Journal of Molecular Evolution

, Volume 33, Issue 5, pp 426–430 | Cite as

Rearrangements of mitochondrial transfer RNA genes in marsupials

  • Svante Pääbo
  • W. Kelley Thomas
  • Kristina M. Whitfield
  • Yoshinori Kumazawa
  • Allan C. Wilson
Article

Summary

The nucleotide sequences of the mitochondrial origin of light-strand replication and the five tRNA genes surrounding it were determined for three marsupials. The region was found to be rearranged, leaving only the tRNATyr gene at the same position as in placental mammals andXenopus. Distribution of the same rearranged genotype among two marsupial families indicates that the events causing the rearrangements took place in an early marsupial ancestor. The putative mitochondrial light-strand origin of replication in marsupials contains a hairpin structure similar to other vertebrate origins and, in addition, extensive flanking sequences that are not found in other vertebrates. Sequence comparisons among the marsupials as well as placentals indicate that the tRNATyr gene has been evolving under more constraints than the other tRNA genes.

Key words

Mitochondrial DNA Marsupials tRNA genes Genome organization Evolutionary constraints 

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References

  1. 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 290:457–465CrossRefPubMedGoogle Scholar
  2. Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA. J Mol Biol 156:683–717CrossRefPubMedGoogle Scholar
  3. Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180CrossRefPubMedGoogle Scholar
  4. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239CrossRefPubMedGoogle Scholar
  5. Buroker NE, Brown JR, Gilbert TA, O'Hara PJ, Beckenbach AT, Thomas WK, Smith MJ (1990) Length heteroplasmy of sturgeon mitochondrial DNA: an illegitimate elongation model. Genetics 124:157–163PubMedPubMedCentralGoogle Scholar
  6. Cantatore P, Gadaleta MN, Roberti M, Saccone C, Wilson AC (1987) Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature 329:853–855CrossRefPubMedGoogle Scholar
  7. Cantatore P, Roberti M, Rainaldi G, Gadaleta MN, Saccone C (1989) The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome ofParacentrotus lividus. J Biol Chem 264:10965–10975PubMedGoogle Scholar
  8. Cifelli RL, Eaton JG (1987) Marsupial from the earliest Late Cretaceous of western US. Nature 325:520–522CrossRefGoogle Scholar
  9. Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule ofDrosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271CrossRefPubMedGoogle Scholar
  10. Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome. J Mol Biol 212:599–634CrossRefPubMedGoogle Scholar
  11. Gadaleta G, Pepe G, De Candia G, Quagliariello C, Sbisà E, Saccone C (1989) The complete nucleotide sequence of theRattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516CrossRefPubMedGoogle Scholar
  12. Gaines G, Rossi C, Attardi G (1987) The excised leader of human cytochromec oxidase subunit I mRNA which contains the origin of mitochondrial DNA light-strand synthesis accumulates in mitochondria and is polyadenylated. Mol Cell Biol 7:925–931CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gelfand R, Attardi G (1981) Synthesis and turnover of mitochondrial ribonucleic acid in HeLa cells: the mature ribosomal messenger ribonucleic acid species are metabolically unstable. Mol Cell Biol 1:497–511CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hixson JE, Wong TW, Clayton DA (1986) Both the conserved stem-loop and divergent 5′-flanking sequences are required for initiation at the human mitochondrial origin of light-strand replication. J Biol Chem 261:2384–2390PubMedGoogle Scholar
  15. Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217CrossRefPubMedGoogle Scholar
  16. Johansen S, Guddal PH, Johansen T (1990) Organization of the mitochondrial genome of Atlantic cod,Gadus morhua. Nucleic Acids Res 18:411–419CrossRefPubMedPubMedCentralGoogle Scholar
  17. Maxson LR, Sarich VM, Wilson AC (1975) Continental drift and the use of albumin as an evolutionary clock. Nature 255: 397–400CrossRefGoogle Scholar
  18. Moritz C, Browm WM (1986) Tandem duplications of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science 233:1425–1427CrossRefPubMedGoogle Scholar
  19. Moritz C, Brown WM (1987) Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA 84:7183–7187CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ojala D, Merkel C, Gelfand R, Attardi G (1980) The tRNA genes punctuate the reading of genetic information in human mitochondrial DNA. Cell 22:393–403CrossRefPubMedGoogle Scholar
  21. Pääbo S, Gifford JA, Wilson AC (1988) Mitochondrial DNA sequences from a 7000 year old brain. Nucleic Acids Res 16: 9775–9787CrossRefPubMedPubMedCentralGoogle Scholar
  22. Roe BA, Ma D-P, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of theXenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774PubMedGoogle Scholar
  23. Sprinzl M, Hartmann T, Meissner F, Moll J, Vorderwülbecke T (1987) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res [suppl] 15:r53-r188CrossRefPubMedPubMedCentralGoogle Scholar
  24. Thomas RH, Schaffner W, Wilson AC, Pääbo S (1989) DNA phylogeny of the extinct marsupial wolf. Nature 340:465–467CrossRefPubMedGoogle Scholar
  25. 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 84:1324–1328CrossRefPubMedPubMedCentralGoogle Scholar
  26. Yoneyama Y (1987) The nucleotide sequences of the heavy and light strand replication origins of theRana catesbeiana mitochondrial genome. Nippon Ika Daioaku Zasshi 54:429–440 [in Japanese]CrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1991

Authors and Affiliations

  • Svante Pääbo
    • 1
    • 2
  • W. Kelley Thomas
    • 1
  • Kristina M. Whitfield
    • 1
  • Yoshinori Kumazawa
    • 1
    • 3
  • Allan C. Wilson
    • 1
  1. 1.Division of Biochemistry and Molecular BiologyUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of ZoologyUniversity of MunichMunich 2Germany
  3. 3.Department of Life ChemistryTokyo Institute of TechnologyNagatsuta, YokohamaJapan

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