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. 1994 Jul 11;22(13):2437–2446. doi: 10.1093/nar/22.13.2437

Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases.

M Stenico 1, A T Lloyd 1, P M Sharp 1
PMCID: PMC308193  PMID: 8041603

Abstract

Synonymous codon usage varies considerably among Caenorhabditis elegans genes. Multivariate statistical analyses reveal a single major trend among genes. At one end of the trend lie genes with relatively unbiased codon usage. These genes appear to be lowly expressed, and their patterns of codon usage are consistent with mutational biases influenced by the neighbouring nucleotide. At the other extreme lie genes with extremely biased codon usage. These genes appear to be highly expressed, and their codon usage seems to have been shaped by selection favouring a limited number of translationally optimal codons. Thus, the frequency of these optimal codons in a gene appears to be correlated with the level of gene expression, and may be a useful indicator in the case of genes (or open reading frames) whose expression levels (or even function) are unknown. A second, relatively minor trend among genes is correlated with the frequency of G at synonymously variable sites. It is not yet clear whether this trend reflects variation in base composition (or mutational biases) among regions of the C.elegans genome, or some other factor. Sequence divergence between C.elegans and C.briggsae has also been studied.

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Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Aota S., Gojobori T., Ishibashi F., Maruyama T., Ikemura T. Codon usage tabulated from the GenBank Genetic Sequence Data. Nucleic Acids Res. 1988;16 (Suppl):r315–r402. doi: 10.1093/nar/16.suppl.r315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aota S., Ikemura T. Diversity in G + C content at the third position of codons in vertebrate genes and its cause. Nucleic Acids Res. 1986 Aug 26;14(16):6345–6355. doi: 10.1093/nar/14.16.6345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernardi G., Olofsson B., Filipski J., Zerial M., Salinas J., Cuny G., Meunier-Rotival M., Rodier F. The mosaic genome of warm-blooded vertebrates. Science. 1985 May 24;228(4702):953–958. doi: 10.1126/science.4001930. [DOI] [PubMed] [Google Scholar]
  5. Bernardi G. The isochore organization of the human genome. Annu Rev Genet. 1989;23:637–661. doi: 10.1146/annurev.ge.23.120189.003225. [DOI] [PubMed] [Google Scholar]
  6. Bulmer M. Neighboring base effects on substitution rates in pseudogenes. Mol Biol Evol. 1986 Jul;3(4):322–329. doi: 10.1093/oxfordjournals.molbev.a040401. [DOI] [PubMed] [Google Scholar]
  7. Bulmer M. The effect of context on synonymous codon usage in genes with low codon usage bias. Nucleic Acids Res. 1990 May 25;18(10):2869–2873. doi: 10.1093/nar/18.10.2869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics. 1991 Nov;129(3):897–907. doi: 10.1093/genetics/129.3.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. D'Onofrio G., Bernardi G. A universal compositional correlation among codon positions. Gene. 1992 Jan 2;110(1):81–88. doi: 10.1016/0378-1119(92)90447-w. [DOI] [PubMed] [Google Scholar]
  10. Eyre-Walker A. C. An analysis of codon usage in mammals: selection or mutation bias? J Mol Evol. 1991 Nov;33(5):442–449. doi: 10.1007/BF02103136. [DOI] [PubMed] [Google Scholar]
  11. Gouy M., Gautier C., Attimonelli M., Lanave C., di Paola G. ACNUC--a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. Comput Appl Biosci. 1985 Sep;1(3):167–172. doi: 10.1093/bioinformatics/1.3.167. [DOI] [PubMed] [Google Scholar]
  12. Gouy M., Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 1982 Nov 25;10(22):7055–7074. doi: 10.1093/nar/10.22.7055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 1981 Jan 10;9(1):r43–r74. doi: 10.1093/nar/9.1.213-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Holm L. Codon usage and gene expression. Nucleic Acids Res. 1986 Apr 11;14(7):3075–3087. doi: 10.1093/nar/14.7.3075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Huang X. Y., Barrios L. A., Vonkhorporn P., Honda S., Albertson D. G., Hecht R. M. Genomic organization of the glyceraldehyde-3-phosphate dehydrogenase gene family of Caenorhabditis elegans. J Mol Biol. 1989 Apr 5;206(3):411–424. doi: 10.1016/0022-2836(89)90490-7. [DOI] [PubMed] [Google Scholar]
  16. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985 Jan;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335. [DOI] [PubMed] [Google Scholar]
  17. Ikemura T., Wada K., Aota S. Giant G+C% mosaic structures of the human genome found by arrangement of GenBank human DNA sequences according to genetic positions. Genomics. 1990 Oct;8(2):207–216. doi: 10.1016/0888-7543(90)90273-w. [DOI] [PubMed] [Google Scholar]
  18. Kennedy B. P., Aamodt E. J., Allen F. L., Chung M. A., Heschl M. F., McGhee J. D. The gut esterase gene (ges-1) from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J Mol Biol. 1993 Feb 20;229(4):890–908. doi: 10.1006/jmbi.1993.1094. [DOI] [PubMed] [Google Scholar]
  19. Kramer J. M., Cox G. N., Hirsh D. Expression of the Caenorhabditis elegans collagen genes col-1 and col-2 is developmentally regulated. J Biol Chem. 1985 Feb 10;260(3):1945–1951. [PubMed] [Google Scholar]
  20. Lee Y. H., Huang X. Y., Hirsh D., Fox G. E., Hecht R. M. Conservation of gene organization and trans-splicing in the glyceraldehyde-3-phosphate dehydrogenase-encoding genes of Caenorhabditis briggsae. Gene. 1992 Nov 16;121(2):227–235. doi: 10.1016/0378-1119(92)90126-a. [DOI] [PubMed] [Google Scholar]
  21. Li W. H. Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J Mol Evol. 1987;24(4):337–345. doi: 10.1007/BF02134132. [DOI] [PubMed] [Google Scholar]
  22. Li W. H., Tanimura M., Sharp P. M. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol. 1987;25(4):330–342. doi: 10.1007/BF02603118. [DOI] [PubMed] [Google Scholar]
  23. Li W. H. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol. 1993 Jan;36(1):96–99. doi: 10.1007/BF02407308. [DOI] [PubMed] [Google Scholar]
  24. Lloyd A. T., Sharp P. M. CODONS: a microcomputer program for codon usage analysis. J Hered. 1992 May-Jun;83(3):239–240. doi: 10.1093/oxfordjournals.jhered.a111205. [DOI] [PubMed] [Google Scholar]
  25. Marín A., Bertranpetit J., Oliver J. L., Medina J. R. Variation in G + C-content and codon choice: differences among synonymous codon groups in vertebrate genes. Nucleic Acids Res. 1989 Aug 11;17(15):6181–6189. doi: 10.1093/nar/17.15.6181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miller D. M., 3rd, Ortiz I., Berliner G. C., Epstein H. F. Differential localization of two myosins within nematode thick filaments. Cell. 1983 Sep;34(2):477–490. doi: 10.1016/0092-8674(83)90381-1. [DOI] [PubMed] [Google Scholar]
  27. Oliver S. G., van der Aart Q. J., Agostoni-Carbone M. L., Aigle M., Alberghina L., Alexandraki D., Antoine G., Anwar R., Ballesta J. P., Benit P. The complete DNA sequence of yeast chromosome III. Nature. 1992 May 7;357(6373):38–46. doi: 10.1038/357038a0. [DOI] [PubMed] [Google Scholar]
  28. Sharp P. M., Cowe E., Higgins D. G., Shields D. C., Wolfe K. H., Wright F. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res. 1988 Sep 12;16(17):8207–8211. doi: 10.1093/nar/16.17.8207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sharp P. M., Cowe E. Synonymous codon usage in Saccharomyces cerevisiae. Yeast. 1991 Oct;7(7):657–678. doi: 10.1002/yea.320070702. [DOI] [PubMed] [Google Scholar]
  30. Sharp P. M., Li W. H. On the rate of DNA sequence evolution in Drosophila. J Mol Evol. 1989 May;28(5):398–402. doi: 10.1007/BF02603075. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Sharp P. M., Lloyd A. T. Regional base composition variation along yeast chromosome III: evolution of chromosome primary structure. Nucleic Acids Res. 1993 Jan 25;21(2):179–183. doi: 10.1093/nar/21.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sharp P. M., Stenico M., Peden J. F., Lloyd A. T. Codon usage: mutational bias, translational selection, or both? Biochem Soc Trans. 1993 Nov;21(4):835–841. doi: 10.1042/bst0210835. [DOI] [PubMed] [Google Scholar]
  34. Shields D. C., Sharp P. M., Higgins D. G., Wright F. "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol. 1988 Nov;5(6):704–716. doi: 10.1093/oxfordjournals.molbev.a040525. [DOI] [PubMed] [Google Scholar]
  35. Shields D. C., Sharp P. M. Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Res. 1987 Oct 12;15(19):8023–8040. doi: 10.1093/nar/15.19.8023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Snutch T. P., Heschl M. F., Baillie D. L. The Caenorhabditis elegans hsp70 gene family: a molecular genetic characterization. Gene. 1988 Apr 29;64(2):241–255. doi: 10.1016/0378-1119(88)90339-3. [DOI] [PubMed] [Google Scholar]
  37. Spieth J., Nettleton M., Zucker-Aprison E., Lea K., Blumenthal T. Vitellogenin motifs conserved in nematodes and vertebrates. J Mol Evol. 1991 May;32(5):429–438. doi: 10.1007/BF02101283. [DOI] [PubMed] [Google Scholar]
  38. Sueoka N. Directional mutation pressure, selective constraints, and genetic equilibria. J Mol Evol. 1992 Feb;34(2):95–114. doi: 10.1007/BF00182387. [DOI] [PubMed] [Google Scholar]
  39. Sulston J., Du Z., Thomas K., Wilson R., Hillier L., Staden R., Halloran N., Green P., Thierry-Mieg J., Qiu L. The C. elegans genome sequencing project: a beginning. Nature. 1992 Mar 5;356(6364):37–41. doi: 10.1038/356037a0. [DOI] [PubMed] [Google Scholar]
  40. Thomas W. K., Wilson A. C. Mode and tempo of molecular evolution in the nematode caenorhabditis: cytochrome oxidase II and calmodulin sequences. Genetics. 1991 Jun;128(2):269–279. doi: 10.1093/genetics/128.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. doi: 10.1038/368032a0. [DOI] [PubMed] [Google Scholar]
  42. Wright F. The 'effective number of codons' used in a gene. Gene. 1990 Mar 1;87(1):23–29. doi: 10.1016/0378-1119(90)90491-9. [DOI] [PubMed] [Google Scholar]

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