Advertisement

Journal of Molecular Evolution

, Volume 37, Issue 4, pp 441–456 | Cite as

Mammalian gene evolution: Nucleotide sequence divergence between mouse and rat

  • Kenneth H. Wolfe
  • Paul M. Sharp
Article

Abstract

As a paradigm of mammalian gene evolution, the nature and extent of DNA sequence divergence between homologous protein-coding genes from mouse and rat have been investigated. The data set examined includes 363 genes totalling 411 kilobases, making this by far the largest comparison conducted between a single pair of species. Mouse and rat genes are on average 93.4% identical in nucleotide sequence and 93.9% identical in amino acid sequence. Individual genes vary substantially in the extent of nonsynonymous nucleotide substitution, as expected from protein evolution studies; here the variation is characterized. The extent of synonymous (or silent) substitution also varies considerably among genes, though the coefficient of variation is about four times smaller than for nonsynonymous substitutions. A small number of genes mapped to the X-chromosome have a slower rate of molecular evolution than average, as predicted if molecular evolution is “male-driven.” Base composition at silent sites varies from 33% to 95% G + C in different genes; mouse and rat homologues differ on average by only 1.7% in silent-site G + C, but it is shown that this is not necessarily due to any selective constraint on their base composition. Synonymous substitution rates and silent site base composition appear to be related (genes at intermediate G + C have on average higher rates), but the relationship is not as strong as in our earlier analyses. Rates of synonymous and nonsynonymous substitution are correlated, apparently because of an excess of substitutions involving adjacent pairs of nucleotides. Several factors suggest that synonymous codon usage in rodent genes is not subject to selection.

Key words

Molecular clocks Rodents Genome evolution G + C content Codon usage Dinucleotide mutation effects 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alonso S, Minty A, Bourlet Y, Buckingham M (1986) Comparison of three actin-coding sequences in the mouse; evolutionary relationships between the actin genes of warm-blooded vertebrates. J Mol Evol 23:11–22Google Scholar
  2. Andersson SGE and Kurland CG (1990) Codon preferences in free-living microorganisms. Microbiol Rev 54:198–210Google Scholar
  3. Aota S, Ikemura T (1986) Diversity in G + C content at the third position of codons in vertebrate genes and its cause. Nucleic Acids Res 14:6345–6355, and correction 14:8702Google Scholar
  4. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958Google Scholar
  5. Bernardi G, Mouchiroud D, Gautier C, Bernardi G (1988) Compositional patterns in vertebrate genomes: conservation and change in evolution. J Mol Evol 28:7–18Google Scholar
  6. Bulmer M, Wolfe KH, Sharp PM (1991) Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci USA 88:5974–5978Google Scholar
  7. Catzeflis FM, Sheldon FH, Ahlquist JE, Sibley CG (1987) DNA-DNA hybridization evidence of the rapid rate of muroid rodent DNA evolution. Mol Biol Evol 4:242–253PubMedGoogle Scholar
  8. Catzeflis FM, Nevo E, Ahlquist JE, Sibley CG (1989) Relationship of the chromosomal species in the Eurasian mole rats of the Spalax ehrenbergi group as determined by DNA-DNA hybridization, and an estimate of the spalacid-murid divergence time. J Mol Evol 29:223–232Google Scholar
  9. Catzeflis FM, Aguilar J-P, Jaeger J-J (1992) Muroid rodents: phylogeny and evolution. Trends Ecol Evol 7:122–126Google Scholar
  10. Chen YH, Pentecost BT, McLachlan JA, Teng CT (1987) The androgen-dependent mouse seminal vesicle secretory protein IV: characterization and complementary deoxyribonucleic acid cloning. Mol Endocrinol 1:707–716Google Scholar
  11. Cohen DR, Hapel AJ, Young IG (1986) Cloning and expression of the rat interleukin-3 gene. Nucleic Acids Res 14:3641–3658Google Scholar
  12. Dickerson RE (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45Google Scholar
  13. Dickinson DP, Mirels L, Tabak LA, Gross KW (1989) Rapid evolution of variants in a rodent multigene family encoding salivary proteins. Mol Biol Evol 6:80–102Google Scholar
  14. Dietrich W, Katz H, Lincoln SE, Shin H-S, Friedman J, Dracopoli NC, Lander ES (1992) A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131:423–447Google Scholar
  15. Durnam DM, Perrin F, Gannon F, Palmiter RD (1980) Isolation and characterization of the mouse metallothionein-I gene. Proc Natl Acad Sci USA 77:6511–6515Google Scholar
  16. Eyre-Walker A (1991) An analysis of codon usage in mammals: selection or mutation bias? J Mol Evol 33:442–449Google Scholar
  17. Filipski J (1987) Correlation between molecular clock ticking, codon usage, fidelity of DNA repair, chromosome banding and chromatin compactness in germline cells. FEBS Lett 217:184–186Google Scholar
  18. Filipski J (1988) Why the rate of silent codon substitutions is variable within a vertebrate's genome. J Theor Biol 134:159–164Google Scholar
  19. Fitch WM (1980) Estimating the total number of nucleotide sub, stitutions since the common ancestor of a pair of genes: comparison of several methods and three beta hemoglobin messenger RNA's. J Mol Evol 16:153–209Google Scholar
  20. Giannelli F, Green PM, High KA, Sommer S, Lillicrap DP, Ludwig M, Olek K, Reitsma PH, Goossens M, Yoshioka A, Brownlee GG (1991) Haemophilia B: database of point mutations and short additions and deletions—second edition. Nucleic Acids Res 19 (suppl.):2193–2219Google Scholar
  21. Goodman M, Koop BF, Czelusniak J, Fitch DHA, Tagle DA, Slightom JL (1989) Molecular phylogeny of the family of apes and humans. Genome 31:316–335Google Scholar
  22. Gouy M (1987) Codon contexts in enterobacterial and coliphage genes. Mol Biol Evol 4:426–444Google Scholar
  23. Gouy M, Gautier C, Attimonelli M, Lanave C, di Paola G (1985) ACNUC—a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. Comp Appl Biosci 1:167–172Google Scholar
  24. Graur D (1985) Amino acid composition and the evolutionary rates of protein-coding genes. J Mol Evol 22:53–62Google Scholar
  25. Hard DL, Clark AG (1989) Principles of population genetics. Sinauer Associates, Sunderland, MAGoogle Scholar
  26. Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on a microcomputer. Comp Appl Biosci 5:151–153Google Scholar
  27. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex loci reveals overdominant selection. Nature 335:167–170CrossRefPubMedGoogle Scholar
  28. Iizasa T, Taira M, Shimada H, Ishijima S, Tatibana M (1989) Molecular cloning and sequencing of human cDNA for phosphoriboxyl pyrophosphate synthetase subunit II. FEBS Lett 244:47–50Google Scholar
  29. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34Google Scholar
  30. Ikemura T, Aota S (1988) Global variation in G + C content along vertebrate genome DNA. J Mol Biol 203:1–13Google Scholar
  31. Jagodzinski LL, Sargent TD, Yang M, Glackin C, Bonner J (1981) Sequence homology between RNAs encoding rat alpha-fetoprotein and rat serum albumin. Proc Natl Acad Sci USA 78:3521–3525Google Scholar
  32. Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276Google Scholar
  33. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedGoogle Scholar
  34. Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458Google Scholar
  35. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, EnglandGoogle Scholar
  36. King JL, Jukes TH (1969) Non-Darwinian evolution. Science 164:788–798Google Scholar
  37. Lawrence JG, Hard DL, Ochman H (1991) Molecular considerations in the evolution of bacterial genes. J Mol Evo1 33:241–250Google Scholar
  38. Lipman DJ, Wilbur WJ (1985) Interaction of silent and replacement changes in eukaryotic coding sequences. J Mol Evol 21:161–167Google Scholar
  39. Li W-H, Wu C-I, Luo C-C (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 2:150–174Google Scholar
  40. Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342Google Scholar
  41. Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332Google Scholar
  42. Miyata T, Hayashida H, Kuma K, Yasunaga T (1987a) Male-driven molecular evolution demonstrated by different rates of silent substitutions between autosome- and sex chromosome-linked genes. Proc Jpn Acad Ser B 63:327–331Google Scholar
  43. Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunaga T (1987b) Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harbor Symp Quant Bio 152:863–867Google Scholar
  44. Miyata T, Kuma K, Iwabe N, Hayashida H, Yasunaga T (1990) Different rates of evolution of autosome-, X chromosome and Y chromosome-linked genes: hypothesis of male-driven molecular evolution. In: Takahata N, Crow JF (eds) Population biology of genes and molecules. Baifukan, Tokyo, Japan, pp 341–357Google Scholar
  45. Mouchiroud D, Gautier C, Bernardi G (1988) The compositional distribution of coding sequences and DNA molecules in humans and murids. J Mol Evol 27:311–320Google Scholar
  46. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  47. Newgard CB, Nakano K, Hwang PK, Fletterick RJ (1986) Sequence analysis of the cDNA encoding human liver glycogen phosphorylase reveals tissue-specific codon usage. Proc Natl Acad Sci USA 83:8132–8136Google Scholar
  48. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86Google Scholar
  49. Sharp PM (1989) Evolution at ‘silent’ sites in DNA. In: Hill WG, Mackay TFC (eds) Evolution and animal breeding; reviews on molecular and quantitative approaches in honour of Alan Robertson. C.A.B. International, Wallingford, UK, pp 24–32Google Scholar
  50. Sharp PM (1991) Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J Mol Evol 33:23–33Google Scholar
  51. Sharp PM, Li W-H (1987) The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4:222–230Google Scholar
  52. Sharp PM, Li W-H (1989) On the rate of DNA sequence evolution in Drosophila. J Mol Evol 28:398–402Google Scholar
  53. Sharp PM, Tuohy TMF, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates between highly and lowly expressed genes. Nucleic Acids Res 14: 5125–5143Google Scholar
  54. Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F (1988) 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 16:8207–8211Google Scholar
  55. Shields DC, Sharp PM, Higgins DG, Wright F (1988) “Silent” sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 5:704–716PubMedGoogle Scholar
  56. Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657Google Scholar
  57. Tajima F, Nei M (1984) Estimation of evolutionary distances between nucleotide sequences. Mol Biol Evol 1:269–285Google Scholar
  58. Ticher A, Graur D (1989) Nucleic acid composition, codon usage, and the rate of synonymous substitution in protein-coding genes. J Mol Evol 28:286–298Google Scholar
  59. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Ann Rev Biochem 46:573–639Google Scholar
  60. Wilson AC, Ochman H, Prager EM (1987) Molecular time scale for evolution. Trends Genet 3:241–247Google Scholar
  61. Wolfe KH (1991) Mammalian DNA replication: mutation biases and the mutation rate. J Theor Biol 149:441–451Google Scholar
  62. Wolfe KH, Sharp PM (1988) Identification of functional open reading frames in chloroplast genomes. Gene 66:215–222Google Scholar
  63. Wolfe KH, Sharp PM, Li W-H (1989) Mutation rates differ among regions of the mammalian genome. Nature 337:283–285CrossRefPubMedGoogle Scholar
  64. Zuckerkandl E, Pauling L (1962) Molecular disease, evolution, and genic heterogeneity. In: Kasha M, Pullman B (eds) Horizons in biochemistry. Academic Press, New York, pp 189–225Google Scholar

Copyright information

© Springer-Verlag New York Inc 1993

Authors and Affiliations

  • Kenneth H. Wolfe
    • 1
  • Paul M. Sharp
    • 1
  1. 1.Department of Genetics, University of DublinTrinity CollegeDublin 2Ireland

Personalised recommendations