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. 1991 Jun;128(2):269–279. doi: 10.1093/genetics/128.2.269

Mode and Tempo of Molecular Evolution in the Nematode Caenorhabditis: Cytochrome Oxidase II and Calmodulin Sequences

W K Thomas 1, A C Wilson 1
PMCID: PMC1204465  PMID: 1649066

Abstract

Through direct sequencing methods, the mitochondrial gene for cytochrome oxidase subunit two (CO II) and the single-copy nuclear gene for calmodulin were compared among strains of Caenorhabditis elegans and two other Caenorhabditis species (C. remanei and C. briggsae). In addition the CO II sequence was determined from a distantly related nematode, Steinernema intermedii. Among the 11 strains of C. elegans tested, there are four types of CO II gene, arising from two major lineages. Levels of intraspecific difference in the CO II gene are low (<2.0%) compared to the extraordinary divergence between congeneric species, which is about 50% when corrected for multiple hits. Concordant with the increase in divergence between taxa is a change in the pattern of substitution from a strong transition bias (24 transitions compared to two transversions) within species to a substitution pattern that appears to reflect the base composition of the mitochondrial genome when more divergent nematodes are compared. The base composition of the Caenorhabditis CO II gene is strongly biased toward A + T at all three positions of codons and appears to constrain the amino acid composition of the protein. Both the CO II and calmodulin genes show extreme conservation of amino acid sequences. When the accumulation of changes at silent sites in the two genes is compared among strains, it becomes evident that the mitochondrial gene is changing faster than the nuclear gene.

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Selected References

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  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. Bisson R., Steffens G. C., Buse G. Localization of lipid binding domain(s) on subunit II of beef heart cytochrome c oxidase. J Biol Chem. 1982 Jun 25;257(12):6716–6720. [PubMed] [Google Scholar]
  3. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown G. G., Simpson M. V. Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci U S A. 1982 May;79(10):3246–3250. doi: 10.1073/pnas.79.10.3246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. Butler M. H., Wall S. M., Luehrsen K. R., Fox G. E., Hecht R. M. Molecular relationships between closely related strains and species of nematodes. J Mol Evol. 1981;18(1):18–23. doi: 10.1007/BF01733207. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Cantatore P., Saccone C. Organization, structure, and evolution of mammalian mitochondrial genes. Int Rev Cytol. 1987;108:149–208. doi: 10.1016/s0074-7696(08)61438-2. [DOI] [PubMed] [Google Scholar]
  10. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  11. Crozier R. H., Crozier Y. C., Mackinlay A. G. The CO-I and CO-II region of honeybee mitochondrial DNA: evidence for variation in insect mitochondrial evolutionary rates. Mol Biol Evol. 1989 Jul;6(4):399–411. doi: 10.1093/oxfordjournals.molbev.a040553. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Edwards S. V., Wilson A. C. Phylogenetically informative length polymorphism and sequence variability in mitochondrial DNA of Australian songbirds (Pomatostomus). Genetics. 1990 Nov;126(3):695–711. doi: 10.1093/genetics/126.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Garey J. R., Wolstenholme D. R. Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNA(serAGN) that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. J Mol Evol. 1989 May;28(5):374–387. doi: 10.1007/BF02603072. [DOI] [PubMed] [Google Scholar]
  15. Gyllensten U. B., Erlich H. A. Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7652–7656. doi: 10.1073/pnas.85.20.7652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heschl M. F., Baillie D. L. Functional elements and domains inferred from sequence comparisons of a heat shock gene in two nematodes. J Mol Evol. 1990 Jul;31(1):3–9. doi: 10.1007/BF02101786. [DOI] [PubMed] [Google Scholar]
  17. Higuchi R., Bowman B., Freiberger M., Ryder O. A., Wilson A. C. DNA sequences from the quagga, an extinct member of the horse family. Nature. 1984 Nov 15;312(5991):282–284. doi: 10.1038/312282a0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Millett F., de Jong C., Paulson L., Capaldi R. A. Identification of specific carboxylate groups on cytochrome c oxidase that are involved in binding cytochrome c. Biochemistry. 1983 Feb 1;22(3):546–552. doi: 10.1021/bi00272a004. [DOI] [PubMed] [Google Scholar]
  21. Powell J. R., Caccone A., Amato G. D., Yoon C. Rates of nucleotide substitution in Drosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9090–9093. doi: 10.1073/pnas.83.23.9090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Schaaper R. M., Dunn R. L. Spectra of spontaneous mutations in Escherichia coli strains defective in mismatch correction: the nature of in vivo DNA replication errors. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6220–6224. doi: 10.1073/pnas.84.17.6220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sharp P. M., Li W. H. The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol. 1987 May;4(3):222–230. doi: 10.1093/oxfordjournals.molbev.a040443. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Thomas W. K., Maa J., Wilson A. C. Shifting constraints on tRNA genes during mitochondrial DNA evolution in animals. New Biol. 1989 Oct;1(1):93–100. [PubMed] [Google Scholar]
  27. Thomas W. K., Päbo S., Villablanca F. X., Wilson A. C. Spatial and temporal continuity of kangaroo rat populations shown by sequencing mitochondrial DNA from museum specimens. J Mol Evol. 1990 Aug;31(2):101–112. doi: 10.1007/BF02109479. [DOI] [PubMed] [Google Scholar]
  28. Vawter L., Brown W. M. Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science. 1986 Oct 10;234(4773):194–196. doi: 10.1126/science.3018931. [DOI] [PubMed] [Google Scholar]
  29. Wolstenholme D. R., Clary D. O. Sequence evolution of Drosophila mitochondrial DNA. Genetics. 1985 Apr;109(4):725–744. doi: 10.1093/genetics/109.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wolstenholme D. R., Macfarlane J. L., Okimoto R., Clary D. O., Wahleithner J. A. Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1324–1328. doi: 10.1073/pnas.84.5.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]

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