Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Apr;148(4):1907–1919. doi: 10.1093/genetics/148.4.1907

Heteroplasmy, length and sequence variation in the mtDNA control regions of three percid fish species (Perca fluviatilis, Acerina cernua, Stizostedion lucioperca).

C L Nesbø 1, M O Arab 1, K S Jakobsen 1
PMCID: PMC1460080  PMID: 9560404

Abstract

The nucleotide sequence of the control region and flanking tRNA genes of perch (Perca fluviatilis) mtDNA was determined. The organization of this region is similar to that of other vertebrates. A tandem array of 10-bp repeats, associated with length variation and heteroplasmy was observed in the 5' end. While the location of the array corresponds to that reported in other species, the length of the repeated unit is shorter than previously observed for tandem repeats in this region. The repeated sequence was highly similar to the Mt5 element which has been shown to specifically bind a putative D-loop DNA termination protein. Of 149 perch analyzed, 74% showed length variation heteroplasmy. Single-cell PCR on oocytes suggested that the high level of heteroplasmy is passively maintained by maternal transmission. The array was also observed in the two other percid species, ruffe (Acerina cernua) and zander (Stizostedion lucioperca). The array and the associated length variation heteroplasmy are therefore likely to be general features of percid mtDNAs. Among the perch repeats, the mutation pattern is consistent with unidirectional slippage, and statistical analyses supported the notion that the various haplotypes are associated with different levels of heteroplasmy. The variation in array length among and within species is ascribed to differences in predicted stability of secondary structures made between repeat units.

Full Text

The Full Text of this article is available as a PDF (231.8 KB).

Selected References

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

  1. 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]
  2. 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]
  3. Bentzen P., Leggett W. C., Brown G. G. Length and restriction site heteroplasmy in the mitochondrial DNA of american shad (alosa sapidissima). Genetics. 1988 Mar;118(3):509–518. doi: 10.1093/genetics/118.3.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bogenhagen D. F., Yoza B. K. Accurate in vitro transcription of Xenopus laevis mitochondrial DNA from two bidirectional promoters. Mol Cell Biol. 1986 Jul;6(7):2543–2550. doi: 10.1128/mcb.6.7.2543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Broughton R. E., Dowling T. E. Length variation in mitochondrial DNA of the minnow Cyprinella spiloptera. Genetics. 1994 Sep;138(1):179–190. doi: 10.1093/genetics/138.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown J. R., Beckenbach A. T., Smith M. J. Mitochondrial DNA length variation and heteroplasmy in populations of white sturgeon (Acipenser transmontanus). Genetics. 1992 Sep;132(1):221–228. doi: 10.1093/genetics/132.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown J. R., Beckenbach K., Beckenbach A. T., Smith M. J. Length variation, heteroplasmy and sequence divergence in the mitochondrial DNA of four species of sturgeon (Acipenser). Genetics. 1996 Feb;142(2):525–535. doi: 10.1093/genetics/142.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buroker N. E., Brown J. R., Gilbert T. A., O'Hara P. J., Beckenbach A. T., Thomas W. K., Smith M. J. Length heteroplasmy of sturgeon mitochondrial DNA: an illegitimate elongation model. Genetics. 1990 Jan;124(1):157–163. doi: 10.1093/genetics/124.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Casane D., Dennebouy N., de Rochambeau H., Mounolou J. C., Monnerot M. Genetic analysis of systematic mitochondrial heteroplasmy in rabbits. Genetics. 1994 Oct;138(2):471–480. doi: 10.1093/genetics/138.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Casane D., Dennebouy N., de Rochambeau H., Mounolou J. C., Monnerot M. Nonneutral evolution of tandem repeats in the mitochondrial DNA control region of lagomorphs. Mol Biol Evol. 1997 Aug;14(8):779–789. doi: 10.1093/oxfordjournals.molbev.a025818. [DOI] [PubMed] [Google Scholar]
  11. Cecconi F., Giorgi M., Mariottini P. Unique features in the mitochondrial D-loop region of the European seabass Dicentrarchus labrax. Gene. 1995 Jul 28;160(2):149–155. doi: 10.1016/0378-1119(95)00232-u. [DOI] [PubMed] [Google Scholar]
  12. Chang D. D., Clayton D. A. Precise identification of individual promoters for transcription of each strand of human mitochondrial DNA. Cell. 1984 Mar;36(3):635–643. doi: 10.1016/0092-8674(84)90343-x. [DOI] [PubMed] [Google Scholar]
  13. Clayton D. A. Nuclear gadgets in mitochondrial DNA replication and transcription. Trends Biochem Sci. 1991 Mar;16(3):107–111. doi: 10.1016/0968-0004(91)90043-u. [DOI] [PubMed] [Google Scholar]
  14. Clayton D. A. Replication and transcription of vertebrate mitochondrial DNA. Annu Rev Cell Biol. 1991;7:453–478. doi: 10.1146/annurev.cb.07.110191.002321. [DOI] [PubMed] [Google Scholar]
  15. Clayton D. A. Replication of animal mitochondrial DNA. Cell. 1982 Apr;28(4):693–705. doi: 10.1016/0092-8674(82)90049-6. [DOI] [PubMed] [Google Scholar]
  16. Foran D. R., Hixson J. E., Brown W. M. Comparisons of ape and human sequences that regulate mitochondrial DNA transcription and D-loop DNA synthesis. Nucleic Acids Res. 1988 Jul 11;16(13):5841–5861. doi: 10.1093/nar/16.13.5841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fumagalli L., Taberlet P., Favre L., Hausser J. Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Mol Biol Evol. 1996 Jan;13(1):31–46. doi: 10.1093/oxfordjournals.molbev.a025568. [DOI] [PubMed] [Google Scholar]
  18. Hayasaka K., Ishida T., Horai S. Heteroplasmy and polymorphism in the major noncoding region of mitochondrial DNA in Japanese monkeys: association with tandemly repeated sequences. Mol Biol Evol. 1991 Jul;8(4):399–415. doi: 10.1093/oxfordjournals.molbev.a040660. [DOI] [PubMed] [Google Scholar]
  19. Hoelzel A. R., Hancock J. M., Dover G. A. Evolution of the cetacean mitochondrial D-loop region. Mol Biol Evol. 1991 Jul;8(4):475–493. doi: 10.1093/oxfordjournals.molbev.a040662. [DOI] [PubMed] [Google Scholar]
  20. Hultman T., Ståhl S., Hornes E., Uhlén M. Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res. 1989 Jul 11;17(13):4937–4946. doi: 10.1093/nar/17.13.4937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johansen S., Guddal P. H., Johansen T. Organization of the mitochondrial genome of Atlantic cod, Gadus morhua. Nucleic Acids Res. 1990 Feb 11;18(3):411–419. doi: 10.1093/nar/18.3.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Johansen S., Johansen T. The putative origin of heavy strand replication (oriH) in mitochondrial DNA is highly conserved among the teleost fishes. DNA Seq. 1993;3(6):397–399. doi: 10.3109/10425179309020843. [DOI] [PubMed] [Google Scholar]
  23. L'Abbé D., Duhaime J. F., Lang B. F., Morais R. The transcription of DNA in chicken mitochondria initiates from one major bidirectional promoter. J Biol Chem. 1991 Jun 15;266(17):10844–10850. [PubMed] [Google Scholar]
  24. 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]
  25. Madsen C. S., Ghivizzani S. C., Hauswirth W. W. In vivo and in vitro evidence for slipped mispairing in mammalian mitochondria. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7671–7675. doi: 10.1073/pnas.90.16.7671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Madsen C. S., Ghivizzani S. C., Hauswirth W. W. Protein binding to a single termination-associated sequence in the mitochondrial DNA D-loop region. Mol Cell Biol. 1993 Apr;13(4):2162–2171. doi: 10.1128/mcb.13.4.2162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miracle A. L., Campton D. E. Tandem repeat sequence variation and length heteroplasmy in the mitochondrial DNA D-loop of the threatened Gulf of Mexico sturgeon, Acipenser oxyrhynchus desotoi. J Hered. 1995 Jan-Feb;86(1):22–27. doi: 10.1093/oxfordjournals.jhered.a111520. [DOI] [PubMed] [Google Scholar]
  28. Ohno K., Tanaka M., Suzuki H., Ohbayashi T., Ikebe S., Ino H., Kumar S., Takahashi A., Ozawa T. Identification of a possible control element, Mt5, in the major noncoding region of mitochondrial DNA by intraspecific nucleotide conservation. Biochem Int. 1991 May;24(2):263–272. [PubMed] [Google Scholar]
  29. Rand D. M., Harrison R. G. Molecular population genetics of mtDNA size variation in crickets. Genetics. 1989 Mar;121(3):551–569. doi: 10.1093/genetics/121.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rudi K., Kroken M., Dahlberg O. J., Deggerdal A., Jakobsen K. S., Larsen F. Rapid, universal method to isolate PCR-ready DNA using magnetic beads. Biotechniques. 1997 Mar;22(3):506–511. doi: 10.2144/97223rr01. [DOI] [PubMed] [Google Scholar]
  31. Shedlock A. M., Parker J. D., Crispin D. A., Pietsch T. W., Burmer G. C. Evolution of the salmonid mitochondrial control region. Mol Phylogenet Evol. 1992 Sep;1(3):179–192. doi: 10.1016/1055-7903(92)90014-8. [DOI] [PubMed] [Google Scholar]
  32. Stewart D. T., Baker A. J. Patterns of sequence variation in the mitochondrial D-loop region of shrews. Mol Biol Evol. 1994 Jan;11(1):9–21. doi: 10.1093/oxfordjournals.molbev.a040096. [DOI] [PubMed] [Google Scholar]
  33. Templeton A. R., Boerwinkle E., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics. 1987 Oct;117(2):343–351. doi: 10.1093/genetics/117.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Templeton A. R., Crandall K. A., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics. 1992 Oct;132(2):619–633. doi: 10.1093/genetics/132.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Templeton A. R., Sing C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics. 1993 Jun;134(2):659–669. doi: 10.1093/genetics/134.2.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tracy R. L., Stern D. B. Mitochondrial transcription initiation: promoter structures and RNA polymerases. Curr Genet. 1995 Aug;28(3):205–216. doi: 10.1007/BF00309779. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Wilkinson G. S., Mayer F., Kerth G., Petri B. Evolution of repeated sequence arrays in the D-loop region of bat mitochondrial DNA. Genetics. 1997 Jul;146(3):1035–1048. doi: 10.1093/genetics/146.3.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES