Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Sep;150(1):313–329. doi: 10.1093/genetics/150.1.313

The complete nucleotide sequence of a snake (Dinodon semicarinatus) mitochondrial genome with two identical control regions.

Y Kumazawa 1, H Ota 1, M Nishida 1, T Ozawa 1
PMCID: PMC1460336  PMID: 9725849

Abstract

The 17,191-bp mitochondrial DNA (mtDNA) of a Japanese colubrid snake, akamata (Dinodon semicarinatus), was cloned and sequenced. The snake mtDNA has some peculiar features that were found in our previous study using polymerase chain reaction: duplicate control regions that have completely identical sequences over 1 kbp, translocation of tRNALeu(UUR) gene, shortened TpsiC arm for most tRNA genes, and a pseudogene for tRNAPro. Phylogenetic analysis of amino acid sequences of protein genes suggested an unusually high rate of molecular evolution in the snake compared to other vertebrates. Southern hybridization experiments using mtDNAs purified from multiple akamata individuals showed that the duplicate state of the control region is not a transient or unstable feature found in a particular individual, but that it stably occurs in mitochondrial genomes of the species. This may, therefore, be regarded as an unprecedented example of stable functional redundancy in animal mtDNA. However, some of the examined individuals contain a rather scanty proportion of heteroplasmic mtDNAs with an organization of genes distinct from that of the major mtDNA. The gene organization of the minor mtDNA is in agreement with one of models that we present to account for the concerted evolution of duplicate control regions.

Full Text

The Full Text of this article is available as a PDF (782.1 KB).

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. Adachi J., Hasegawa M. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol. 1996 Apr;42(4):459–468. doi: 10.1007/BF02498640. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  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. Asakawa S., Himeno H., Miura K., Watanabe K. Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics. 1995 Jul;140(3):1047–1060. doi: 10.1093/genetics/140.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Asakawa S., Kumazawa Y., Araki T., Himeno H., Miura K., Watanabe K. Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol. 1991 Jun;32(6):511–520. doi: 10.1007/BF02102653. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Christianson T. W., Clayton D. A. A tridecamer DNA sequence supports human mitochondrial RNA 3'-end formation in vitro. Mol Cell Biol. 1988 Oct;8(10):4502–4509. doi: 10.1128/mcb.8.10.4502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clayton D. A. Transcription and replication of animal mitochondrial DNAs. Int Rev Cytol. 1992;141:217–232. doi: 10.1016/s0074-7696(08)62067-7. [DOI] [PubMed] [Google Scholar]
  11. Desjardins P., Morais R. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990 Apr 20;212(4):599–634. doi: 10.1016/0022-2836(90)90225-B. [DOI] [PubMed] [Google Scholar]
  12. Doda J. N., Wright C. T., Clayton D. A. Elongation of displacement-loop strands in human and mouse mitochondrial DNA is arrested near specific template sequences. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6116–6120. doi: 10.1073/pnas.78.10.6116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drouin J. Cloning of human mitochondrial DNA in Escherichia coli. J Mol Biol. 1980 Jun 15;140(1):15–34. doi: 10.1016/0022-2836(80)90354-x. [DOI] [PubMed] [Google Scholar]
  14. Gach M. H., Brown W. M. Characteristics and distribution of large tandem duplications in brook stickleback (Culaea inconstans) mitochondrial DNA. Genetics. 1997 Feb;145(2):383–394. doi: 10.1093/genetics/145.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Gelfand R., Attardi G. Synthesis and turnover of mitochondrial ribonucleic acid in HeLa cells: the mature ribosomal and messenger ribonucleic acid species are metabolically unstable. Mol Cell Biol. 1981 Jun;1(6):497–511. doi: 10.1128/mcb.1.6.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hedges S. B. Molecular evidence for the origin of birds. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2621–2624. doi: 10.1073/pnas.91.7.2621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Härlid A., Janke A., Arnason U. The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. Mol Biol Evol. 1997 Jul;14(7):754–761. doi: 10.1093/oxfordjournals.molbev.a025815. [DOI] [PubMed] [Google Scholar]
  19. Janke A., Arnason U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles). Mol Biol Evol. 1997 Dec;14(12):1266–1272. doi: 10.1093/oxfordjournals.molbev.a025736. [DOI] [PubMed] [Google Scholar]
  20. Janke A., Feldmaier-Fuchs G., Thomas W. K., von Haeseler A., Päbo S. The marsupial mitochondrial genome and the evolution of placental mammals. Genetics. 1994 May;137(1):243–256. doi: 10.1093/genetics/137.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Janke A., Gemmell N. J., Feldmaier-Fuchs G., von Haeseler A., Päbo S. The mitochondrial genome of a monotreme--the platypus (Ornithorhynchus anatinus). J Mol Evol. 1996 Feb;42(2):153–159. doi: 10.1007/BF02198841. [DOI] [PubMed] [Google Scholar]
  22. Kumazawa Y., Nishida M. Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol. 1993 Oct;37(4):380–398. doi: 10.1007/BF00178868. [DOI] [PubMed] [Google Scholar]
  23. Kumazawa Y., Nishida M. Variations in mitochondrial tRNA gene organization of reptiles as phylogenetic markers. Mol Biol Evol. 1995 Sep;12(5):759–772. doi: 10.1093/oxfordjournals.molbev.a040254. [DOI] [PubMed] [Google Scholar]
  24. Kumazawa Y., Ota H., Nishida M., Ozawa T. Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Mol Biol Evol. 1996 Nov;13(9):1242–1254. doi: 10.1093/oxfordjournals.molbev.a025690. [DOI] [PubMed] [Google Scholar]
  25. Lee W. J., Conroy J., Howell W. H., Kocher T. D. Structure and evolution of teleost mitochondrial control regions. J Mol Evol. 1995 Jul;41(1):54–66. doi: 10.1007/BF00174041. [DOI] [PubMed] [Google Scholar]
  26. Lunt D. H., Hyman B. C. Animal mitochondrial DNA recombination. Nature. 1997 May 15;387(6630):247–247. doi: 10.1038/387247a0. [DOI] [PubMed] [Google Scholar]
  27. Macey J. R., Larson A., Ananjeva N. B., Fang Z., Papenfuss T. J. Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Mol Biol Evol. 1997 Jan;14(1):91–104. doi: 10.1093/oxfordjournals.molbev.a025706. [DOI] [PubMed] [Google Scholar]
  28. Macey J. R., Schulte J. A., 2nd, Larson A., Papenfuss T. J. Tandem duplication via light-strand synthesis may provide a precursor for mitochondrial genomic rearrangement. Mol Biol Evol. 1998 Jan;15(1):71–75. doi: 10.1093/oxfordjournals.molbev.a025849. [DOI] [PubMed] [Google Scholar]
  29. Moritz C., Brown W. M. Tandem duplication of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science. 1986 Sep 26;233(4771):1425–1427. doi: 10.1126/science.3018925. [DOI] [PubMed] [Google Scholar]
  30. Moritz C., Brown W. M. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7183–7187. doi: 10.1073/pnas.84.20.7183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ojala D., Montoya J., Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981 Apr 9;290(5806):470–474. doi: 10.1038/290470a0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Quinn T. W., Mindell D. P. Mitochondrial gene order adjacent to the control region in crocodile, turtle, and tuatara. Mol Phylogenet Evol. 1996 Apr;5(2):344–351. doi: 10.1006/mpev.1996.0029. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Seutin G., Lang B. F., Mindell D. P., Morais R. Evolution of the WANCY region in amniote mitochondrial DNA. Mol Biol Evol. 1994 May;11(3):329–340. doi: 10.1093/oxfordjournals.molbev.a040116. [DOI] [PubMed] [Google Scholar]
  36. Stanton D. J., Daehler L. L., Moritz C. C., Brown W. M. Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA. Genetics. 1994 May;137(1):233–241. doi: 10.1093/genetics/137.1.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tapper D. P., Van Etten R. A., Clayton D. A. Isolation of mammalian mitochondrial DNA and RNA and cloning of the mitochondrial genome. Methods Enzymol. 1983;97:426–434. doi: 10.1016/0076-6879(83)97153-7. [DOI] [PubMed] [Google Scholar]
  38. Thomas W. K., Beckenbach A. T. Variation in salmonid mitochondrial DNA: evolutionary constraints and mechanisms of substitution. J Mol Evol. 1989 Sep;29(3):233–245. doi: 10.1007/BF02100207. [DOI] [PubMed] [Google Scholar]
  39. Thyagarajan B., Padua R. A., Campbell C. Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem. 1996 Nov 1;271(44):27536–27543. doi: 10.1074/jbc.271.44.27536. [DOI] [PubMed] [Google Scholar]
  40. Tzeng C. S., Hui C. F., Shen S. C., Huang P. C. The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res. 1992 Sep 25;20(18):4853–4858. doi: 10.1093/nar/20.18.4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wallis G. P. Mitochondrial DNA insertion polymorphism and germ line heteroplasmy in the Triturus cristatus complex. Heredity (Edinb) 1987 Apr;58(Pt 2):229–238. doi: 10.1038/hdy.1987.37. [DOI] [PubMed] [Google Scholar]
  42. Wolstenholme D. R. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 1992;141:173–216. doi: 10.1016/s0074-7696(08)62066-5. [DOI] [PubMed] [Google Scholar]
  43. Wong T. W., Clayton D. A. In vitro replication of human mitochondrial DNA: accurate initiation at the origin of light-strand synthesis. Cell. 1985 Oct;42(3):951–958. doi: 10.1016/0092-8674(85)90291-0. [DOI] [PubMed] [Google Scholar]
  44. Yokobori S. I., Päbo S. tRNA editing in metazoans. Nature. 1995 Oct 12;377(6549):490–490. doi: 10.1038/377490a0. [DOI] [PubMed] [Google Scholar]
  45. Yokobori S., Päbo S. Transfer RNA editing in land snail mitochondria. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10432–10435. doi: 10.1073/pnas.92.22.10432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yoneyama Y. [The nucleotide sequences of the heavy and light strand replication origins of the Rana catesbeiana mitochondrial genome]. Nihon Ika Daigaku Zasshi. 1987 Aug;54(4):429–440. doi: 10.1272/jnms1923.54.429. [DOI] [PubMed] [Google Scholar]
  47. Zardoya R., Meyer A. The complete DNA sequence of the mitochondrial genome of a "living fossil," the coelacanth (Latimeria chalumnae). Genetics. 1997 Jul;146(3):995–1010. doi: 10.1093/genetics/146.3.995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zardoya R., Meyer A. The complete nucleotide sequence of the mitochondrial genome of the lungfish (Protopterus dolloi) supports its phylogenetic position as a close relative of land vertebrates. Genetics. 1996 Apr;142(4):1249–1263. doi: 10.1093/genetics/142.4.1249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zevering C. E., Moritz C., Heideman A., Sturm R. A. Parallel origins of duplications and the formation of pseudogenes in mitochondrial DNA from parthenogenetic lizards (Heteronotia binoei; Gekkonidae). J Mol Evol. 1991 Nov;33(5):431–441. doi: 10.1007/BF02103135. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES