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Synonymous substitution-rate constants in Escherichia coli and Salmonella typhimurium and their relationship to gene expression and selection pressure

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Abstract

Based on the differences in synonymous codon use between E. coli and S. typhimurium, the synonymous substitution rates can be estimated. In contrast to previous studies on the substitution rates in these two organisms, we use a kinetic model that explicitly takes the selection bias into account. The selection pressure on synonymous codons for a particular amino acid can be calculated from the observed codon bias. This offers a unique opportunity to study systematically the relationship between substitution-rate constants and selection pressure. The results indicate that the codon bias in these organisms is determined by a mutation-selection balance rather than by stabilizing selection. A best fit to the data implies that the mutation rate constant increases about threefold in genes at low expression levels relative to those that are highly expressed.

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References

  • Berg OG (1992) The evolutionary selection of DNA base pairs in gene-regulatory binding sites. Proc Natl Acad Sci U S A 89:7501–7505

    Google Scholar 

  • Berg OG (1995a) Kinetics of synonymous codon change for an amino acid of arbitrary degeneracy. J Mol Evol (in press)

  • Berg OG (1995b) Periodic selection and hitchhiking in a bacterial population. J Theor Biol (in press)

  • Bulmer M (1987) Coevolution of codon usage and transfer RNA abundance. Nature 325:728–730

    Google Scholar 

  • Bulmer M (1988a) Codon usage and intragenic position. J Theor Biol 133:67–71

    Google Scholar 

  • Bulmer M (1988b) Are codon usage patterns in unicellular organisms determined by selection mutation balance? J Evol Biol 1:15–26

    Google Scholar 

  • Bulmer M (1990) The effect of context on synonymous codon usage in genes with low codon usage bias. Nucleic Acids Res 18:2869–2873

    Google Scholar 

  • Bulmer M (1991) The selection-mutation drift theory of synonymous codon usage. Genetics 129:897–907

    Google Scholar 

  • Ehrenberg M, Kurland CG (1984) Costs of accuracy determined by a maximal growth rate constant. Q Rev Biophys 17:45–82

    Google Scholar 

  • Emilsson V, Kurland CG (1990) Growth rate dependence of transfer RNA abundance in Escherichia coli. EMBO 19:4359–4366

    Google Scholar 

  • Emilsson V, Näslund AK, Kurland CG (1993) Growth-rate dependent accumulation of twelve tRNA species in Escherichia coli. J Mol Biol 230:483–491

    Google Scholar 

  • Eyre-Walker A, Bulmer M (1993) Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res 21: 4599–4603

    Google Scholar 

  • Ikemura T (1981) Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 146:1–21

    Google Scholar 

  • Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Google Scholar 

  • Kimura M (1981) Possibility of extensive neutral evolution under stabilizing selection with special reference to nonrandom usage of synonymous codons. Proc Natl Acad Sci USA 78:5773–5777

    Google Scholar 

  • Kimura M (1983) The neutral theory of evolution. Cambridge University Press, Cambridge, pp 183–193

    Google Scholar 

  • Li WH, Wu CI, Luo CC (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174

    Google Scholar 

  • Li WH, Graur D (1991) Fundamentals of molecular evolution. Sinauer Associated, Sunderland, MA p 32

    Google Scholar 

  • Ochman H, Wilson AC (1987) Evolutionary history of enteric bacteria. In: Neidhardt FC (ed) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. ASM Press, Washington, DC, p 1649

    Google Scholar 

  • Selby CP, Sancar A (1993) Transcription-repair coupling and mutation frequency decline. J Bacteriol 175:7509–7514

    Google Scholar 

  • Sharp PM (1991) Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J Mol Evol 33:23–33

    Google Scholar 

  • Sharp PM, Li WH (1987) The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4:222–230

    Google Scholar 

  • Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592

    Google Scholar 

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Correspondence to: O.G. Berg

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Berg, O.G., Martelius, M. Synonymous substitution-rate constants in Escherichia coli and Salmonella typhimurium and their relationship to gene expression and selection pressure. J Mol Evol 41, 449–456 (1995). https://doi.org/10.1007/BF00160316

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  • DOI: https://doi.org/10.1007/BF00160316

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