Abstract
It has been shown previously that the synonymous substitution rate between Escherichia coli and Salmonella typhimurium is lower in highly than in weakly expressed genes, and it has been suggested that this is due to stronger selection for translational efficiency in highly expressed genes as reflected in their greater codon usage bias. This hypothesis is tested here by comparing the substitution rate in codon families with different patterns of synonymous codon use. It is shown that the decline in the substitution rate across expression levels is as great for codon families that do not appear to be subject to selection for translational efficiency as for those that are. This implies that selection on translational efficiency is not responsible for the decline in the substitution rate across genes. It is argued that the most likely explanation for this decline is a decrease in the mutation rate. It is also shown that a simple evolutionary model in which synonymous codon use is determined by a balance between mutation, selection for an optimal codon, and genetic drift predicts that selection should have little effect on the substitution rate in the present case.
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Selected References
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- Akashi H. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics. 1995 Feb;139(2):1067–1076. doi: 10.1093/genetics/139.2.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Bulmer M., Wolfe K. H., Sharp P. M. Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):5974–5978. doi: 10.1073/pnas.88.14.5974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drake J. W. A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160–7164. doi: 10.1073/pnas.88.16.7160. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eyre-Walker A., Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 1993 Sep 25;21(19):4599–4603. doi: 10.1093/nar/21.19.4599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eyre-Walker A. DNA mismatch repair and synonymous codon evolution in mammals. Mol Biol Evol. 1994 Jan;11(1):88–98. doi: 10.1093/oxfordjournals.molbev.a040095. [DOI] [PubMed] [Google Scholar]
- Friedberg E. C., Bardwell A. J., Bardwell L., Wang Z., Dianov G. Transcription and nucleotide excision repair--reflections, considerations and recent biochemical insights. Mutat Res. 1994 May 1;307(1):5–14. doi: 10.1016/0027-5107(94)90272-0. [DOI] [PubMed] [Google Scholar]
- Gutiérrez G., Casadesús J., Oliver J. L., Marín A. Compositional heterogeneity of the Escherichia coli genome: a role for VSP repair? J Mol Evol. 1994 Oct;39(4):340–346. doi: 10.1007/BF00160266. [DOI] [PubMed] [Google Scholar]
- Hartl D. L., Moriyama E. N., Sawyer S. A. Selection intensity for codon bias. Genetics. 1994 Sep;138(1):227–234. doi: 10.1093/genetics/138.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hori H., Osawa S. Evolution of ribosomal proteins in Enterobacteriaceae. J Bacteriol. 1978 Mar;133(3):1089–1095. doi: 10.1128/jb.133.3.1089-1095.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Jiang X. M., Neal B., Santiago F., Lee S. J., Romana L. K., Reeves P. R. Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2). Mol Microbiol. 1991 Mar;5(3):695–713. doi: 10.1111/j.1365-2958.1991.tb00741.x. [DOI] [PubMed] [Google Scholar]
- Sharp P. M., Li W. H. An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol. 1986;24(1-2):28–38. doi: 10.1007/BF02099948. [DOI] [PubMed] [Google Scholar]
- Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984 Apr;1(3):269–285. doi: 10.1093/oxfordjournals.molbev.a040317. [DOI] [PubMed] [Google Scholar]
- Wang L., Romana L. K., Reeves P. R. Molecular analysis of a Salmonella enterica group E1 rfb gene cluster: O antigen and the genetic basis of the major polymorphism. Genetics. 1992 Mar;130(3):429–443. doi: 10.1093/genetics/130.3.429. [DOI] [PMC free article] [PubMed] [Google Scholar]