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. 1996 Feb;142(2):525–535. doi: 10.1093/genetics/142.2.525

Length Variation, Heteroplasmy and Sequence Divergence in the Mitochondrial DNA of Four Species of Sturgeon (Acipenser)

J R Brown 1, K Beckenbach 1, A T Beckenbach 1, M J Smith 1
PMCID: PMC1206985  PMID: 8852850

Abstract

The extent of mtDNA length variation and heteroplasmy as well as DNA sequences of the control region and two tRNA genes were determined for four North American sturgeon species: Acipenser transmontanus, A. medirostris, A. fulvescens and A. oxyrhnychus. Across the Continental Divide, a division in the occurrence of length variation and heteroplasmy was observed that was concordant with species biogeography as well as with phylogenies inferred from restriction fragment length polymorphisms (RFLP) of whole mtDNA and pairwise comparisons of unique sequences of the control region. In all species, mtDNA length variation was due to repeated arrays of 78-82-bp sequences each containing a D-loop strand synthesis termination associated sequence (TAS). Individual repeats showed greater sequence conservation within individuals and species rather than between species, which is suggestive of concerted evolution. Differences in the frequencies of multiple copy genomes and heteroplasmy among the four species may be ascribed to differences in the rates of recurrent mutation. A mechanism that may offset the high rate of mutation for increased copy number is suggested on the basis that an increase in the number of functional TAS motifs might reduce the frequency of successfully initiated H-strand replications.

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Selected References

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  1. Aquadro C. F., Greenberg B. D. Human mitochondrial DNA variation and evolution: analysis of nucleotide sequences from seven individuals. Genetics. 1983 Feb;103(2):287–312. doi: 10.1093/genetics/103.2.287. [DOI] [PMC free article] [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. Avise J. C., Bowen B. W., Lamb T., Meylan A. B., Bermingham E. Mitochondrial DNA evolution at a turtle's pace: evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol Biol Evol. 1992 May;9(3):457–473. doi: 10.1093/oxfordjournals.molbev.a040735. [DOI] [PubMed] [Google Scholar]
  4. Birky C. W., Jr, Fuerst P., Maruyama T. Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics. 1989 Mar;121(3):613–627. doi: 10.1093/genetics/121.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bogenhagen D., Clayton D. A. Mechanism of mitochondrial DNA replication in mouse L-cells: kinetics of synthesis and turnover of the initiation sequence. J Mol Biol. 1978 Feb 15;119(1):49–68. doi: 10.1016/0022-2836(78)90269-3. [DOI] [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., Gilbert T. L., Kowbel D. J., O'Hara P. J., Buroker N. E., Beckenbach A. T., Smith M. J. Nucleotide sequence of the apocytochrome B gene in white sturgeon mitochondrial DNA. Nucleic Acids Res. 1989 Jun 12;17(11):4389–4389. doi: 10.1093/nar/17.11.4389. [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. 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]
  10. 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]
  11. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  12. Gilbert T. L., Brown J. R., O'Hara P. J., Buroker N. E., Beckenbach A. T., Smith M. J. Sequence of tRNA(Thr) and tRNA(Pro) from white sturgeon (Acipenser transmontanus) mitochondria. Nucleic Acids Res. 1988 Dec 23;16(24):11825–11825. doi: 10.1093/nar/16.24.11825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hale L. R., Singh R. S. Extensive variation and heteroplasmy in size of mitochondrial DNA among geographic populations of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8813–8817. doi: 10.1073/pnas.83.22.8813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hauswirth W. W., Laipis P. J. Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4686–4690. doi: 10.1073/pnas.79.15.4686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  16. Koehler C. M., Lindberg G. L., Brown D. R., Beitz D. C., Freeman A. E., Mayfield J. E., Myers A. M. Replacement of bovine mitochondrial DNA by a sequence variant within one generation. Genetics. 1991 Sep;129(1):247–255. doi: 10.1093/genetics/129.1.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Laskey R. A. The use of intensifying screens or organic scintillators for visualizing radioactive molecules resolved by gel electrophoresis. Methods Enzymol. 1980;65(1):363–371. doi: 10.1016/s0076-6879(80)65047-2. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Martin A. P., Naylor G. J., Palumbi S. R. Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature. 1992 May 14;357(6374):153–155. doi: 10.1038/357153a0. [DOI] [PubMed] [Google Scholar]
  21. Martin A. P., Palumbi S. R. Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4087–4091. doi: 10.1073/pnas.90.9.4087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  23. Nei M., Stephens J. C., Saitou N. Methods for computing the standard errors of branching points in an evolutionary tree and their application to molecular data from humans and apes. Mol Biol Evol. 1985 Jan;2(1):66–85. doi: 10.1093/oxfordjournals.molbev.a040333. [DOI] [PubMed] [Google Scholar]
  24. Nei M., Tajima F. Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics. 1983 Sep;105(1):207–217. doi: 10.1093/genetics/105.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rand D. M. Endotherms, ectotherms, and mitochondrial genome-size variation. J Mol Evol. 1993 Sep;37(3):281–295. doi: 10.1007/BF00175505. [DOI] [PubMed] [Google Scholar]
  26. Rand D. M., Harrison R. G. Mitochondrial DNA transmission genetics in crickets. Genetics. 1986 Nov;114(3):955–970. doi: 10.1093/genetics/114.3.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Roff D. A., Bentzen P. The statistical analysis of mitochondrial DNA polymorphisms: chi 2 and the problem of small samples. Mol Biol Evol. 1989 Sep;6(5):539–545. doi: 10.1093/oxfordjournals.molbev.a040568. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Vigilant L., Pennington R., Harpending H., Kocher T. D., Wilson A. C. Mitochondrial DNA sequences in single hairs from a southern African population. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9350–9354. doi: 10.1073/pnas.86.23.9350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. White W. H. Further Observations on the Histology and Function of the Mammalian Sympathetic Ganglia. J Physiol. 1889 Jul;10(5):341–357. doi: 10.1113/jphysiol.1889.sp000307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Yang Y. J., Lin Y. S., Wu J. L., Hui C. F. Variation in mitochondrial DNA and population structure of the Taipei treefrog Rhacophorus taipeianus in Taiwan. Mol Ecol. 1994 Jun;3(3):219–228. doi: 10.1111/j.1365-294x.1994.tb00055.x. [DOI] [PubMed] [Google Scholar]

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