Skip to main content
SpringerLink
Log in

Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes

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

Summary

The gene organization of starfish mitochondrial DNA is identical with that of the sea urchin counterpart except for a reported inversion of an approximately 4.6-kb segment containing two structural genes for NADH dehydrogenase subunits 1 and 2 (ND 1 and ND 2). When the codon usage of each structural gene in starfish, sea urchin, and vertebrate mitochondrial DNAs is examined, it is striking that codons ending in T and G are preferentially used more for heavy strand-encoded genes, including starfish ND 1 and ND 2, than for light strand-encoded genes, including sea urchin ND 1 and ND 2. On the contrary, codons ending in A and Care preferentially used for the light strand-encoded genes rather than for the heavy strand-encoded ones. Moreover, G-U base pairs are more frequently found in the possible secondary structures of heavy strandencoded tRNAs than in those of light strand-encoded tRNAs. These observations suggest the existence of a certain constraint operating on mitochondrial genomes from various animal phyla, which results in the accumulation of G and T on one strand, and A and C on the other.

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

  • Aloni Y, Attardi G (1971) Expression of the mitochondrial genome in Hela cells. II. Evidence for complete transcription of mitochondrial DNA. J Mol Biol 55:251–270

    PubMed  Google Scholar 

  • 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 (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    PubMed  Google Scholar 

  • Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717

    PubMed  Google Scholar 

  • Bibb MJ, van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180

    PubMed  Google Scholar 

  • Bogenhagen D, Clayton DA (1978) Mechanism of mitochondrial DNA replication in mouse L-cells: kinetics of synthesis and turnover of the initiation sequence. J Mol Biol 119:49–68

    PubMed  Google Scholar 

  • Bolden A, Noy GP, Weissbach A (1977) DNA polymerase of mitochondria is a γ-polymerase. J Biol Chem 252:3351–3356

    PubMed  Google Scholar 

  • Brown WM (1981) Mechanisms of evolution in animal mitochondrial DNA. Ann NY Acad Sci 361:119–134

    PubMed  Google Scholar 

  • Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequence of primates: tempo and mode of evolution. J Mol Evol 18:225–239

    PubMed  Google Scholar 

  • Cantatore P, Roberti M, Rainaldi G, Gadaleta MN, Saccone C (1989) The complete nucleotide sequence, gene organization, and genetic code of mitochondrial genome ofParacentrotus lividus. J Biol Chem 264:10965–10975

    PubMed  Google Scholar 

  • Chang DD, Clayton DA (1985) Priming of human mitochondrial DNA replication occurs at the light-strand promoter. Proc Natl Acad Sci USA 82:351–355

    PubMed  Google Scholar 

  • Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule ofDrosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271

    PubMed  Google Scholar 

  • Clayton DA, Doda JN, Friedberg EC (1974) The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proc Natl Acad Sci USA 71:2777–2781

    PubMed  Google Scholar 

  • Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol 212:599–634

    PubMed  Google Scholar 

  • Doda JN, Wright CT, Clayton DA (1981) Elongation of displacement-loop strands in human and mouse mitochondrial DNA is arrested near specific template sequences. Proc Natl Acad Sci USA 78:6116–6120

    PubMed  Google Scholar 

  • Gadaleta G, Pepe G, De Candia G, Quagliariello C, Sbisá E, Saccone C (1989) The complete nucleotide sequence of theRattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516

    PubMed  Google Scholar 

  • Goddard JM, Wolstenholme DR (1980) Origin and direction of replication in mitochondrial DNA molecules from the genusDrosophila. Nucleic Acids Res 8:741–757

    PubMed  Google Scholar 

  • Hasegawa M, Kishino H (1989) Heterogeneity of tempo and mode of mitochondrial DNA evolution among mammalian orders. Jpn J Genet 64:243–258

    PubMed  Google Scholar 

  • Heckman JE, Sarnoff J, Alzner-De Weed B, Yin S, RajBhandary UL (1980) Novel features in the genetic code and codon reading patterns inNeurospora crassa mitochondria based on sequences of six mitochondrial tRNAs. Proc Natl Acad Sci USA 77:3159–3163

    PubMed  Google Scholar 

  • Himeno H, Masaki H, Kawai T, Ohta T, Kumagai I, Miura K, Watanabe K (1987) Unusual genetic codes and a novel gene structure for tRNA SerAGY in starfish mitochondrial DNA. Gene 56:219–230

    PubMed  Google Scholar 

  • Ikemura T (1981) Correlation between the abundance ofEscherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for theE. coli translational system. J Mol Biol 151:389–409

    PubMed  Google Scholar 

  • Ikemura T (1982) Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. J Mol Biol 158:573–597

    PubMed  Google Scholar 

  • Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217

    PubMed  Google Scholar 

  • Jacobs HT, Asakawa S, Araki T, Miura K, Smith MJ, Watanabe K (1989a) Conserved tRNA cluster in starfish mitochondrial DNA. Curr Genet 15:193–206

    PubMed  Google Scholar 

  • Jacobs HT, Herbert ER, Rankine J (1989b) Sea urchin egg mitochondrial DNA contains a short displacement loop (D-loop) in the replication orgigin region. Nucleic Acids Res 17: 8949–8965

    PubMed  Google Scholar 

  • Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J Mol Evol 24:39–44

    PubMed  Google Scholar 

  • Jukes TH, Osawa S, Muto A, Lehman N (1987) Evolution of anticodons: variations in the genetic code. Cold Spring Harbor Symp Quant Biol 52:769–776

    PubMed  Google Scholar 

  • Kumazawa Y, Yokogawa T, Hasegawa E, Miura K, Watanabe K (1989) The aminoacylation of structually variant phenylalanine tRNAs from mitochondria and various nonmitochondria sources by bovine mitochondrial phenylalanyl-tRNA synthetase. J Biol Chem 264:13005–13011

    PubMed  Google Scholar 

  • Kunkel TA (1985) The mutational specificity of DNA polymerase-α and-γ duringin vitro DNA synthesis. J Biol Chem 260:12866–12874

    PubMed  Google Scholar 

  • Martens PA, Clayton DA (1979) Mechanism of mitochondrial DNA replication in mouse L-cell: localization and sequence of the light-strand origin of replication. J Mol Biol 135:327–351

    PubMed  Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacteria evolution. Proc Natl Acad Sci USA 84:166–169

    PubMed  Google Scholar 

  • Ohama T, Muto A, Osawa S (1990) Role of GC-biases mutation pressure on synonymous codon choice inMicroccus luteus, a bacterium with a high genomic GC-content. Nucleic Acids Res 18:1565–1569

    PubMed  Google Scholar 

  • Osawa S, Jukes TH (1989) Codon reassignment (codon capture) in evolution. J Mol Evol 28:271–278

    PubMed  Google Scholar 

  • Osawa S, Ohama T, Yamao F, Muto A, Jukes TH, Ozeki H, Umesono K (1988) Directional mutation pressure and transfer RNA in choice of the third nucleotide of synonymous two-codon sets. Proc Natl Acad Sci USA 85:1124–1128

    PubMed  Google Scholar 

  • Robberson DL, Kasamatsu H, Vinograd J (1972) Replication of mitochondrial DNA. Circular replicative intermediates in mouse L cells. Proc Natl Acad Sci USA 69:737–741

    PubMed  Google Scholar 

  • Roe BA, Wong JFH, Chen EY, Armstrong PA (1981) Sequence analysis of mammalian mitochondrial tRNAs. In: Walton AG (ed) Proceedings of the third Cleveland symposium. Elsevier, Amsterdam, pp 167–176

    Google Scholar 

  • Roe BA, Ma D-P, Wilson RK, Wong JFH (1985) The complete nucleotide sequence of theXenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774

    PubMed  Google Scholar 

  • Smith MJ, Banfield DK, Doteval K, Gorski S, Kowbel DJ (1989) Gene arrangement in sea star mitochondrial DNA demonstrates a major inversion event during echinoderm evolution. Gene 76:181–185

    PubMed  Google Scholar 

  • Sprinzl M, Hartmann, T, Weber J, Blank J, Zeidler R (1989) compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 17:r1-r171

    Google Scholar 

  • Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592

    PubMed  Google Scholar 

  • Takeishi K, Gotoh O (1982) Sequence relationship among various 4.5S RNA species. J Biochem 92:1173–1177

    PubMed  Google Scholar 

  • Thomas WK, Maa J, Wilson AC (1989) Shifting constraints on tRNA genes during mitochondrial DNA evolution in animals. New Biol 1:93–100

    PubMed  Google Scholar 

  • Wolstenholme DR, Macfarlane JL, Okimoto R, Clary DO, Wahleithner JA (1987) Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci USA 84:1324–1328

    PubMed  Google Scholar 

  • Yokogawa T, Kumazawa Y, Miura K, Watanabe K (1989) Purification and characterization of two serine isoaccepter tRNAs from bovine mitochondria by using a hybridization assay method. Nucleic Acids Res 17:2623–2638

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Yoshinori Kumazawa

    Present address: Department of Molecular and Cell Biology, University of California, 94720, Berkeley, CA, USA

Authors and Affiliations

  1. Department of Industrial Chemistry, Faculty of Engineering, University of Tokyo, Hongo, Bunkyo-ku, 113, Tokyo, Japan

    Shuichi Asakawa, Takeyoshi Araki & Kin-ichiro Miura

  2. Department of Biological Sciences, Faculty of Bioscience and Biotechnology, Tokyo Institute of Technology, Nagatsuta, 227, Yokohama, Japan

    Yoshinori Kumazawa & Kimitsuna Watanabe

  3. Institute of Space and Astronautical Science, 229, Sagamihara, Kanagawa, Japan

    Hyouta Himeno

Authors
  1. Shuichi Asakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshinori Kumazawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takeyoshi Araki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hyouta Himeno
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kin-ichiro Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kimitsuna Watanabe
    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

Asakawa, S., Kumazawa, Y., Araki, T. et al. Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32, 511–520 (1991). https://doi.org/10.1007/BF02102653

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02102653

Key words

Search

Navigation