Skip to main content
Log in

Directional mutation pressure, selective constraints, and genetic equilibria

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Rates of substitution mutations in two directions, v [from an A-T or T-A nucleotide pair (AT-pair) to a G-C or C-G nucleotide pair (GC-pair)] and u [from a GC-pair to an AT-pair], are usually not the same. The net effect, v/(u + v), has previously been defined as directional mutation pressure (μ d ), which explains the wide interspecific variation and narrow intragenomic heterogeneity of DNA G+C content in bacteria. In this article, first, a theory of the evolution of DNA G+C content is presented that is based on the equilibrium among three components: directional mutation pressure, DNA G+C content, and selective constraints. According to this theory, consideration of both u and v as well as selective constraints is essential to explain the molecular evolution of the DNA base composition and sequence. Second, the theory of directional mutation pressure is applied to the analysis of the wide intragenomic heterogeneity of DNA G+C content in multicellular eukaryotes. The theory explains the extensive intragenomic heterogeneity of G+C content of higher eukaryotes primarily as the result of the intragenomic differences of directional mutation pressure and selective constraints rather than the result of positive selections for functional advantages of the DNA G+C content itself.

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

  • Andachi Y, Yamao F, Muto A, Osawa S (1989) Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species in Mycoplasma capricolum: resemblance to mitochondria. J Mol Biol 209:37–54

    Google Scholar 

  • Belozersky AN, Spirin AS (1958) A correlation between the compositions of deoxyribonucleic and ribonucleic acids. Nature 182:111–112

    Google Scholar 

  • Bernardi G, Olfsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of the vertebrates. Science 228:953–958

    Google Scholar 

  • Brahim A, D'Onofrio G, Mouchiroud D, Gardiner K, Gautier C, Bernardi G (1991) The compositional properties of human genes. J Mol Evol 32:493–503

    Google Scholar 

  • Braun G, Cole ST (1984) DNA sequence analysis of the Serratia marcescens ompA gene: implications for the organization of an enterobacterial outer membrane protein. Mol Gen Genet 195:321–328

    Google Scholar 

  • Chen GT, Inouye M (1990) Suppression of the negative effect of minor arginine codons on gene expression; preferential usage of minor codons within the first 25 codons of the Escherichia coli genes. Nucleic Acids Res 18:1465–1473

    Google Scholar 

  • Cox EC, Yanofsky C (1967) Altered base ratios in the DNA of an Escherichia coli mutator strain. Proc Natl Acad Sci USA 58:1895–1902

    Google Scholar 

  • Crow JF (1958) Some possibilities for measuring selection intensities in man. Hum Biol 30:1–13

    Google Scholar 

  • D'Onofrio G, Mouchiroud D, Aissani B, Gautier C, Bernardi G (1991) Correlations between the compositional properties of human genes, codon usage and amino acid composition of proteins. J Mol Evol 32:504–510

    Google Scholar 

  • Filipski J (1987) Correlation between molecular clock ticking, codon usage, fidelity of DNA repair, chromosome banding and chromatin compactness in the germline cells. FEBS Lett 217:184–186

    Google Scholar 

  • Filipski J (1990) Evolution of DNA sequence: contributions of mutational bias and selection to the origin of chromosomal compartments. Adv Mutagen Res 2:1–54

    Google Scholar 

  • Freese E (1962) On the evolution of base composition of DNA. J Theor Biol 3:82–101

    Google Scholar 

  • Gasser SM, Laemmli UK (1987) A glimpse at chromosomal order. Trends Genet 3:16–22

    Google Scholar 

  • Grantham R, Gauter 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

    Google Scholar 

  • Graur D (1985) Amino acid composition and the evolutionary rates of protein-coding genes. J Mol Evol 22:53–62

    Google Scholar 

  • Grunstein M, Schedl P, Kedes L (1976) Sequence analysis and evolution of sea urchin (Lytechinus pictus and Strongylocentrotus purpuratus) histone H4 messenger RNAs. J Mol Biol 104:351–369

    Google Scholar 

  • Haldane JBS (1937) The effect of variation on fitness. Am Nat 71:337–349

    Google Scholar 

  • Hayashida H, Toh H, Kikuno R, Miyata T (1985) Evolution of influenza virus genes. Mol Biol Evol 2:289–303

    Google Scholar 

  • Hoekema A, Kastelein RA, Vasser M, de Boer HA (1987) Codon replacement in the PGKI gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression. Mol Cell Biol 7:2914–2924

    Google Scholar 

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

    Google Scholar 

  • Ikemura T, Ozeki H (1982) Codon usage and transfer RNA contents: organism-specific codon-choice patterns in reference to the isoacceptor contents. Cold Spring Harbor Symp Quant Biol 42:1087–1097

    Google Scholar 

  • Jukes TH (1965) Genetic code, II. Am Sci 53:477–487

    Google Scholar 

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

    Google Scholar 

  • Kafatos FC, Efstratiadis A, Forget BG, Weissman SM (1977) Molecular evolution of human and rabbit β-globin mRNAs. Proc Natl Acad Sci USA 74:5618–5622

    Google Scholar 

  • Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626

    Google Scholar 

  • Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • King JL, Jukes TH (1969) Non-Darwinian evolution. Science 164:788–798

    Google Scholar 

  • Lee KY, Wahl R, Barbu E (1956) Contenu en bases puriques et pyrimidiques des acids desoxyribonucleiques des batteries. Ann Inst Pasteur 91:212–224

    Google Scholar 

  • Li W-H, Wu C-I, Luo C-C (1985) Anew 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 

  • Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332

    Google Scholar 

  • Mouchiroud D, Grautier C, Bernardi G (1988) The compositional distribution of coding sequences and DNA molecules in humans and murids. J Mol Evol 27:311–320

    Google Scholar 

  • Muller HJ (1950) Our load of mutations. Am J Hum Genet 2:111–176

    Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169

    Google Scholar 

  • Nakamura K, Pirtle RM, Pirtle IL, Taseishi K, Inouye M (1980) Messenger ribonucleic acid of the lipoprotein of the Escherichia coli outer membrane. J Biol Chem 255:210–216

    Google Scholar 

  • Nomura M, Sor F, Yamagishi M, Lawson M (1987) Heterogeneity of GC content within a single bacterial genome and its implication for evolution. Cold Spring Harbor Symp Quant Biol 52:658–663

    Google Scholar 

  • Ohama T, Muto M, Osawa S (1990) Role of GC-biased mutation pressure on synonymous codon choice in Micrococus luteus, a bacterium with a high genomic GC-content. Nucleic Acids Res 18:1565–1569

    Google Scholar 

  • Ohno S (1988) Universal rule for coding sequence construction: TA/CG deficiency TG/CT excess. Proc Natl Acad Sci USA 85:9630–9634

    Google Scholar 

  • Osawa S, Ohama T, Yamao F, Muto A, Jukes TH, Ozeki H, Umesono K (1988) Directional mutation pressure and transfer RNA in choice of the third nucleotide of synonymous two codon sets. Proc Natl Acad Sci USA 85:1124–1128

    Google Scholar 

  • Post LE, Stycharz GD, Nomura M, Lewis H, Dennis PP (1979) Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit β in Escherichia coli. Proc Natl Acad Sci USA 76:1697–1701

    Google Scholar 

  • Rolfe R, Meselson M (1959) The relative homogeneity of microbial DNA. Proc Natl Acad Sci USA 45:1039–1043

    Google Scholar 

  • Sharp PM, Li WH (1989) On the rate of DNA sequence evolution in Drosophila. J Mol Evol 28:398–402

    Google Scholar 

  • Sueoka N (1959) A statistical analysis of deoxyribonucleic acid distribution in density gradient centrifugation. Proc Natl Acad Sci USA 45:1480–1490

    Google Scholar 

  • Sueoka N (1961) Compositional correlation between deoxyribonucleic acid and protein. Cold Spring Harbor Symp Quant Biol 26:35–43

    Google Scholar 

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

    Google Scholar 

  • Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657

    Google Scholar 

  • Sueoka N, Marmur J, Doty P (1959) Heterogeneity in deoxyribonucleic acids. II. Dependence of the density of deoxyribonucleic acids on guanine-cytosine. Nature 183:1427–1431

    Google Scholar 

  • Wada A, Suyama A (1986) Local stability of DNA and RNA secondary structure and its relation to biological functions. Prog Biophys Mol Biol 47:113–157

    Google Scholar 

  • Wada K, Aota S, Tsuchiya R, Ishibashi F, Gojobori T, Ikemura T (1990) Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res [Suppl] 18:2367–2411

    Google Scholar 

  • Wright S (1938) The distribution of gene frequencies under irreversible mutation. Proc Natl Acad Sci USA 24:253–259

    Google Scholar 

  • Yomo T, Ohno S (1989) Concordant evolution of coding and noncoding regions of DNA made possible by the universal rule of TA/CG deficiency-TG/CT excess. Proc Natl Acad Sci USA 86:8452–8456

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sueoka, N. Directional mutation pressure, selective constraints, and genetic equilibria. J Mol Evol 34, 95–114 (1992). https://doi.org/10.1007/BF00182387

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00182387

Key words

Navigation