Ribulose 1,5-bisphosphate carboxylase: Effect on the catalytic properties of changing methionine-330 to leucine in the Rhodo spirillum rubrum enzyme, Biochem J 235:839–846 (1986).PubMedGoogle Scholar
  96. 96.
    F. C. Hartman, T. S. Soper, S. K. Niyogi, R. J. Mural, R. S. Foote, S. Mitra, E. H. Lee, R. Machanoff, and F. W. Larimer, Function of Lys-166 of Rhodo spirillum rubrum ribulosebisphosphate carboxylase/ oxygenase as examined by site-directed mutagenesis, J Biol Chem 262:3496–3501 (1987).PubMedGoogle Scholar
  97. 97.
    E. H. Lee, T. S. Soper, R. J. Mural, C. D. Stringer, and F. C. Hartman, An intersubunit interaction at the active site of D-ribulose-1,5-bisphosphate carboxylase/ oxgenase as revealed by cross-linking and site-directed mutagenesis, Biochem 26:4599–4604 (1987).CrossRefGoogle Scholar
  98. 98.
    F. C. Hartman, F. W. Larimer, R. J. Mural, R. Machanoff, and T. S. Soper, Essentiality of Glu-48 of ribulose bisphosphate carboxylase/ oxygenase as demonstrated by site-directed mutagenesis, Biochem Biophy Res Com 145:1158–1163 (1987).CrossRefGoogle Scholar
  99. 99.
    F. W. Larimer, E. H. Lee, R. J. Mural, T. S. Soper, and F. C. Hartman, Intersubunit location of the active site of ribulose-bisphosphate carboxylase/ oxygenase as determined by in vivo hybridization of site-directed mutants, J Biol Chem 262:15327–15329 (1987).PubMedGoogle Scholar
  100. 100.
    H. B. Smith and F. C. Hartman, Restoration of activity to catalytically deficient mutnats of ribulosebisphosphate carboxylase/ oxygenase by aminoethylation, J. Biol Chem. 263:4921–4925 (1988).PubMedGoogle Scholar
  101. 101.
    G. H. Lorimer and F. C. Hartman, Evidence supporting Lysine 166 of Rhodo spirillum rubrum ribulosebisphosphate carboxylase as the essential base which initiates catalysis, J. Biol. Chem. 263:6468–6471 (1988).PubMedGoogle Scholar
  102. 102.
    G. H. Lorimer, S. Gutteridge, and M. Madden, Exploring the active-site of Rubisco using partial reactions and site-direct mutants, with guidance from crysallography, abstract 1–01–2 from XIV International Botanical Congress, Berlin, July 24-Aug 1, 1987.Google Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • Robert T. Ramage
    • 1
  • Hans J. Bohnert
    • 1
    • 2
  1. 1.Department of BiochemistryUniversity of ArizonaTucsonUSA
  2. 2.Departments of Molecular and Cellular Biology and Plant SciencesUniversity of ArizonaTucsonUSA

Personalised recommendations