Plant Molecular Biology

, Volume 17, Issue 4, pp 853–863 | Cite as

Evolution of the Rubisco operon from prokaryotes to algae: Structure and analysis of the rbcS gene of the brown alga Pylaiella littoralis

  • Nour-Eddine Assali
  • William F. Martin
  • Charles C. Sommerville
  • Susan Loiseaux-de Goër
Article

Abstract

The rbcS gene coding for the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) of the brown alga Pylaiella littoralis is located within the plastid genome and is transcribed as a single polycistronic mRNA with the gene for the large subunit of Rubisco, rbcL. The structure of the Rubisco operon from P. littoralis was determined. Molecular phylogenies for rbcS and rbcL with a wide range of prokaryotes and eukaryotes were constructed which are congruent with recent evidence for polyphyletic plastid origins. Both rbcL and rbcS of the β-purple bacterium Alcaligenes eutrophus clearly cluster with the rhodophyte and chromophyte proteins. The data suggest that the Rubisco operons of red algal and chromophytic plastids derive from β-purple eubacterial antecedents, rather than the cyanobacterial lineage of eubacteria from which other of their genes derive. This implies a lateral transfer of Rubisco genes from β-purple eubacterial ancestors to the cyanobacterial ancestor of rhodophyte and chromophyte plastids.

Key words

algae endosymbiosis evolution plastidial DNA Rubisco operon 

References

  1. 1.
    Anderson, K, Caton, J: Sequence analysis of the Alcaligenes eutrophus chromosomally encoded ribulose bisphosphate carboxylase large and small subunit genes and their gene product. J Bact 169: 4547–4558 (1987).Google Scholar
  2. 2.
    Assali, NE, Mache, R, Loiseaux-de Goër, S: Evidence for a composite phylogenetic origin of the plastid genome of the brown alga Pylaiella littoralis (L.) Kjellm. Plant Mol Biol 15: 307–315 (1990).Google Scholar
  3. 3.
    Bhattacharya, D, Elwood, HJ, Goff, L, Sogin, ML: Phylogeny of Gracilaria lemaneiformis (Rhodophyta). J Phycol 26: 181–186 (1990).Google Scholar
  4. 4.
    Boczar, BA, Delaney, TP, Cattolico, RA: Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine alga Olisthodiscus luteus is similar to that of a chemoautoptrophic bacterium. Proc Natl Acad Sci USA 86: 4996–4999 (1989).Google Scholar
  5. 5.
    Chan, RL, Keller, M, Canaday, S, Weil, JH, Imbault, P: 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 (1990).Google Scholar
  6. 6.
    Dalmon, J, Loiseaux, S, Bazetoux, S: Heterogeneity of plastid DNA of two species of brown algae. Plant Sci Lett 29: 243–253 (1983).Google Scholar
  7. 7.
    Devereux, J, Heaberli, P, Smithies, O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).Google Scholar
  8. 8.
    Dickerson, R: The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1: 26–45 (1971).Google Scholar
  9. 9.
    Douglas, SE, Durnford, DG: The small subunit of ribulose-1,5-bisphosphate carboxylase is plastid-encoded in the chlorophyll c-containing alga Cryptomonas F. Plant Mol Biol 13: 13–20 (1989).Google Scholar
  10. 10.
    Douglas, SE, Durnford, DG, Morden, CW: Nucleotide sequence of the gene for the large subunit of ribulose-1,5 bisphosphate carboxylase/oxygenase from Cryptomonas F: evidence supporting the polyphyletic origin of plastids. J Phycol 26: 500–508 (1990).Google Scholar
  11. 11.
    Felsenstein, J: Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 17: 368–376 (1981).Google Scholar
  12. 12.
    Gibbs, SP: The evolution of algal chloroplasts. In: Weissner, W, Robinson, DG, Starr, RC (eds) Experimental Phycology I, pp. 145–157, Springer-Verlag, Berlin (1990).Google Scholar
  13. 13.
    Gibson, JL, Tabita, FR: Different molecular forms of ribulose-1,5-bisphosphate from Rhodopseudomonas sphaeroides. J Biol Chem 252: 943–949 (1977).Google Scholar
  14. 14.
    Glover, HE: Ribulose bisphosphate carboxylase/oxygenase in marine organisms. Int Rev Cytol 115: 67–138 (1988).Google Scholar
  15. 15.
    Goldschmidt-Clermont, M, Rahire, M: Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. J Mol Biol 191: 421–432 (1986).Google Scholar
  16. 16.
    Gray, MW: The bacterial ancestry of plastids and mitochondria. Bioscience 33: 693–699 (1983).Google Scholar
  17. 17.
    Guoy, M, Li, WH: Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339: 145–147 (1989).Google Scholar
  18. 18.
    Gunderson, H, Elwood, H, Ingold, A, Kindle, K, Sogin, ML: Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proc Natl Acad Sci USA 84: 5823–5827 (1987).Google Scholar
  19. 19.
    Hori, H, Osawa, S: Origin and evolution of organisms as deduced from 5S Ribosomal RNA sequences. Mol Biol Evol 4: 445–472 (1987).Google Scholar
  20. 20.
    Jin, L, Nei, M: Limitations of the evolutionary parsimony method of phylogenetic analysis. Mol Biol Evol 7: 82–102 (1990).Google Scholar
  21. 21.
    Keen, JN, Pappin, DJC, Evans, LV: Amino acid sequence analysis of the small subunit of ribulose bisphosphate carboxylase from Fucus (Phaeophyceae). J Phycol 24: 324–327 (1988).Google Scholar
  22. 22.
    Kostrzewa, M, Valentin, K, Maid, U, Radetzky, R, Zetsche, K: Structure of the rubisco-operon from the multicellular red alga Antithamnion spec. Curr Genet 18: 465–469 (1990).Google Scholar
  23. 23.
    Lewin, RA, Gibbs, SP: Algae of uncertain taxonomic position: introduction and bibliography. In: Rosowski, JR, Parker, BC (eds) Selected Papers in Phycology II, pp. 659–662, PSA, USA (1990).Google Scholar
  24. 24.
    Ludwig, W, Weizenegger, M, Betzl, D, Leidel, E, Lenz, T, Ludvigsen, A, Möllenhoff, D, Wenzig, P, Schleifer, KH: Complete nucleotide sequences of seven eubacterial genes coding for the elongation factor Tu: functional structural and phylogenetic evaluations. Arch Microbiol 153: 241–247 (1990).Google Scholar
  25. 25.
    Mazur, BJ, Chui, CF: Sequence of a genomic DNA clone for the small subunit of ribulose bisphosphate carboxylase/oxygenase from tobacco. Nucl Acids Res 13: 2373–2386 (1985).Google Scholar
  26. 26.
    Miziorko, HM, Lorimer, GH: Ribulose-1,5-bisphosphate carboxylase/oxygenase. Ann Rev Biochem 52: 507–535 (1983).Google Scholar
  27. 27.
    Nierzwicki-Bauer, SA, Curtis, SE, Haselkorn, R: Cotranscription of genes encoding the small and large subunits of ribulose-1,5-bisphosphate carboxylase in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 81: 5961–5965 (1984).Google Scholar
  28. 28.
    Palmer JD: Evolution of chloroplast and mitochondrial DNA in plants and algae. In: McIntyre RJ (ed) Monographs in Evolutionary Biology: Molecular Evolutionary Genetics, pp. 131–240. Plenum Press, New York.Google Scholar
  29. 29.
    Palmer JD, Baldauf SL, Calie PJ, de Pamphilis CW: Chloroplast gene instability and transfer to the nucleus. In: Clegg M, O'Brien S (eds) Molecular Evolution, vol 122, pp. 1–10. Alan R. Liss, New York.Google Scholar
  30. 30.
    Reith, M, Cattolico, RA: Inverted repeat of Olisthodiscus luteus chloroplast DNA contains genes for both subunits of ribulose-1,5-bisphosphate carboxylase and the 32000 dalton QB protein: Phylogenetic implications. Proc Natl Acad Sci USA 83: 8599–8603 (1986).Google Scholar
  31. 31.
    Saitou, N, Imanishi, T: Relative efficiencies of the Fitch Margoliash, Maximum-Parsimony, maximum-likelihood, minimum-evolution and neighbor-joining methods of phylogenetic tree construction in obtaining the correct tree. Mol Biol Evol 6: 514–525 (1989).Google Scholar
  32. 32.
    Saitou, N, Nei, M: The neighbor joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425 (1987).Google Scholar
  33. 33.
    Shinozaki, K, Sugiura, M: The gene for the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is located close to the gene for the large subunit in cyanobacterium Anacystis nidulans 6301. Nucl Acids Res 11: 6956–6964 (1983).Google Scholar
  34. 34.
    Sogin, ML, Gunderson, JH: Structural diversity of Eukaryotic small subunit ribosomal RNAs. Evolutionary implications. Ann NY Acad Sci 503: 125–139 (1987).Google Scholar
  35. 35.
    Sogin, ML, Gunderson, JH, Elwood, HJ, Alonso, RA, Peattie, DA: Phylogenetic meaning of the kindom concept, an unusual ribosomal RNA from Giardia lamblia. Science 243: 75–77 (1989).Google Scholar
  36. 36.
    Sourdis, J, Nei, M: Relative efficiencies of the maximum parsimony and distance matrix methods in obtaining the correct phylogenetic tree. Mol Biol Evol 5: 298–311 (1988).Google Scholar
  37. 37.
    Starnes, SM, Lambert, DH, Maxwell, ES, Stevens, SE, Jr, Portis, RD, Shively, JM: Cotranscription of the large and small subunit genes of ribulose-1,5-bisphosphate carboxylase/oxygenase in Cyanophora paradoxa. FEMS Microbial Lett 28: 165–169 (1985).Google Scholar
  38. 38.
    Stein, JL, Haygood, M, Felbeck, H: Nucleotide sequence and expression of a deep-sea ribulose-1,5-bisphosphate carboxylase gene cloned from a chemoautotrophic bacterial endosymbiont. Proc Natl Acad Sci USA 87: 8850–8854 (1990).Google Scholar
  39. 39.
    Stern, DB, Jones, H, Gruissem, W: Function of plastid mRNA 3′ inverted repeats. RNA stabilization and genespecific protein binding. J Biol Chem 264: 18742–18750 (1989).Google Scholar
  40. 40.
    Tabita, FR, McFadden, BA: D-Ribulose-1,5-diphosphate carboxylase from Rhodospirullum rubrum II: Quaternary structure, composition, catalytic and immunological properties. J Mol Chem 249: 3459–3464 (1974).Google Scholar
  41. 41.
    Valentin, K, Zetshe, K: The genes of both subunits of ribulose-1,5-bisphosphate carboxylase constitute an operon on the plastome of a red alga. Curr Genet 16: 203–209 (1989).Google Scholar
  42. 42.
    Valentin, K, Zetsche, K: Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta. Plant Mol Biol 15: 575–584 (1990).Google Scholar
  43. 43.
    Valentin, K, Zetsche, K: Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: Evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222: 425–430 (1990).Google Scholar
  44. 44.
    Valentin, K, Zetsche, K: Nucleotide sequence of the gene for the large subunit of Rubisco from Cyanophora paradoxa. Phylogenetic implications. Curr Genet 18: 199–202 (1990).Google Scholar
  45. 45.
    Viale, AM, Kobayashi, H, Akazawa, T: Expressed genes for plant-type ribulose 1,5 bisphosphate carboxylase/oxygenase in the photosynthetic bacterium Chromatium vinosum, which possesses two complete sets of the genes. J Bact 171: 2391–2400 (1989).Google Scholar
  46. 46.
    Whatley, JM, Whatley, FR: Chloroplast evolution. New Phytol 87: 233–247 (1981).Google Scholar
  47. 47.
    Woese, CR: Bacterial evolution. Microbiol Rev 51: 221–270 (1987).Google Scholar
  48. 48.
    Wolter, FP, Fritz, CC, Willmitzel, L, Schell, J, Schreier, P: rbcS genes in Solanum tuberosum: Conservation of transit peptide and exon shuffing during evolution. Proc Natl Acad Sci USA 85: 846–850 (1988).Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • Nour-Eddine Assali
    • 1
  • William F. Martin
    • 2
  • Charles C. Sommerville
    • 3
  • Susan Loiseaux-de Goër
    • 3
  1. 1.Laboratoire de Biologie Moléculaire Végétale, CNRS, URA 57Université Joseph FourierGrenoble
  2. 2.Institut für GenetikTechnische Universität BraunschweigBraunschweigFRG
  3. 3.Station Biologique de RoscoffCNRS UPR 4601RoscoffFrance
  4. 4.Laboratoire de BiochimieI.A.V. Hassan IIRabatMorocco

Personalised recommendations