Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family

Plant Cell

Volumn 8, Issue 3, 1996, Pages 539-553

  Rowan, Rob ^a,b,d   Whitney, Spencer M ^c   Fowler, Amanda ^c   Yellowlees, David ^c  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^c JAMES COOK UNIVERSITY   (Australia)

^d UNIVERSITY OF GUAM MARINE LABORATORY   (Guam)

Author keywords

[No Author keywords available]

Indexed keywords

BIVALVIA; DINOPHYCEAE; EUKARYOTA; RHODOSPIRILLUM RUBRUM; SYMBIODINIUM; TRIDACNA GIGAS;

RIBULOSEBISPHOSPHATE CARBOXYLASE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOSYNTHESIS; BIVALVE; CELL NUCLEUS; CHEMISTRY; COMPARATIVE STUDY; DINOFLAGELLATE; ENZYMOLOGY; GENE; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RESTRICTION MAPPING; RHODOSPIRILLUM RUBRUM; SEQUENCE HOMOLOGY; SYMBIOSIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BIVALVIA; CELL NUCLEUS; CLONING, MOLECULAR; DINOFLAGELLIDA; GENES, PROTOZOAN; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; POLYMERASE CHAIN REACTION; RESTRICTION MAPPING; RHODOSPIRILLUM RUBRUM; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SEQUENCE HOMOLOGY, AMINO ACID; SYMBIOSIS;

EID: 0030096623     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.8.3.539     Document Type: Article

References (69)

1. Andersen, K., and Caton, J. (1987). 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.
2. Andrews, T.J., Lorimer, G.H., and Tolbert, N.E. (1973). Ribulose diphosphate oxygenase. I. Synthesis of phosphoglycolate by fraction-1 protein of leaves. Biochemistry 12, 11-18.
3. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K., eds (1989). Current Protocols in Molecular Biology. (New York: John Wiley and Sons).
4. Beardall, J. (1989). Photosynthesis and photorespiration in marine phytoplankton. Aquat. Bot. 34, 105-130.
5. Blank, R.J. (1987). Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa. Mar. Biol. 94, 143-155.
6. Blank, R.J., and Trench, R.K. (1985). Speciation and symbiotic dinoflagellates. Science 229, 656-658.
7. Blank, R.J., Huss, V.A.R., and Kersten, W. (1988). Base composition of DNA from symbiotic dinoflagellates: A tool for phylogenetic classification. Arch. Microbiol. 149, 515-520.
8. Brändén, C.-I., Lindqvist, Y., and Schneider, G. (1991). Protein engineering of rubisco. Acta Crystallogr. B 47, 824-835.
9. Cavalier-Smith, T. (1992). The number of symbiotic origins of organelles. BioSystems 28, 91-106.
10. Chan, R.L., Keller, M., Canaday, J., Weil, J.-H., and Imbault, P. (1990). Eight small subunits of Euglena ribulose 1-5 bisphosphate carboxylase/oxygenase are translated from a large mRNA as a polyprotein. EMBO J. 9, 333-338.
11. Chang, S.S., Prezlin, B.B., and Trench, R.K. (1983). Mechanisms of photoadaption in three strains of symbiotic dinoflagellate Symbiodinium microadriaticum. Mar. Biol. 76, 219-229.
12. Coleman, A.W. (1980). Enhanced detection of bacteria in natural environments by fluorochrome staining of DNA. Limnol. Oceanogr. 25, 948-951.
13. Crossland, C.J., and Barnes, D.J. (1977). Gas-exchange studies with staghorn coral Acropora acuminata and its zooxanthellae. Mar. Biol. 40, 185-194.
14. 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.
15. Dykens, J.A., and Shick, J.M. (1982). Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297, 579-580.
16. Fenchel, T., and Bernard, C. (1993). A purple protist. Nature 362, 300.
17. Gibbs, S.P. (1990). The evolution of algal chloroplasts. In Experimental Phycology, Vol. 1, Cell Walls and Surfaces, Reproduction, Photosynthesis, W. Wiessner, D.G. Robinson, and R.C. Starr, eds (Berlin: Springer-Verlag), pp. 145-157.
18. Guillard, R.R.L. (1975). Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals, W.L. Smith and M.H. Chanley, eds (New York: Plenum), pp. 29-59.
19. Hartman, F.C., and Harpel, M.R. (1994). Structure, function, regulation, and assembly of D-ribulose-1,5-bisphosphate carboxylase/ oxygenase. Annu. Rev. Biochem. 63, 197-234.
20. 4-pathway of photosynthesis. In Photosynthesis and Photorespiration, M.D. Hatch, C.B. Osmond, and R.O. Slatyer, eds (New York: John Wiley and Sons), pp. 139-152.
21. Houlné, G., and Schantz, R. (1988). Characterization of cDNA sequences for LHCI apoproteins in Euglena gracilis: The mRNA encodes a large precursor containing several consecutive divergent polypeptides. Mol. Gen. Genet. 213, 479-486.
22. Houlné, G., and Schantz, R. (1993). Expression of polyproteins in Euglena. Crit. Rev. Plant Sci. 12, 1-17.
23. Jordan, D.B., and Ogren, W.L. (1981). Species variation in the specificity of ribulose 0iphosphate carboxylase/oxygenase. Nature 291, 513-515.
24. Keegstra, K., Olsen, L.J., and Theg, S.M. (1989). Chloroplastic precursors and their transport across the envelope membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 471-501.
25. Kowallik, K.V. (1992). Origin and evolution of plastids from chlorophyll-a+c-containing algae: Suggested ancestral relationships to red and green algal plastids. In Origins of Plastids, R.A. Lewin, ed (New York: Chapman and Hall), pp. 223-263.
26. Larimer, F.W., Lee, E.H., Mural, R.H., Soper, T.S., and Hartman, F.C. (1987). Inter-subunit location of the active site of ribulosebisphosphate carboxylase/oxygenase as determined by in vivo hybridization of site-directed mutants. J. Biol. Chem. 262, 15327-15329.
27. Lorimer, G.H., Badger, M.R, and Andrews, T.J. (1976). The activation of ribulose-1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry 15, 529-536.
28. Martin, W., Somerville, C.C., and Loiseaux-de Goer, L. (1992). Molecular phylogenies of plastid origins and algal evolution. J. Mol. Evol. 35, 385-404.
29. McLaughlln, J.J.A., and Zahl, P.A. (1959). Axenic culture of zooxanthellae from various invertebrate hosts. Ann. NY Acad. Sci. 77, 55-72.
30. Morden, C.W., Delwiche, C.F., Kushel, M., and Palmer, J.D. (1992). Gene phylogenies and the endosymbiotic origin of plastids. BioSystems 28, 75-90.
31. Morse, D., Salois, P., Markovic, P., and Hastings, J.W. (1995). A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268, 1622-1624.
32. Muchhal, U.S., and Schwartzbach, S.D. (1992). Characterization of a Euglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll a/b protein of photosystem II. Plant Mol. Biol. 18, 287-299.
33. Muscatine, L. (1980). Productivity of zooxanthellae. In Primary Productivity in the Sea, P.G. Falkowski, ed (New York: Plenum Press), pp. 381-402.
34. Narang, F., McIntosh, L., and Somerville, C. (1984). Nucleotide sequence of the ribulosebisphosphate carboxylase gene from Rhodospirillum rubrum. Mol. Gen. Genet. 193, 220-224.
35. Newman, S.M., and Cattolico, R.A. (1990). Ribulose bisphosphate carboxylase in algae: Synthesis, enzymology and evolution. Photosynth. Res. 26, 69-85.
36. Ohta, T. (1980). Evolution and Variation of Multigene Families. (Berlin: Springer-Verlag).
37. Palmer, J.D. (1985). Comparative organizations of chloroplast genomes. Annu. Rev. Genet. 19, 325-354.
38. Palmer, J.D. (1993). A genetic rainbow of plastids. Nature 364, 762-763.
39. Pierce, J., Carlson, T.J., and Williams, J.G.K. (1989). A cyanobacterial mutant requiring the expression of ribulose bisphosphate carboxylase from a photosynthetic anaerobe. Proc. Natl. Acad. Sci. USA 86, 5753-5757.
40. Read, B.A., and Tabita, F.R. (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.
41. Reith, M. (1995). Molecular biology of rhodophyte and chromophyte plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 549-575.
42. Reith, M., and Munholland, J. (1993). A high-resolution gene map of the chloroplast genome of the red alga Porphyre purpurea. Plant Cell 5, 465-475.
43. Rizzo, P.J., and Nooden, L.D. (1973). Isolation and chemical composition of dinoflagellate nuclei. J. Protozool. 20, 666-672.
44. Rowan, R. (1991). Molecular systematics of symbiotic algae. J. Phycol. 27, 661-666.
45. Rowan, R., and Knowlton, N. (1995). Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc. Natl. Acad. Sci. USA 92, 2850-2853.
46. Rowan, R., and Powers, D.A. (1991a). The molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar. Ecol. Prog. Ser. 71, 65-73.
47. Rowan, R., and Powers, D.A. (1991b). A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251, 1348-1351.
48. Rowan, R., and Powers, D.A. (1992). Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates. Proc. Natl. Acad. Sci. USA 89, 3639-3643.
49. Schiff, J.A., Schwartzbach, S.D., Osafune, T., and Hase, E. (1991). Photocontrol and processing of LHCP II apoprotein in Euglena: Possible role of Golgi and other cytoplasmic sites. J. Photochem. Photobiol. B 11, 219-236.
50. Shashidhara, L.S., Lim, S.H., Shackleton, J.B., Robinson, C., and Smith, A.G. (1992). Protein targeting across the three membranes of the Euglena chloroplast envelope. J. Biol. Chem. 267, 12885-12891.
51. Silva, E. da S. (1978). Endonuclear bacteria in two species of dinoflagellates. Protistologica 14, 113-119.
52. Spector, D.L. (1984). Dinoflagellate nuclei. In Dinoflagellates, D.L. Spector, ed (New York: Academic Press), pp. 107-147.
53. Steele, R.D. (1977). The significance of zooxanthella-containing pellets extruded by sea anemones. Bull. Mar. Sci. 27, 591-594.
54. Stoner, M.T., and Shively, J.M. (1993). Cloning and expression of the D-ribulose-1,5-bisphosphate carboxylase/oxygenase form II gene from Thiobacillus intermedius in Escherichia coli. FEMS Microbiol. Lett. 107, 287-292.
55. Streamer, M., McNeil, Y.R., and Yellowlees, D. (1993). Photosynthetic carbon dioxide fixation in zooxanthellae. Mar. Biol. 115, 195-198.
56. Tabita, F.R. (1988). Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol. Rev. 52, 155-189.
57. Taylor, D.L. (1969). Identity of zooxanthellae isolated from Pacific Tridacnidae. J. Phycol. 5, 336-340.
58. Taylor, F.J.R. (1983). Possible free-living Symbiodinium microadriaticum (Dinophyceae) in tide pools in southern Thailand. In Endocytobiology, Vol. 2, H.E.A. Schenk and W. Schwemmler, eds (Berlin: de Gruyter), pp. 1009-1014.
59. Tessier, L.H., Paulus, F., Keller, M., Vial, C., and Imbault, P. (1995). Structure and expression of Euglena gracilis nuclear rbcS genes encoding the small subunits of the ribulose 1,5-bisphosphate carboxylase/oxygenase: A novel splicing process for unusual intervening sequences? J. Mol. Biol. 245, 22-33.
60. Trench, R.K. (1987). Dinoflagellates in non-parasitic symbioses. In Botanical Monographs, Vol. 21, The Biology of Dinoflagellates, F.J.R. Taylor, ed (Oxford: Blackwell), pp. 530-570.
61. Trench, R.K. (1992). Microalgal-invertebrate symbiosis, current trends. In Encyclopedia of Microbiology, Vol. 3, J. Lederberg, ed (New York: Academic Press), pp. 129-142.
62. Viale, A.M., Kobayashi, H., and Akazawa, T. (1990). Distinct properties of Escherichia coli products of plant-type ribulose-1,5-bisphosphate carboxylase/oxygenase directed by two sets of genes from the photosynthetic bacterium Chromatium vinosum. J. Biol. Chem. 265, 18386-18392.
63. Wagner, S.J., Stevens, S.E., Jr., Nixon, B.T., Lambert, D.H., Quivey, R.G., Jr., and Tabita, F.R. (1988). Nucleotide and deduced amino acid sequence of the Rhodobacter sphaeroides gene encoding form II ribulose-1,5-bisphosphate carboxylase/oxygenase and comparison with other deduced form I and form II sequences. FEMS Microbiol. Lett. 55, 217-222.
64. Whatley, J.M. (1993). The endosymbiotic origin of chloroplasts. Int. Rev. Cytol. 44, 259-299.
65. Whitney, S.M., and Yellowlees, D. (1995). Preliminary investigations into the structure and activity of ribulose bisphosphate carboxylase from two photosynthetic dinoflagellates. J. Phycol. 31, 138-146.
66. Whitney, S.M., Shaw, D.C., and Yellowlees, D. (1995). Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the α-proteobacteria. Proc. R. Soc. Lond. B 259, 271-275.
67. 3 plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 533-594.
68. 2 form of rubisco from a marine obligately autotrophic hydrogen-oxidizing bacterium Hydrogenovibrio marinus strain MH-110. Biosci. Biotech. Biochem. 58, 1733-1737.
69. Zhang, K.Y.J., Cascio, D., and Eisenberg, D. (1994). Crystal structure of the unactivated ribulose 1,5-bisphosphate carboxylase/ oxygenase complexed with a transition state analog, 2-carboxy-D-arabinitol 1,5-bisphosphate. Protein Sci. 3, 64-69.