Skip to main content
Log in

An Analytical Model of Gene Evolution with 9 Mutation Parameters: An Application to the Amino Acids Coded by the Common Circular Code

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

We develop here an analytical evolutionary model based on a trinucleotide mutation matrix 64× 64 with nine substitution parameters associated with the three types of substitutions in the three trinucleotide sites. It generalizes the previous models based on the nucleotide mutation matrices 4× 4 and the trinucleotide mutation matrix 64× 64 with three and six parameters. It determines at some time t the exact occurrence probabilities of trinucleotides mutating randomly according to these nine substitution parameters. An application of this model allows an evolutionary study of the common circular code \(\mathcal{C}\) of eukaryotes and prokaryotes and its 12 coded amino acids. The main property of this code \(\mathcal{C}\) is the retrieval of the reading frames in genes, both locally, i.e. anywhere in genes and in particular without a start codon, and automatically with a window of a few nucleotides. However, since its identification in 1996, amino acid information coded by \(\mathcal{C}\) has never been studied. Very unexpectedly, this evolutionary model demonstrates that random substitutions in this code \(\mathcal{C}\) and with particular values for the nine substitutions parameters retrieve after a certain time of evolution a frequency distribution of these 12 amino acids very close to the one coded by the actual genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akashi, H., Eyre-Walker, A., 1998. Translational selection and molecular evolution. Curr. Opin. Genet. Dev. 8, 688–693.

    Article  Google Scholar 

  • Antezana, M.A., Kreitman, M., 1999. The nonrandom location of synonymous codons suggests that reading frame-independent forces have patterned codon preferences. J. Mol. Evol. 49, 36–43.

    Article  Google Scholar 

  • Arquès, D.G., Fallot, J.-P., Michel, C.J., 1998. An evolutionary analytical model of a complementary circular code simulating the protein coding genes, the 5′ and 3′ regions. Bull. Math. Biol. 60, 163–194.

    Article  MATH  Google Scholar 

  • Arquès, D.G., Michel, C.J., 1996. A complementary circular code in the protein coding genes. J. Theor. Biol. 182, 45–58.

    Article  Google Scholar 

  • Béal, M.-P., 1993. Codage Symbolique. Masson, Paris.

    Google Scholar 

  • Berg, O.G., Silva, P.J.N., 1997. Codon bias in Escherichia coli: The influence of codon context on mutation and selection. Nucleic Acids Res. 25, 1397–1404.

    Article  Google Scholar 

  • Berstel, J., Perrin, D., 1985. Theory of Codes. Academic Press, New York.

    MATH  Google Scholar 

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

    Google Scholar 

  • Campbell, A., Mrázek, J., Karlin, S., 1999. Genomic signature comparisons among prokaryote, plasmid, and mitochondrial DNA. Proc. Natl. Acad. Sci. U.S.A. 96, 9184–9189.

    Article  Google Scholar 

  • Crick, F.H.C., Brenner, S., Klug, A., Pieczenik, G., 1976. A speculation on the origin of protein synthesis. Orig. Life 7, 389–397.

    Article  Google Scholar 

  • Crick, F.H.C., Griffith, J.S., Orgel, L.E., 1957. Codes without commas. Proc. Natl. Acad. Sci. 43, 416–421.

    Article  Google Scholar 

  • Fedorov, A., Saxonov, S., Gilbert, W., 2002. Regularities of context-dependent codon bias in eukaryotic genes. Nucleic Acids Res. 30, 1192–1197.

    Article  Google Scholar 

  • Grantham, R., Gautier, C., Gouy, M., Mercier, R., Pave, A., 1980. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 8, r49–r62.

    Google Scholar 

  • Grantham, R., Gautier, C., Gouy, M., Jacobzone, M., Mercier, R., 1981. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 9, r43–r74.

    Article  Google Scholar 

  • Eigen, M., Schuster, P., 1978. The hypercycle. A principle of natural self-organization. Part C: The realistic hypercycle. Naturwissenschaften 65, 341–369.

    Article  Google Scholar 

  • Ermolaeva, M.D., 2001. Synonymous codon usage in bacteria. Curr. Issues Mol. Biol. Oct. 3, 91–97.

    Google Scholar 

  • Frey, G., Michel, C.J., 2006. An analytical model of gene evolution with 6 mutation parameters: An application to archaeal circular codes. J. Comput. Biol. Chem. 30, 1–11.

    Article  MATH  Google Scholar 

  • Ikemura, T., 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2, 12–34.

    Google Scholar 

  • Jukes, T.H., Bhushan, V., 1986. Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J. Mol. Evol. 24, 39–44.

    Article  Google Scholar 

  • Jukes, T.H., Cantor, C.R., 1969. Evolution of protein molecules. In: Munro, H.N. (Ed.), Mammalian Protein Metabolism. Academic Press, New York, 21–132.

    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.

    Article  Google Scholar 

  • Koch, A.J., Lehmann, J., 1997. About a symmetry of the genetic code. J. Theor. Biol. 189, 171–174.

    Article  Google Scholar 

  • Konu, O., Li, M.D., 2002. Correlations between mRNA expression levels and GC contents of coding and untranslated regions of genes in rodents. J. Mol. Evol. 54, 35–41.

    Article  Google Scholar 

  • Krakauer, D.C., Jansen, A.A., 2002. Red Queen Dynamics of protein Translation. J. Theor. Biol. 218, 97–109.

    Article  Google Scholar 

  • Lacan, J., Michel, C.J., 2001. Analysis of a circular code model. J. Theor. Biol. 213, 159–170.

    Article  Google Scholar 

  • Lange, K., 2005. Applied Probability, Springer-Verlag, New York.

    Google Scholar 

  • Llopart, A., Aguade, M., 2000. Nucleotide polymorphism at the RpII215 gene in Drosophila subobscura: Weak selection on synonymous mutations. Genetics 155, 1245–1252.

    Google Scholar 

  • Nirenberg, M.W., Matthaei, J.H., 1961. The dependance of cell-free protein synthesis in E. coli upon naturally occurring or synthetic polyribonucleotides. Proc. Natl. Acad. Sci. 47, 1588–1602.

    Article  Google Scholar 

  • Ochman, H., 2003. Neutral mutations and neutral substitutions in bacterial genomes. Mol. Biol. Evol. 20, 2091–2096.

    Article  Google Scholar 

  • Rogozin, I.B., Malyarchuk, B.A., Pavlov, Y.I., Milanesi, L., 2005. From context-dependance of mutations to molecular mechanisms of mutagenesis. Pac Symp. Biocomput., 409–420.

  • Rosenberg, M.S., Subramanian, S., Kumar, S., 2003. Patterns of transitional mutation biases within and among mammalian genomes. Mol. Biol. Evol. 20, 988–993.

    Article  Google Scholar 

  • Sharp, P.M., Bailes, E., Grocock, R.J., Peden, J.F., Sockett, R.E., 2005. Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res. 33, 1141–1153.

    Article  Google Scholar 

  • Sharp, P.M., Matassi, G., 1994. Codon usage and genome evolution. Curr. Opin. Genet. Dev. 4, 851–860.

    Article  Google Scholar 

  • Shpaer, E.G., 1986. Constraints on codon context in Escherichia coli genes. Their possible role in modulating the efficiency of translation. J. Mol. Biol. 188, 555–564.

    Article  Google Scholar 

  • Smith, N.G.C., Eyre-Walker, A., 2001. Synonymous codon bias is not caused by mutation bias in G+C-rich genes in humans. Mol. Biol. Evol. 18, 982–986.

    Google Scholar 

  • Yarus, M., Folley, L.S., 1984. Sense codons are found in specific contexts. J. Mol. Biol. 182, 529–540.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian J. Michel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Michel, C.J. An Analytical Model of Gene Evolution with 9 Mutation Parameters: An Application to the Amino Acids Coded by the Common Circular Code. Bull. Math. Biol. 69, 677–698 (2007). https://doi.org/10.1007/s11538-006-9147-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-006-9147-z

Keywords

Navigation