Skip to main content
SpringerLink
Log in

Rubisco genes indicate a close phylogenetic relation between the plastids of Chromophyta and Rhodophyta

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The genes for both subunits of Rubisco (rbcL, rbcS) are located on the plastome of the brown alga Ectocarpus siliculosus (Chromophyta, Phaeophyceae). The organization of these genes in the form of an operon was similar to that found in rhodoplasts, cyanobacteria and the plastids of Cryptomonas Φ. Sequence analysis of the complete operon revealed a high degree of homology and great structural similarities to corresponding genes from two red algae. In contrast, sequence homology to Rubisco genes from chloroplasts and cyanobacteria was much lower. This clearly indicated a close phylogenetic relationship between the plastids of Rhodophyta and Chromophyta which seem to have evolved independently from the chloroplasts (polyphyletic origin). Our data suggest that the plastids of Chromophyta and Cryptophyta have originated from endosymbiotic unicellular red algae. Surprisingly, red and brown algal Rubiscos show a significantly higher degree of homology to that from a hydrogen bacterium than to those from cyanobacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Andersen K, Caton J: Sequence analysis of the Alcaligenes eutrophus chromosomally encoded Ribulose bisphosphate carboxylase large and small subunit genes and their products. J Bact 169: 4547–4558 (1987).

    PubMed  Google Scholar 

  2. Boczar BA, Delaney TP, Cattolico RA: Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci USA 86: 4996–4999 (1989).

    PubMed  Google Scholar 

  3. Broglie R, Coruzzi G, Lamppa G, Keith B, Chua N-H: Structural analysis of nuclear genes coding for the precursor to the small subunit of wheat ribulose-1,5-bisphosphate carboxylase. Bio/technology 1: 55–61 (1983).

    Article  Google Scholar 

  4. Cavalier-Smith T: The origin of eucaryote and archaebacterial cells. Ann N Y Acad Sci 503: 17–54 (1987).

    PubMed  Google Scholar 

  5. Christeller JT, Terzhaghi BE, Hill DF, Laing WA: Activity expressed from cloned Anacystis nidulans large and small subunit ribulose-1,5-bisphosphate carboxylase genes. Plant Mol Biol 5: 257–263 (1985).

    Google Scholar 

  6. Curtis SE, Haselkorn R: Isolation and sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacterium Anabaena 7120. Proc Natl Acad Sci USA 80: 1835–1839 (1983).

    Google Scholar 

  7. Douglas SE, Durnford DG: The small subunit of ribulose-1,5-bisphosphate carboxylase in plastid encoded in the chlorophyll c-containing alga Cryptomonas Φ. Plant Mol Biol 13: 13–20 (1989).

    PubMed  Google Scholar 

  8. Dron M, Rahire M, Rochaix J-D: Sequence of the chloroplast DNA region of Chlamydomonas reinhardii containing the gene of the large subunit of ribulose bisphosphate carboxylase and parts of its flanking genes. J Mol Biol 162: 775–793 (1982).

    PubMed  Google Scholar 

  9. Gatenby AA, van der Vies SM, Bradley D: Assembly in E. coli of a functional multi-subunit ribulose-1,5-bisphosphate carboxylase from a blue green alga. Nature 314: 361–366 (1985).

    PubMed  Google Scholar 

  10. Gibbs SP: The plastids of some algal groups may have evolved from endosymbiotic eucaryotic algae. Ann N Y Acad Sci: 193–207 (1981).

  11. Gingrich JC, Hallick RB: The Euglena gracilis ribulose-1,5-bisphosphate carboxylase gene. II The spliced mRNA and its product. J Biol Chem 260: 16162–16168 (1985).

    PubMed  Google Scholar 

  12. Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR: Evolutionary relationships among cyanobacteria and green chloroplasts. J Bact 170: 3548–3592 (1988).

    Google Scholar 

  13. 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 reinhardii. J Mol Biol 191: 421–432 (1986).

    PubMed  Google Scholar 

  14. Hansmann P, Falk H, Sitte P: DNA in the nucleomorph of Cryptomonas demonstrated by DAPI fluorescence. Zeitschr Naturforsch 40 c: 933–935 (1985).

    Google Scholar 

  15. Heda DG, Madigan MT: Purification and characterization of the thermostable ribulose-1,5-bisphosphate carboxylase/oxygenase from the thermophilic purple bacterium Chromatium tepidum. Eur J Biochem 184: 313–319 (1989).

    PubMed  Google Scholar 

  16. Higgins DG, Sharp PM: CLUSTAL: a package for performing multiple sequence alignments on a microcomputer. Gene 73: 237–244 (1988).

    Article  PubMed  Google Scholar 

  17. Hwang S-R, Tabita FR: Cloning and expression of the chloroplast-encoded rbcL and rbcS genes from the marine diatom Cylindrotheca sp. strain N1. Plant Mol Biol 13: 69–79 (1989).

    PubMed  Google Scholar 

  18. Keen JF, Pappin DJC, Evans LV: Amino acid sequence analysis of the small subunit of ribulosebisphosphate carboxylase from Fucus (Phaeophyceae). J Phycol 24: 324–327 (1988).

    Google Scholar 

  19. Kröger M, Kröger-Block A: Extension of a flexible computer program for handling DNA sequence data. Nucleic Acids Res 12: 113–123 (1984).

    PubMed  Google Scholar 

  20. Ludwig M, Gibbs SP: DNA is present in the nucleomorph of cryptomonads: further evidence that the chloroplast evolved from a eucaryotic endosymbiont. Protoplasma 127: 9–20 (1985).

    Google Scholar 

  21. Maid U, Valentin K, Zetsche K: The psbA-gene from a red alga resembles those from cyanobacteria and cyanelles. Curr Genet 17: 255–259 (1990).

    PubMed  Google Scholar 

  22. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  23. Margulis L: Symbiosis in cell evolution. W.H. Freeman & Co., San Francisco (1981).

    Google Scholar 

  24. Markowicz Y, Mache R, Loiseaux-De Goër S: Sequence of the plastid rDNA spacer region of the brown alga Phylaiella littoralis (L.) Kjellm. Evolutionary significance. Plant Mol Biol 10: 465–469 (1988).

    Google Scholar 

  25. Mazur BJ, Chui CF: Sequence of a genomic clone for the small subunit of ribulose bisphosphate carboxylase/oxygenase from tobacco. Nucleic Acids Res 13: 2373–2386 (1985).

    PubMed  Google Scholar 

  26. McFadden BA, Torrez-Ruiz J, Daniell H, Sarojini G: Interaction, functional relations and evolution of large and small subunits in Rubisco from Procaryota and Eucaryota. Phil Trans R Soc Lond B 313: 347–358 (1986).

    Google Scholar 

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

    Google Scholar 

  28. Morden CW, Golden SS: psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385 (1989).

    Article  PubMed  Google Scholar 

  29. Newman S, Cattolico RA: Synthesis of active Olisthodiscus luteus ribulose-1,5-bisphosphate carboxylase in Escherichia coli. Plant Mol Biol 11: 821–831 (1988).

    Google Scholar 

  30. Newman SM, Derocher J, Cattolico RA: Analysis of chromophytic and rhodophytic ribulose-1,5-bisphosphate carboxylase indicates extensive structural and functional similarities among evolutionarily diverse algae. Plant Physiol 91: 939–946 (1989).

    Google Scholar 

  31. 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).

    PubMed  Google Scholar 

  32. Palmer JD: Comparative organization of chloroplast genomes. Ann Rev Genet 19: 325–354 (1985).

    Article  PubMed  Google Scholar 

  33. Reith M, Cattolico RA: Inverted repeat of Olisthodiscus luteus chloroplast DNA contains genes for both subunits of ribulose-1,5-bisphosphate carboxylase and the 32 000 dalton QB protein: phylogenetic implications. Proc Natl Acad Sci USA 83: 8599–8603 (1986).

    Google Scholar 

  34. Shinozaki K, Yamada C, Takahata N, Sugiura M: Molecular cloning and sequence analysis of the cyanobacterial gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 80: 4050–4054 (1983).

    Google Scholar 

  35. Shinozaki K, Sugiura M: The gene for the small subunit of ribulose-1,5-bisphosphate carboxylase is located close to the gene for the large subunit in the cyanobacterium Anacystis nidulans 6301. Nucleic Acids Res 11: 6957–6964 (1983).

    PubMed  Google Scholar 

  36. Starnes SM, Lambert DH, Maxwell ES, StevensJr SE, Porter RD, Shively JM: Cotranscription of the large and small subunit genes of ribulose-1,5-bisphosphate carboxylase/oxygenase in Cyanophora paradoxa. FEMS Microbiol Lett 28: 165–169 (1985).

    Article  Google Scholar 

  37. Tabita FR, McFadden BA: Ribulose 1,5-diphosphate carboxylase from Rhodospirillum rubrum II: Quaternary structure, composition, catalytic and immunological properties. J Biol Chem 249: 3459–3464 (1974).

    PubMed  Google Scholar 

  38. Tabita FR, Small CL: Expression and assembly of active cyanobacterial ribulose-1,5-bisphosphate carboxylase/-oxygenase in E. coli containing stoichometric amounts of large and small subunits. Proc Natl Acad Sci USA 82: 6100–6103 (1985).

    PubMed  Google Scholar 

  39. Torrez-Ruiz J, McFadden BA: Isolation of L8 and L8S8 of ribulose-1,5-bisphosphate carboxylase/oxygenase from Chromatium vinosum. Arch Microbiol 142: 55–60 (1985).

    Article  PubMed  Google Scholar 

  40. Turner S, Burger-Wiersma T, Giovannoni SJ, Mur LR: The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337: 380–382 (1989).

    Article  PubMed  Google Scholar 

  41. Valentin K, Zetsche 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).

    PubMed  Google Scholar 

  42. Valentin K, Zetsche K: Structure of the Rubisco-operon from the unicellular red alga Cyanidium caldarium-evidence of a polyphyletic origin of the plastids. Mol Gen Genet, in press (1990).

  43. Zurawski G, Perrot B, Bottomley W, Whitfeld PR: The structure of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from spinach chloroplast DNA. Nucleic Acids Res 9: 3251–3269 (1981).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Pflanzenphysiologie, Justus Liebig Universität, D-63, Giessen, FRG

    Klaus Valentin & Klaus Zetsche

Authors
  1. Klaus Valentin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klaus Zetsche
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

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). https://doi.org/10.1007/BF00017832

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00017832

Key words

Search

Navigation