Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1994 May;137(1):243–256. doi: 10.1093/genetics/137.1.243

The Marsupial Mitochondrial Genome and the Evolution of Placental Mammals

A Janke 1, G Feldmaier-Fuchs 1, W K Thomas 1, A von-Haeseler 1, S Paabo 1
PMCID: PMC1205941  PMID: 8056314

Abstract

The entire nucleotide sequence of the mitochondrial genome of the American opossum, Didelphis virginiana, was determined. Two major features distinguish this genome from those of other mammals. First, five tRNA genes around the origin of light strand replication are rearranged. Second, the anticodon of tRNA(Asp) is posttranscriptionally changed by an RNA editing process such that its coding capacity is altered. When the complete protein-coding region of the mitochondrial genome is used as an outgroup for placental mammals it can be shown that rodents represent an earlier branch among placental mammals than primates and artiodactyls and that artiodactyls share a common ancestor with carnivores. The overall rates of evolution of most of the mitochondrial genome of placentals are clocklike. Furthermore, the data indicate that the lineages leading to the mouse and rat may have diverged from each other as much as 35 million years ago.

Full Text

The Full Text of this article is available as a PDF (2.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adachi J., Cao Y., Hasegawa M. Tempo and mode of mitochondrial DNA evolution in vertebrates at the amino acid sequence level: rapid evolution in warm-blooded vertebrates. J Mol Evol. 1993 Mar;36(3):270–281. doi: 10.1007/BF00160483. [DOI] [PubMed] [Google Scholar]
  2. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  3. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  4. Arnason E., Rand D. M. Heteroplasmy of short tandem repeats in mitochondrial DNA of Atlantic cod, Gadus morhua. Genetics. 1992 Sep;132(1):211–220. doi: 10.1093/genetics/132.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Arnason U., Gullberg A., Widegren B. The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J Mol Evol. 1991 Dec;33(6):556–568. doi: 10.1007/BF02102808. [DOI] [PubMed] [Google Scholar]
  6. Arnason U., Johnsson E. The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol. 1992 Jun;34(6):493–505. doi: 10.1007/BF00160463. [DOI] [PubMed] [Google Scholar]
  7. Bibb M. J., Van Etten R. A., Wright C. T., Walberg M. W., Clayton D. A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981 Oct;26(2 Pt 2):167–180. doi: 10.1016/0092-8674(81)90300-7. [DOI] [PubMed] [Google Scholar]
  8. Brown W. M., Prager E. M., Wang A., Wilson A. C. Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol. 1982;18(4):225–239. doi: 10.1007/BF01734101. [DOI] [PubMed] [Google Scholar]
  9. Bulmer M., Wolfe K. H., Sharp P. M. Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):5974–5978. doi: 10.1073/pnas.88.14.5974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cabot E. L., Beckenbach A. T. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci. 1989 Jul;5(3):233–234. doi: 10.1093/bioinformatics/5.3.233. [DOI] [PubMed] [Google Scholar]
  11. Chevret P., Denys C., Jaeger J. J., Michaux J., Catzeflis F. M. Molecular evidence that the spiny mouse (Acomys) is more closely related to gerbils (Gerbillinae) than to true mice (Murinae). Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3433–3436. doi: 10.1073/pnas.90.8.3433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Covello P. S., Gray M. W. RNA editing in plant mitochondria. Nature. 1989 Oct 19;341(6243):662–666. doi: 10.1038/341662a0. [DOI] [PubMed] [Google Scholar]
  13. DeSalle R., Freedman T., Prager E. M., Wilson A. C. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol. 1987;26(1-2):157–164. doi: 10.1007/BF02111289. [DOI] [PubMed] [Google Scholar]
  14. Easteal S. A mammalian molecular clock? Bioessays. 1992 Jun;14(6):415–419. doi: 10.1002/bies.950140613. [DOI] [PubMed] [Google Scholar]
  15. Easteal S. The pattern of mammalian evolution and the relative rate of molecular evolution. Genetics. 1990 Jan;124(1):165–173. doi: 10.1093/genetics/124.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. doi: 10.1007/BF01734359. [DOI] [PubMed] [Google Scholar]
  17. Gadaleta G., Pepe G., De Candia G., Quagliariello C., Sbisà E., Saccone C. The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol. 1989 Jun;28(6):497–516. doi: 10.1007/BF02602930. [DOI] [PubMed] [Google Scholar]
  18. Gu X., Li W. H. Higher rates of amino acid substitution in rodents than in humans. Mol Phylogenet Evol. 1992 Sep;1(3):211–214. doi: 10.1016/1055-7903(92)90017-b. [DOI] [PubMed] [Google Scholar]
  19. Gualberto J. M., Lamattina L., Bonnard G., Weil J. H., Grienenberger J. M. RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature. 1989 Oct 19;341(6243):660–662. doi: 10.1038/341660a0. [DOI] [PubMed] [Google Scholar]
  20. Hauswirth W. W., Van de Walle M. J., Laipis P. J., Olivo P. D. Heterogeneous mitochondrial DNA D-loop sequences in bovine tissue. Cell. 1984 Jul;37(3):1001–1007. doi: 10.1016/0092-8674(84)90434-3. [DOI] [PubMed] [Google Scholar]
  21. Hoch B., Maier R. M., Appel K., Igloi G. L., Kössel H. Editing of a chloroplast mRNA by creation of an initiation codon. Nature. 1991 Sep 12;353(6340):178–180. doi: 10.1038/353178a0. [DOI] [PubMed] [Google Scholar]
  22. Hodges P. E., Navaratnam N., Greeve J. C., Scott J. Site-specific creation of uridine from cytidine in apolipoprotein B mRNA editing. Nucleic Acids Res. 1991 Mar 25;19(6):1197–1201. doi: 10.1093/nar/19.6.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Irwin D. M., Kocher T. D., Wilson A. C. Evolution of the cytochrome b gene of mammals. J Mol Evol. 1991 Feb;32(2):128–144. doi: 10.1007/BF02515385. [DOI] [PubMed] [Google Scholar]
  24. Janke A., Päbo S. Editing of a tRNA anticodon in marsupial mitochondria changes its codon recognition. Nucleic Acids Res. 1993 Apr 11;21(7):1523–1525. doi: 10.1093/nar/21.7.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lansman R. A., Shade R. O., Shapira J. F., Avise J. C. The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. III. Techniques and potential applications. J Mol Evol. 1981;17(4):214–226. doi: 10.1007/BF01732759. [DOI] [PubMed] [Google Scholar]
  26. Li W. H., Gouy M., Sharp P. M., O'hUigin C., Yang Y. W. Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6703–6707. doi: 10.1073/pnas.87.17.6703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ma D. P., Zharkikh A., Graur D., VandeBerg J. L., Li W. H. Structure and evolution of opossum, guinea pig, and porcupine cytochrome b genes. J Mol Evol. 1993 Apr;36(4):327–334. doi: 10.1007/BF00182180. [DOI] [PubMed] [Google Scholar]
  28. Mignotte F., Gueride M., Champagne A. M., Mounolou J. C. Direct repeats in the non-coding region of rabbit mitochondrial DNA. Involvement in the generation of intra- and inter-individual heterogeneity. Eur J Biochem. 1990 Dec 12;194(2):561–571. doi: 10.1111/j.1432-1033.1990.tb15653.x. [DOI] [PubMed] [Google Scholar]
  29. Muto A., Osawa S. The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci U S A. 1987 Jan;84(1):166–169. doi: 10.1073/pnas.84.1.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Novacek M. J. Mammalian phylogeny: shaking the tree. Nature. 1992 Mar 12;356(6365):121–125. doi: 10.1038/356121a0. [DOI] [PubMed] [Google Scholar]
  31. Päbo S., Thomas W. K., Whitfield K. M., Kumazawa Y., Wilson A. C. Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol. 1991 Nov;33(5):426–430. doi: 10.1007/BF02103134. [DOI] [PubMed] [Google Scholar]
  32. Roe B. A., Ma D. P., Wilson R. K., Wong J. F. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem. 1985 Aug 15;260(17):9759–9774. [PubMed] [Google Scholar]
  33. Saccone C., Pesole G., Sbisá E. The main regulatory region of mammalian mitochondrial DNA: structure-function model and evolutionary pattern. J Mol Evol. 1991 Jul;33(1):83–91. doi: 10.1007/BF02100199. [DOI] [PubMed] [Google Scholar]
  34. Simpson L., Shaw J. RNA editing and the mitochondrial cryptogenes of kinetoplastid protozoa. Cell. 1989 May 5;57(3):355–366. doi: 10.1016/0092-8674(89)90911-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Solignac M., Monnerot M., Mounolou J. C. Mitochondrial DNA heteroplasmy in Drosophila mauritiana. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6942–6946. doi: 10.1073/pnas.80.22.6942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sueoka N. Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2653–2657. doi: 10.1073/pnas.85.8.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Walberg M. W., Clayton D. A. Sequence and properties of the human KB cell and mouse L cell D-loop regions of mitochondrial DNA. Nucleic Acids Res. 1981 Oct 24;9(20):5411–5421. doi: 10.1093/nar/9.20.5411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wilkinson G. S., Chapman A. M. Length and sequence variation in evening bat D-loop mtDNA. Genetics. 1991 Jul;128(3):607–617. doi: 10.1093/genetics/128.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wilson A. C., Carlson S. S., White T. J. Biochemical evolution. Annu Rev Biochem. 1977;46:573–639. doi: 10.1146/annurev.bi.46.070177.003041. [DOI] [PubMed] [Google Scholar]
  40. Yokogawa T., Watanabe Y., Kumazawa Y., Ueda T., Hirao I., Miura K., Watanabe K. A novel cloverleaf structure found in mammalian mitochondrial tRNA(Ser) (UCN). Nucleic Acids Res. 1991 Nov 25;19(22):6101–6105. doi: 10.1093/nar/19.22.6101. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES