Skip to main content
Log in

Evolution of fragmented mitochondrial ribosomal RNA genes inChlamydomonas

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The fragmented mitochondrial ribosomal RNAs (rRNAs) of the green algaeChlamydomonas eugametos andChlamydomonas reinhardtii are discontinuously encoded in subgenic modules that are scrambled in order and interspersed with protein coding and tRNA genes. The mitochondrial rRNA genes of these two algae differ, however, in both the distribution and organization of rRNA coding information within their respective genomes. The objectives of this study were (1) to examine the phylogenetic relationships between the mitochondrial rRNA gene sequences ofC. eugametos andC. reinhardtii and those of the conventional mitochondrial rRNA genes of the green alga,Prototheca wickerhamii, and land plants and (2) to attempt to deduce the evolutionary pathways that gave rise to the unusual mitochondrial rRNA gene structures in the genusChlamydomonas. Although phylogenetic analysis revealed an affiliation between the mitochondrial rRNA gene sequences of the twoChlamydomonas taxa to the exclusion of all other mitochondrial rRNA gene sequences tested, no specific affiliation was noted between theChlamydomonas sequences andP. wickerhamii or land plants. Calculations of the minimal number of transpositions required to convert hypothetical ancestral rRNA gene organizations to the arrangements observed forC. eugametos andC. reinhardtii mitochondrial rRNA genes, as well as a limited survey of the size of mitochondrial rRNAs in other members of the genus, lead us to propose that the last common ancestor ofChlamydomonas algae contained fragmented mitochondrial rRNA genes that were nearly co-linear with conventional rRNA genes.

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.

Similar content being viewed by others

References

  • Boer PH, Gray MW (1988) Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell 55:399–411

    Article  PubMed  CAS  Google Scholar 

  • Bourque DP, Boynton JE, Gillham NW (1971) Studies on the structure and cellular location of various ribosomes and ribosomal RNA species in the green algaChlamydomonas reinhardtii. J Cell Science 8:153–158

    PubMed  CAS  Google Scholar 

  • Buchheim MA, Turmel M, Zimmer EA, Chapman RL (1990) Phylogeny ofChlamydomonas (Chlorophyta) based on cladistic analysis of nuclear 18S sequence data. J Phycol 26:689–699

    Article  Google Scholar 

  • Cedergren R, Gray MW, Abel Y, Sankoff D (1988) The evolutionary relationships among known life forms. J Mol Evol 28:98–112

    Article  PubMed  CAS  Google Scholar 

  • Chapman DJ, Ragan MA (1980) Evolution of biochemical pathways: evidence from comparative biochemistry. Ann Rev Plant Physiol 31:639–678

    Article  CAS  Google Scholar 

  • Denovan-Wright EM, Lee RW (1992) Comparative analysis of the mitochondrial genomes ofChlamydomonas eugametos andChlamydomonas moewusii. Curr Genet 21:197–202

    Article  PubMed  CAS  Google Scholar 

  • Denovan-Wright EM, Lee RW (1994) Comparative structure and genomic organization of the discontinuous mitochondrial ribosomal RNA genes ofChlamydomonas eugametos andChlamydomonas reinhardtii. J Mol Biol 241:298–311

    Article  PubMed  CAS  Google Scholar 

  • Dron M, Rahire M, Darlix J-D (1982) Sequence of the chloroplast 16S rRNA gene and its surrounding regions inChlamydomonas reinhardtii. Nucleic Acids Res 10:7609–7620

    PubMed  CAS  Google Scholar 

  • Durocher V, Gauthier A, Bellemare G, Lemieux C (1989) An optional group I intron between the chloroplast small subunit rRNA genes ofChlamydomonas moewusii andC. eugametos. Curr Genet 15:277–282

    Article  PubMed  CAS  Google Scholar 

  • Ettl H (1976) Die GattungChlamydomonas Ehrenberg. Beih. Nova Hedwigia 49:1–1122

    Google Scholar 

  • Feagin J, Werner E, Gardner MJ, Williamson DH, Wilson RJM (1992) Homologies between the contiguous and fragmented rRNAs of the twoPlasmodium falciparum extrachromosomal DNAs are limited to core sequences. Nucleic Acids Res 20:879–887

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.53c (computer software package and manual distributed by the author, Dept Genetics, University of Washington, Seattle, WA)

  • Gray MW (1989) Origin and evolution of mitochondrial DNA. Ann Rev Cell Biol 5:25–50

    PubMed  CAS  Google Scholar 

  • Gray MW (1992) The endosymbiont hypothesis revisited. Int Rev Cytol 141:233–357

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1–42

    PubMed  CAS  Google Scholar 

  • Gray MW, Schnare MN (1995) Evolution of rRNA gene organization. In: Zimmermann RA, Dalhberg AE (eds) Ribosomal RNA: structure, evolution, processing and function in protein biosynthesis. CRC Press, Boca Raton, pp 49–69

    Google Scholar 

  • Gray MW, Cedergren RJ, Abel Y, Sankoff D (1989) On the evolutionary origin of the plant mitochondrion and its genome. Proc Natl Acad Sci USA 86:2267–2271

    Article  PubMed  CAS  Google Scholar 

  • Gunderson JH, Elwood H, Ingold H, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proc Natl Acad Sci 84:5823–5827

    Article  PubMed  CAS  Google Scholar 

  • Heinonen TYK, Schnare MN, Young PS, Gray MW (1987) Rearranged coding segments, separated by a transfer RNA gene, specify the two parts of a discontinuous large subunit ribosomal RNA inTetrahymena pyriformis mitochondria. J Biol Chem 262:2879–2887

    PubMed  CAS  Google Scholar 

  • Hendriks L, De Baere R, Van de Peer Y, Neefs J, Goris A, De Wachter R (1991) The evolutionary position of the rhodophytePorphyra umbicalis and the basidiomyceteLeucosporidium scottii among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J Mol Evol 32:167–177

    PubMed  CAS  Google Scholar 

  • Hoober JK, Blobel G (1969) Characterization of the chloroplastic and cytoplasmic ribosomes ofChlamydomonas reinhardtii. J Mol Biol 41:121–138

    Article  PubMed  CAS  Google Scholar 

  • Jupe ER, Chapman RL, Zimmer EA (1988) Nuclear ribosomal RNA genes and algal phylogeny—theChlamydomonas example. Bio-Systems 21:223–230

    PubMed  CAS  Google Scholar 

  • Kairo A, Fairlamb AH, Gobright E, Nene V (1994) A 7.1 kb linear DNA molecule ofTheileria parva has scrambled rRNA sequences and open reading frames for mitochondrial encoded proteins. EMBO J 13:898–905

    PubMed  CAS  Google Scholar 

  • Kück U, Godehardt I, Schmidt U (1990) A self splicing group II intron in the mitochondrial large subunit rRNA (LSU rRNA) gene of the eukaryotic algaScenedesmus obliquus. Nucleic Acids Res 18:2691–2697

    PubMed  Google Scholar 

  • Lemieux C, Turmel M, Lee RW (1980) Characterization of chloroplast DNA inChlamydomonas eugametos andC. moewusii and its inheritance in hybrid progeny. Curr Genet 2:139–147

    Article  CAS  Google Scholar 

  • Lemieux C, Boulanger J, Otis C, Turmel M (1989) Nucleotide sequence of the chloroplast large subunit rRNA gene fromChlamydomonas reinhardtii. Nucleic Acids Res 17:7997

    PubMed  CAS  Google Scholar 

  • Lonergan KM, Gray MW (1994) The ribosomal RNA gene region inAcanthamoeba castellanii mitochondrial RNA. A case of evolutionary transfer of introns between mitochondria and plastids? J Mol Biol 239:476–499

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Mattox KR, Stewart KD (1984) Classification of the green algae: a concept based on comparative cytology. In: Irvine DEG, John DM (eds) Systematics of the green algae. Academic Press, London, pp 29–72

    Google Scholar 

  • Noller HF (1984) Structure of ribosomal RNA. Ann Rev Biochem 53:119–162

    Article  PubMed  CAS  Google Scholar 

  • Rochaix JD, Darlix JL (1982) Composite structure of the chloroplast 23S ribosomal RNA genes ofChlamydomonas reinhardtii. Evolutionary and functional implications. J Mol Biol 159:383–395

    Article  PubMed  CAS  Google Scholar 

  • Sankoff D, Leduc G, Antoine N, Paquin B, Lang BF, Cedergren R (1992) Gene order comparisons for phylogenetic inference: evolution of the mitochondrial genome. Proc Natl Acad Sci USA 89:6575–6579

    Article  PubMed  CAS  Google Scholar 

  • Schnare MN, Heinonen TYK, Young PG, Gray MW (1986) A discontinuous small subunit ribosomal RNA inTetrahymena pyriformis mitochondria. J Biol Chem 261:5187–5193

    PubMed  CAS  Google Scholar 

  • Sogin ML, Ingold A, Karlik M, Nielsen H, Engberg J (1986) Phylogenetic evidence for the acquisition of ribosomal RNA introns subsequent to the divergence of some of the major Tetrahymena groups. EMBO J 5:3625–3630

    PubMed  CAS  Google Scholar 

  • Turmel M, Lemieux B, Lemieux C (1988) The chloroplast genome of the green algaChlamydomonas moewusii: localization of protein-coding genes and transcriptionally active regions. Mol Gen Genet 214:412–419

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Gutell RR, Mercier JP, Otis C, Lemieux C (1993) Analysis of the chloroplast large subunit ribosomal RNA gene from 17Chlamydomonas taxa. J Mol Biol 232:446–467

    Article  PubMed  CAS  Google Scholar 

  • Turmel C, Côté V, Otis C, Mercier JP, Gray MW, Lonergan KM, Lemieux C (1995) Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion). Mol Biol Evol 12:533–545

    PubMed  CAS  Google Scholar 

  • Vaidya AB, Akella R, Suplick K (1989) Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6 kilobase-pair DNA of a malarial parasite. Mol Biochem Parasitol 35:97–108

    Article  PubMed  CAS  Google Scholar 

  • Wolff G, Kück U (1990) The structural analysis of the mitochondrial SSU rRNA implies a close phylogenetic relationship between mitochondria from plants and from the heterotrophic algaPrototheca wickerhamii. Curr Genet 17:347–351

    Article  PubMed  CAS  Google Scholar 

  • Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert W. Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Denovan-Wright, E.M., Sankoff, D., Spencer, D.F. et al. Evolution of fragmented mitochondrial ribosomal RNA genes inChlamydomonas . J Mol Evol 42, 382–391 (1996). https://doi.org/10.1007/BF02498632

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02498632

Key words

Navigation