Skip to main content
SpringerLink
Log in

Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The complete nucleotide sequence of the Chlamydomonas eugametos (Chlamydomonadales, Chlorophyceae, sensu Mattox and Stewart) mitochondrial genome has been determined (22 897 bp, 34.6% G + C). The genes identified in this circular-mapping genome include those for apocytochrome b, subunit 1 of the cytochrome oxidase complex, subunits 1, 2, 4, 5, and 6 of the NADH dehydrogenase complex, discontinuous large and small subunit ribosomal rRNAs and three tRNAs whose anticodons CAU, CCA and UUG are specific for methionine, tryptophan and glutamine, respectively. The C. eugametos mitochondrial DNA (mtDNA), therefore, shares almost the same reduced set of coding functions and similar unusual features of rRNA gene organization with the linear 15.8 kb mtDNA of Chlamydomonas reinhardtii, the only other completely sequenced chlamydomonadalean mtDNA. However, sequence analysis of the C. eugametos mtDNA has revealed the following distinguishing features relative to those of C. reinhardtii: (1) the absence of a reverse transcriptase-like gene homologue, (2) the presence of an additional gene for tRNAmet that may be a pseudogene, (3) a completely different gene order, (4) transcription of all genes from the same mtDNA strand, (5) a lower G + C content, (6) less pronounced bias in codon usage, and (7) nine group I introns, several of which contain open reading frames coding for potential maturases/endonucleases and two have a nucleotide at the 5′ or 3′ splice site of the deduced precursor RNAs that deviates from highly conserved nucleotides reported in other group I introns. The features of mitochondrial genome organization and gene content shared by C. eugametos and C. reinhardtii contrast with those of other green algal mtDNAs that have been characterized in detail. The deep evolutionary divergence between these two Chlamydomonas taxa within the Chlamydomonadales suggests that their shared features of mitochondrial genome organization evolved prior to the origin of this group.

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. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 215: 403–410 (1990).

    Article  PubMed  Google Scholar 

  2. Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG: Comparison of the human and bovinemitochondrial genomes. In: Slonimski P, Borst P, Attardi G (eds), Mitochondrial Genes, pp. 5-43. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  3. Antaramian A, Coria R, Ramírez J, González-Halphen D: The deduced primary structure of subunit I from cytochrome c oxidase suggests that the genus Polytomella shares a common mitochondrial origin with Chlamydomonas. Biochim Biophys Acta 1273: 198–202 (1996).

    PubMed  Google Scholar 

  4. Beagley CT, Okada NA, Wolstenholme DR: Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc Natl Acad Sci USA 93: 5619–5623 (1996).

    PubMed  Google Scholar 

  5. Bendich AJ: Reaching for the ring: the study of mitochondrial genome structure. Curr Genet 24: 279–290 (1993).

    PubMed  Google Scholar 

  6. Boer PH, Gray MW: The URF5 gene of Chlamydomonas reinhardtii mitochondria: DNA sequence and mode of transcription. EMBO J 5: 21–28 (1986).

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  8. Boer PH, Gray MW: Genes encoding a subunit of respiratory NADH dehydrogenase (ND1) and a reverse transcriptase-like protein (RTL) are linked to ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. EMBO J 7: 3501–3508 (1988).

    PubMed  Google Scholar 

  9. Boer PH, Gray MW: Transfer RNA genes and the genetic code in Chlamydomonas reinhardtii mitochondria. Curr Genet 14: 583–590 (1988).

    PubMed  Google Scholar 

  10. Boer PH, Gray MW: Short dispersed repeats localized in spacer regions of Chlamydomonas reinhardtii mitochondrial DNA. Curr Genet 19: 309–312 (1991).

    PubMed  Google Scholar 

  11. Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW: Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Nat Acad Sci USA 84: 2391–2395 (1987).

    PubMed  Google Scholar 

  12. Buchheim MA, Lemieux C, Otis C, Gutell RR, Chapman RL, Turmel M: Phylogeny of the Chlamydomonadales (Chlorophyceae): a comparison of ribosomal RNA gene sequences from the nucleus and the chloroplast. Mol Phylogenet Evol 5: 391–402 (1996).

    PubMed  Google Scholar 

  13. Colleaux L, Michel-Wolwertz M-R, Matagne RF, Dujon B: The apocytochrome b gene of Chlamydomonas smithii contains a mobile intron related to both Saccharomyces and Neurospora introns. Mol Gen Genet 223: 288–296 (1990).

    Google Scholar 

  14. Côté M-J, Turmel M: In vitro self-splicing reactions of chloroplast and mitochondrial group-I introns in Chlamydomonas eugametos and Chlamydomonas moewusii. Curr Genet 27: 177–183 (1995).

    PubMed  Google Scholar 

  15. Denovan-Wright EM, Lee RW: Comparative analysis of the mitochondrial genomes of Chlamydomonas eugametos and Chlamydomonas moewusiii. Curr Genet 21: 197–202 (1992).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  17. Denovan-Wright EM, Lee RW: Evidence that the fragmented ribosomal RNAs of Chlamydomonas mitochondria are associated with ribosomes. FEBS Lett 370: 222–226 (1995).

    PubMed  Google Scholar 

  18. Ettl H: Die Gattung Chlamydomonas Ehrenberg. Beih Nova Hedwigia 49: 1–1122 (1976).

    Google Scholar 

  19. Friedl T: Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: a phylogenetic analysis of 18S ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiopheae cl. nov.). J Phycol 31: 632–639 (1995).

    Google Scholar 

  20. Golden B, Cech TR: Conformational switches involved in orchestrating the successive steps of group I RNA splicing. Biochemistry 35: 3754–3763 (1996).

    PubMed  Google Scholar 

  21. Gray MW: Mitochondrial evolution. In: Levings ChS III, Vasil IK (eds) The Molecular Biology of Plant Mitochondria, pp. 635–659. Kluwer Academic Publishers, Dordrecht, Netherlands (1995).

    Google Scholar 

  22. Gray MW, Boer PH: Organization and expression of algal (Chlamydomonas reinhardtii) mitochondrial DNA. Phil Trans R Soc Lond B 319: 135–147 (1988).

    Google Scholar 

  23. Gray MW, Spencer D: Organellar evolution. In: Roberts DMcL, Sharp P, Alderson G, Collins M (eds) Evolution of Microbial Life, pp. 109–126. Cambridge University Press, Cambridge, UK (1996).

    Google Scholar 

  24. Hanson MR, Sutton CA, Lu B: Plant organelle gene expression: altered by RNA editing. Trends Plant Sci 1: 57–64 (1996).

    Google Scholar 

  25. Henikoff S: Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359 (1984).

    Article  PubMed  Google Scholar 

  26. Higgins DG, Bleasby AJ, Fuchs R: CLUSTAL V: improved software formultiple sequence alignment. Comput Appl Biosci 8: 189–191 (1992).

    PubMed  Google Scholar 

  27. Howe CJ, Barker RF, Bowman CM, Dyer TA: Common features of three inversions in wheat chloroplast DNA. Curr Genet 13: 343–349 (1988).

    PubMed  Google Scholar 

  28. Hur M, Waring RB: Two group I introns with a C●C basepair at the 5′ splice-site instead of the very highly conserved U●G basepair: is selection post-translational? Nucl Acids Res 23: 4466–4470 (1995).

    PubMed  Google Scholar 

  29. Karger BD: Preparation of single-stranded DNA from phagemids. Focus 12: 28–29 (1990).

    Google Scholar 

  30. Kessler U, Zetsche K: Physical map and gene organization of the mitochondrial genome from the unicellular green alga Platymonas (Tetraselmis) subcordiformis (Prasinophyceae). Plant Mol Biol 29: 1081–1086 (1995).

    PubMed  Google Scholar 

  31. Kroymann J, Zetsche K: The apocytochrome b gene in Chlorogonium elongatum (Chlamydomonadaceae): an intronic GIYYIGORF in green algalmitochondria. Curr Genet 31: 414–418 (1997).

    PubMed  Google Scholar 

  32. Lee RW, Dumas C, Lemieux C, Turmel M: Cloning and characterization of the Chlamydomonas moewusii mitochondrial genome. Mol Gen Genet 231: 53–58 (1991).

    Article  PubMed  Google Scholar 

  33. Lonergan KM, Gray MW: Editing of transfer RNAs in Acanthamoeba castillanii mitochondria. Science 259: 812–816 (1993).

    PubMed  Google Scholar 

  34. Matagne RF, Rongvaux D, Loppes R: Transmission of mitochondrial DNAin crosses involving diploid gametes homozygous or heterozygous for the mating-type locus in Chlamydomonas. Mol Gen Genet 214: 257–262 (1988).

    Google Scholar 

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

    Google Scholar 

  36. McClain WH: Rules that govern tRNA identity in protein synthesis. J Mol Biol 234: 257–280(1993).

    PubMed  Google Scholar 

  37. Michaelis G, Vahrenholz C, Pratje E: Mitochondrial DNA in Chlamydomonas reinhardtii: the gene for apocytochrome b and the complete functional map of the 15.8 kb DNA. Mol Gen Genet 223: 211–216 (1990).

    PubMed  Google Scholar 

  38. Michel F, Hanna M, Green R, Bartel DP, Szostak JW: The guanosine binding site of the Tetrahymena ribozyme. Nature 342: 391–395 (1989).

    PubMed  Google Scholar 

  39. Michel F, Westhof E: Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol 216: 585–610 (1990).

    PubMed  Google Scholar 

  40. Mikkonen M, Vuoristo J, Alatossava T: Ribosome binding site consensus sequence of Lactobacillus delbrueckii subsp. lactis bacteriophage LL-H. FEMS Microbiol Lett 116: 315–320 (1994).

    PubMed  Google Scholar 

  41. Moore LJ, Coleman AW: The linear 20 kb mitochondrial genome of Pandorina morum (Volvocaceae, Chlorophyta). Plant Mol Biol 13: 459–465 (1989).

    Article  PubMed  Google Scholar 

  42. Nedelcu AM: Fragmented and scrambled mitochondrial ribosomal RNA coding regions: a model for their origin and evolution within the green algal group. Mol Biol Evol 14: 506–512 (1997).

    PubMed  Google Scholar 

  43. Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K: Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. J Mol Biol 223: 1–7 (1992).

    Article  PubMed  Google Scholar 

  44. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Nat Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  45. Shimada H, Sugiura M: Pseudogenes and short repeated sequences in the rice chloroplast genome. Curr Genet 16: 293–301 (1989).

    PubMed  Google Scholar 

  46. Sprinzl M, Steegborn C, Hübel F, Steinberg S: Compilation of tRNA sequences and sequences of tRNA genes. Nucl Acids Res 24: 68–72 (1996).

    PubMed  Google Scholar 

  47. Steinkötter J, Bhattacharya D, Semmelroth I, Bibeau C, Melkonian M: Prasinophytes form independent lineages within the chlorophyta: evidence from ribosomal RNAsequence comparisons. J Phycol 30: 340–345 (1994).

    Google Scholar 

  48. Turmel M, Gutell RR, Mercier J-P, Otis C, Lemieux C: Analysis of the chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa: three internal transcribed spacers and 12 group I intron insertion sites. J Mol Biol 232: 446–467 (1993).

    PubMed  Google Scholar 

  49. Turmel M, Mercier J-P, Côté M-J: Group I introns interrupt the chloroplast psaB and psbC and the mitochondrial rrnL gene in Chlamydomonas. Nucl Acids Res 21: 5242–5250 (1993).

    PubMed  Google Scholar 

  50. Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G: Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet 24: 241–247 (1993).

    PubMed  Google Scholar 

  51. Wolff G, Kück U: Organization and coding capacity of mitochondrial genomes of algae. In: Brennicke A, Kück U (eds) Plant Mitochondria, pp. 103–113. VCH, Weinheim (1993).

    Google Scholar 

  52. Wolff G, Burger G, Lang BF, Kück U: Mitochondrial genes in the colourless alga Prototheca wickerhamii resemble plant genes in their exons but fungal genes in their introns. Nucleic Acids Res 21: 719–726 (1993).

    PubMed  Google Scholar 

  53. Wolff G, Plante I, Lang BF, Kück U, Burger G: Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. J Mol Biol 237: 75–86 (1994).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Dalhousie University, Halifax, Nova Scotia, B3H 4J1, Canada

    Eileen M. Denovan-Wright, Aurora M. Nedelcu & Robert W. Lee

Authors
  1. Eileen M. Denovan-Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aurora M. Nedelcu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert W. Lee
    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

Denovan-Wright, E.M., Nedelcu, A.M. & Lee, R.W. Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol 36, 285–295 (1998). https://doi.org/10.1023/A:1005995718091

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005995718091

Search

Navigation