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 Ξ¦. 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.
Similar content being viewed by others
References
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: 4547β4558 (1987).
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: 4996β4999 (1989).
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: 55β61 (1983).
Cavalier-Smith T: The origin of eucaryote and archaebacterial cells. Ann N Y Acad Sci 503: 17β54 (1987).
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: 257β263 (1985).
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: 1835β1839 (1983).
Douglas SE, Durnford DG: The small subunit of ribulose-1,5-bisphosphate carboxylase in plastid encoded in the chlorophyll c-containing alga Cryptomonas Ξ¦. Plant Mol Biol 13: 13β20 (1989).
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: 775β793 (1982).
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: 361β366 (1985).
Gibbs SP: The plastids of some algal groups may have evolved from endosymbiotic eucaryotic algae. Ann N Y Acad Sci: 193β207 (1981).
Gingrich JC, Hallick RB: The Euglena gracilis ribulose-1,5-bisphosphate carboxylase gene. II The spliced mRNA and its product. J Biol Chem 260: 16162β16168 (1985).
Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR: Evolutionary relationships among cyanobacteria and green chloroplasts. J Bact 170: 3548β3592 (1988).
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: 421β432 (1986).
Hansmann P, Falk H, Sitte P: DNA in the nucleomorph of Cryptomonas demonstrated by DAPI fluorescence. Zeitschr Naturforsch 40 c: 933β935 (1985).
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: 313β319 (1989).
Higgins DG, Sharp PM: CLUSTAL: a package for performing multiple sequence alignments on a microcomputer. Gene 73: 237β244 (1988).
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: 69β79 (1989).
Keen JF, Pappin DJC, Evans LV: Amino acid sequence analysis of the small subunit of ribulosebisphosphate carboxylase from Fucus (Phaeophyceae). J Phycol 24: 324β327 (1988).
KrΓΆger M, KrΓΆger-Block A: Extension of a flexible computer program for handling DNA sequence data. Nucleic Acids Res 12: 113β123 (1984).
Ludwig M, Gibbs SP: DNA is present in the nucleomorph of cryptomonads: further evidence that the chloroplast evolved from a eucaryotic endosymbiont. Protoplasma 127: 9β20 (1985).
Maid U, Valentin K, Zetsche K: The psbA-gene from a red alga resembles those from cyanobacteria and cyanelles. Curr Genet 17: 255β259 (1990).
Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).
Margulis L: Symbiosis in cell evolution. W.H. Freeman & Co., San Francisco (1981).
Markowicz Y, Mache R, Loiseaux-De GoΓ«r S: Sequence of the plastid rDNA spacer region of the brown alga Phylaiella littoralis (L.) Kjellm. Evolutionary significance. Plant Mol Biol 10: 465β469 (1988).
Mazur BJ, Chui CF: Sequence of a genomic clone for the small subunit of ribulose bisphosphate carboxylase/oxygenase from tobacco. Nucleic Acids Res 13: 2373β2386 (1985).
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: 347β358 (1986).
McIntosh L, Poulsen C, Bogorad L: Chloroplast gene sequence for the large subunit of ribulose bisphosphate carboxylase of maize. Nature 288: 556β560 (1980).
Morden CW, Golden SS: psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382β385 (1989).
Newman S, Cattolico RA: Synthesis of active Olisthodiscus luteus ribulose-1,5-bisphosphate carboxylase in Escherichia coli. Plant Mol Biol 11: 821β831 (1988).
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: 939β946 (1989).
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: 5961β5965 (1984).
Palmer JD: Comparative organization of chloroplast genomes. Ann Rev Genet 19: 325β354 (1985).
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: 8599β8603 (1986).
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: 4050β4054 (1983).
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: 6957β6964 (1983).
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: 165β169 (1985).
Tabita FR, McFadden BA: Ribulose 1,5-diphosphate carboxylase from Rhodospirillum rubrum II: Quaternary structure, composition, catalytic and immunological properties. J Biol Chem 249: 3459β3464 (1974).
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: 6100β6103 (1985).
Torrez-Ruiz J, McFadden BA: Isolation of L8 and L8S8 of ribulose-1,5-bisphosphate carboxylase/oxygenase from Chromatium vinosum. Arch Microbiol 142: 55β60 (1985).
Turner S, Burger-Wiersma T, Giovannoni SJ, Mur LR: The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337: 380β382 (1989).
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: 203β209 (1989).
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).
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: 3251β3269 (1981).
Author information
Authors and Affiliations
Rights 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, 575β584 (1990). https://doi.org/10.1007/BF00017832
Received:
Accepted:
Issue date:
DOI: https://doi.org/10.1007/BF00017832


