Skip to main content
Log in

Structure of the Rubisco operon from the unicellular red algaCyanidium caldarium: Evidence for a polyphyletic origin of the plastids

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

The genes for both subunits of ribulose-1,5-bisphosphate-carboxylase/oxygenase (Rubisco) were located on the plastid DNA (ptDNA) of the unicellular red algaCyanidium caldarium. Both genes are organized together in an operon. The sequence homology of both genes to the corresponding genes from the unicellular red algaPorphyridium aerugineum is remarkably high, whereas homology to Rubisco genes from chloroplasts and two recent cyanobacteria is significantly lower. These data provide strong evidence for a polyphyletic origin of chloroplasts and rhodoplasts. In addition the genes for the small subunit of Rubisco (rbcS) from red algae show about 60% homology torbcS genes from cryptophytes and chromophytes. Thus, homologies in therbcS gene indicate a close phylogenetic relationship between rhodoplasts and the plastids of Chromophyta.

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

Access this article

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

  • Allen MB (1959) Studies withCyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32:270–277

    Google Scholar 

  • Bedbrook JR, Smith SM, Ellis RJ (1980) Molecular cloning and sequencing of cDNA encoding the precusor to the small subunit of chloroplast ribulose-1,5-bisphosphate carboxylase. Nature 287:692–697

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Cavalier-Smith TT (1987) The origin of eucaryote and archaebacterial cells. Ann New York Acad Sci 503:17–54

    Google Scholar 

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

    Google Scholar 

  • Dale JW, Greenaway PJ (1984) Identification of recombinant plasmids by in situ colony hybridization. In: Walker JM (eds) Methods in Molecular Biology vol 2, Humana Press, Clifton, New Jersey

    Google Scholar 

  • Davies LG, Dibner MD, Battey JF (1986) Basic methods in molecular biology, Elsevier Scientific Publishing, New York

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Gibbs SP (1981) The plastids of some algal groups may have evolved from endosymbiotic eucaryotic algae. Ann New York Acad Sci 36:193–207

    Google Scholar 

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

    Google Scholar 

  • Goldschmidt-Clermont M, Rahire M (1986) Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase inChlamydomonas reinhardii. J Mol Biol 191:421–432

    Google Scholar 

  • Hansmann P, Falk H, Sitte P (1985) DNA in the nucleomorph ofCryptomonas demonstrated by DAPI fluorescence. Z Naturforsch 40:933–935

    Google Scholar 

  • Hwang S-H, Tabita FR (1989) Cloning and expression of the chloroplast-encodedrbcL andrbcS genes from the marine diatomCylindrotheca sp. strain N1. Plant Mol Biol 13:69–79

    Google Scholar 

  • Keen JF, Pappin DJC, Evans LV (1988) Amino acid sequence analysis of the small subunit of ribulose-bisphosphate carboxylase fromFucus (Phaeophyceae). J Phycol 24:324–327

    Google Scholar 

  • Kowallik KV (1989) Molecular aspects and phylogenetic implications of plastid genomes of certain chromophytes. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte algae: Problems and perspectives. Clarendon Press, Oxford, pp 99–122

    Google Scholar 

  • Kremer BP, Feige GB, Schneider HAW (1978) A new proposal for the systematic position ofCyanidium caldarium. Naturwissenschaften 65:157

    Google Scholar 

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

    Google Scholar 

  • Kuhsel M, Kowallik KV (1987) The plastome of a brown alga,Dictyota dichotoma. II. Location of structural genes coding for ribosomal RNAs, the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase and for polypeptides of photosystem I and II. Mol Gen Genet 207:361–368

    Google Scholar 

  • Kuhsel M, Kowallik KV (1989) The plastome of a brown alga,Dictyota dichotoma. III. Genes coding for polypeptides of the photosynthetic electron chain. Mol Gen Genet (in press)

  • Linne V Berg KH, Kowallik KV (1988) Structural organization and evolution of the plastid genome ofVaucheria sessilis (Xanthophyceae). BioSystems 21:239–247

    Google Scholar 

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

    Google Scholar 

  • Maid U, Valentin K, Zetsche K (1990) ThepsbA gene from a red alga resembles those from Cyanobacteria and Cyanelles. Curr Genet 17:255–259

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Margulis L (1981) Symbiosis in cell evolution. WH Freeman, San Francisco

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Miziorko HM, Lorimer GH (1983) Ribulose-1,5-bisphosphate carboxylase/oxygenase. Annu Rev Biochem 52:507–535

    Google Scholar 

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

    Google Scholar 

  • Nagashima H, Fukuda I (1981) Low molecular weight carbohydrates inCyanidium and some related algae. Phytochemistry 20:439–442

    Google Scholar 

  • Nierzwicki-Bauer SA, Curtis SE, Haselkorn R (1984) Cotranscription of genes encoding the small and large subunits of ribulose-1,5-bisphosphate carboxylase in the cyanobacteriumAnabaena7120. Proc Natl Acad Sci USA 81:5961–5965

    Google Scholar 

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

    Google Scholar 

  • Reith M, Cattolico RA (1986) Inverted repeat ofOlisthodiscus 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

    Google Scholar 

  • Sailland A, Amiri I, Freyssinet G (1986) Amino acid sequence of the ribulose-1,5-bisphosphate carboxylase/oxygenase subunit fromEuglena. Plant Mol Biol 7:213–218

    Google Scholar 

  • Seckbach J, Hammermann LS, Hanania J (1981) Ultrastructural studies ofCyanidium caldarium: contribution to phylogenetics. Ann New York Acad Sci 361:409–425

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Starnes SM, Lambert DH, Maxwell ES, Stevens Jr SE, Porter RD, Shively JM (1985) Cotranscription of the large and small sub-unit genes of ribulose-1,5-bisphosphate carboxylase/oxygenase inCyanophora paradoxa. FEMS Lett 28:165–169

    Google Scholar 

  • Steinmüller K, Kaling M, Zetsche K (1983) In vitro synthesis of phycobiliproteins and ribulose-1,5-bisphosphate carboxylase by non-polyadenylated-RNA ofCyanidium caldarium andPorphyridium aerugineum. Planta 159:308–313

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Valentin K, Zetsche K (1989) 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

    Google Scholar 

  • Zurawski G, Perrot B, Bottomley W, Whitfeld PR (1981) 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by R.G. Herrmann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valentin, K., Zetsche, K. Structure of the Rubisco operon from the unicellular red algaCyanidium caldarium: Evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222, 425–430 (1990). https://doi.org/10.1007/BF00633849

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00633849

Key words

Navigation