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. 1998 Nov;150(3):1115–1123. doi: 10.1093/genetics/150.3.1115

The mitochondrial genome of the hemichordate Balanoglossus carnosus and the evolution of deuterostome mitochondria.

J Castresana 1, G Feldmaier-Fuchs 1, S Yokobori 1, N Satoh 1, S Pääbo 1
PMCID: PMC1460392  PMID: 9799263

Abstract

The complete nucleotide sequence of the mitochondrial genome of the hemichordate Balanoglossus carnosus (acorn worm) was determined. The arrangement of the genes encoding 13 protein, 22 tRNA, and 2 rRNA genes is essentially the same as in vertebrates, indicating that the vertebrate and hemichordate mitochondrial gene arrangement is close to that of their common ancestor, and, thus, that it has been conserved for more than 600 million years, whereas that of echinoderms has been rearranged extensively. The genetic code of hemichordate mitochondria is similar to that of echinoderms in that ATA encodes isoleucine and AGA serine, whereas the codons AAA and AGG, whose amino acid assignments also differ between echinoderms and vertebrates, are absent from the B. carnosus mitochondrial genome. There are three noncoding regions of length 277, 41, and 32 bp: the larger one is likely to be equivalent to the control region of other deuterostomes, while the two others may contain transcriptional promoters for genes encoded on the minor coding strand. Phylogenetic trees estimated from the inferred protein sequences indicate that hemichordates are a sister group of echinoderms.

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Selected References

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

  1. 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]
  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. 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]
  4. Ayala F. J., Rzhetsky A., Ayala F. J. Origin of the metazoan phyla: molecular clocks confirm paleontological estimates. Proc Natl Acad Sci U S A. 1998 Jan 20;95(2):606–611. doi: 10.1073/pnas.95.2.606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boore J. L., Brown W. M. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics. 1994 Oct;138(2):423–443. doi: 10.1093/genetics/138.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boore J. L., Collins T. M., Stanton D., Daehler L. L., Brown W. M. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature. 1995 Jul 13;376(6536):163–165. doi: 10.1038/376163a0. [DOI] [PubMed] [Google Scholar]
  7. Börner G. V., Yokobori S., Mörl M., Dörner M., Päbo S. RNA editing in metazoan mitochondria: staying fit without sex. FEBS Lett. 1997 Jun 16;409(3):320–324. doi: 10.1016/s0014-5793(97)00357-8. [DOI] [PubMed] [Google Scholar]
  8. Cantatore P., Gadaleta M. N., Roberti M., Saccone C., Wilson A. C. Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. 1987 Oct 29-Nov 4Nature. 329(6142):853–855. doi: 10.1038/329853a0. [DOI] [PubMed] [Google Scholar]
  9. Cantatore P., Roberti M., Rainaldi G., Gadaleta M. N., Saccone C. The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J Biol Chem. 1989 Jul 5;264(19):10965–10975. [PubMed] [Google Scholar]
  10. Castresana J., Feldmaier-Fuchs G., Päbo S. Codon reassignment and amino acid composition in hemichordate mitochondria. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3703–3707. doi: 10.1073/pnas.95.7.3703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Christianson T., Rabinowitz M. Identification of multiple transcriptional initiation sites on the yeast mitochondrial genome by in vitro capping with guanylyltransferase. J Biol Chem. 1983 Nov 25;258(22):14025–14033. [PubMed] [Google Scholar]
  12. De Giorgi C., Martiradonna A., Lanave C., Saccone C. Complete sequence of the mitochondrial DNA in the sea urchin Arbacia lixula: conserved features of the echinoid mitochondrial genome. Mol Phylogenet Evol. 1996 Apr;5(2):323–332. doi: 10.1006/mpev.1996.0027. [DOI] [PubMed] [Google Scholar]
  13. Delarbre C., Barriel V., Tillier S., Janvier P., Gachelin G. The main features of the craniate mitochondrial DNA between the ND1 and the COI genes were established in the common ancestor with the lancelet. Mol Biol Evol. 1997 Aug;14(8):807–813. doi: 10.1093/oxfordjournals.molbev.a025821. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Elliott D. J., Jacobs H. T. Mutually exclusive synthetic pathways for sea urchin mitochondrial rRNA and mRNA. Mol Cell Biol. 1989 Mar;9(3):1069–1082. doi: 10.1128/mcb.9.3.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fearnley I. M., Walker J. E. Two overlapping genes in bovine mitochondrial DNA encode membrane components of ATP synthase. EMBO J. 1986 Aug;5(8):2003–2008. doi: 10.1002/j.1460-2075.1986.tb04456.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Halanych K. M. The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Mol Phylogenet Evol. 1995 Mar;4(1):72–76. doi: 10.1006/mpev.1995.1007. [DOI] [PubMed] [Google Scholar]
  18. Hann S. R., King M. W., Bentley D. L., Anderson C. W., Eisenman R. N. A non-AUG translational initiation in c-myc exon 1 generates an N-terminally distinct protein whose synthesis is disrupted in Burkitt's lymphomas. Cell. 1988 Jan 29;52(2):185–195. doi: 10.1016/0092-8674(88)90507-7. [DOI] [PubMed] [Google Scholar]
  19. Hoffmann R. J., Boore J. L., Brown W. M. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics. 1992 Jun;131(2):397–412. doi: 10.1093/genetics/131.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Holland P. W., Hacker A. M., Williams N. A. A molecular analysis of the phylogenetic affinities of Saccoglossus cambrensis Brambell & Cole (Hemichordata). Philos Trans R Soc Lond B Biol Sci. 1991 Jun 29;332(1264):185–189. doi: 10.1098/rstb.1991.0048. [DOI] [PubMed] [Google Scholar]
  21. Jacobs H. T., Asakawa S., Araki T., Miura K., Smith M. J., Watanabe K. Conserved tRNA gene cluster in starfish mitochondrial DNA. Curr Genet. 1989 Mar;15(3):193–206. doi: 10.1007/BF00435506. [DOI] [PubMed] [Google Scholar]
  22. Jacobs H. T., Elliott D. J., Math V. B., Farquharson A. Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol. 1988 Jul 20;202(2):185–217. doi: 10.1016/0022-2836(88)90452-4. [DOI] [PubMed] [Google Scholar]
  23. Jacobs H. T., Herbert E. R., Rankine J. Sea urchin egg mitochondrial DNA contains a short displacement loop (D-loop) in the replication origin region. Nucleic Acids Res. 1989 Nov 25;17(22):8949–8965. doi: 10.1093/nar/17.22.8949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jones D. T., Taylor W. R., Thornton J. M. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992 Jun;8(3):275–282. doi: 10.1093/bioinformatics/8.3.275. [DOI] [PubMed] [Google Scholar]
  25. Kishino H., Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989 Aug;29(2):170–179. doi: 10.1007/BF02100115. [DOI] [PubMed] [Google Scholar]
  26. Kocher T. D., Thomas W. K., Meyer A., Edwards S. V., Päbo S., Villablanca F. X., Wilson A. C. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6196–6200. doi: 10.1073/pnas.86.16.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. L'Abbé D., Lang B. F., Desjardins P., Morais R. Histidine tRNA from chicken mitochondria has an uncoded 5'-terminal guanylate residue. J Biol Chem. 1990 Feb 15;265(5):2988–2992. [PubMed] [Google Scholar]
  28. Naylor G. J., Brown W. M. Structural biology and phylogenetic estimation. Nature. 1997 Aug 7;388(6642):527–528. doi: 10.1038/41460. [DOI] [PubMed] [Google Scholar]
  29. Nei M. Phylogenetic analysis in molecular evolutionary genetics. Annu Rev Genet. 1996;30:371–403. doi: 10.1146/annurev.genet.30.1.371. [DOI] [PubMed] [Google Scholar]
  30. Osawa S., Jukes T. H. Codon reassignment (codon capture) in evolution. J Mol Evol. 1989 Apr;28(4):271–278. doi: 10.1007/BF02103422. [DOI] [PubMed] [Google Scholar]
  31. Peabody D. S. Translation initiation at non-AUG triplets in mammalian cells. J Biol Chem. 1989 Mar 25;264(9):5031–5035. [PubMed] [Google Scholar]
  32. Rasmussen A. S., Janke A., Arnason U. The mitochondrial DNA molecule of the hagfish (Myxine glutinosa) and vertebrate phylogeny. J Mol Evol. 1998 Apr;46(4):382–388. doi: 10.1007/pl00006317. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Shadel G. S., Clayton D. A. Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem. 1997;66:409–435. doi: 10.1146/annurev.biochem.66.1.409. [DOI] [PubMed] [Google Scholar]
  35. Sprinzl M., Hartmann T., Weber J., Blank J., Zeidler R. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1989;17 (Suppl):r1–172. doi: 10.1093/nar/17.suppl.r1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Turbeville J. M., Schulz J. R., Raff R. A. Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. Mol Biol Evol. 1994 Jul;11(4):648–655. doi: 10.1093/oxfordjournals.molbev.a040143. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Wada H., Satoh N. Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1801–1804. doi: 10.1073/pnas.91.5.1801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Yokobori S., Päbo S. Polyadenylation creates the discriminator nucleotide of chicken mitochondrial tRNA(Tyr). J Mol Biol. 1997 Jan 17;265(2):95–99. doi: 10.1006/jmbi.1996.0728. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. 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]

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