Summary
This paper reports on the relationship between the number of silent differences and the codon usage changes in the lineages leading to human and rat. Examination of 102 pairs of homologous genes gives rise to four main conclusions: (1) We have previously demonstrated the existence of a codon usage change (called the minor shift) between human and rat; this was confirmed here with a larger sample. For genes with extreme C+G frequencies, the C+G level in the third codon position is less extreme in rat than in human. (2) Protein similarity and percentage of positive differences are the two main factors that discriminate homologous genes when characterized by differences between rat and human. By definition, positive differences result from silent changes between A or T and C or G with a direction implying a C+G content variation in the same direction as the overall gene variation. (3) For genes showing both codon usage change and low protein similarity, a majority of amino acid replacements contributes to C+G level variation in positions I and II in the same direction as the variation in position III. This is thus a new example of protein evolution due to constraints acting at the DNA level. (4) In heavy isochores (high C+G content) no direct correlation exists between codon usage change (measured by the dissymmetry of differences) and silent dissimilarity. In light isochores the opposite situation is observed: modification of codon usage is associated with a high synonymous dissimilarity. This result shows that, in some cases, modification of constraints acting at the DNA level could accelerate divergence between genomes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Argos P, Rossmann MG, Grau UM, Zuber H, Frank G (1979) Thermal stability and protein structure. Biochemistry 18:5698–5703
Benzecri JP (1973) L'analyse des correspondances. In: L'analyse des données, tome 2. Dunod, Paris
Bernardi G (1989) The isochore organization of the human genome. Annu Rev Genet 23:637–661
Bernardi G, Bernardi G (1986) Compositional constraints and genome composition. J Mol Evol, 24:1–11
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 228:953–958
Bernardi G, Mouchiroud D, Gautier C, Bernardi G (1988) Compositional patterns in vertebrate genomes: conservation and change in evolution. J Mol Evol 28:7–18
Bilofsky HS, Burks C, Fickett JW, Goad WB, Lewitter FI, Rindone WP, Swindell LD, Tung CS (1986) The Genbank genetic sequence data base. Nucleic Acids Res 14:1–4
Blaisdell BE (1985) A method of estimating from two aligned present-day DNA sequences their ancestral composition and subsequent rates of substitution, possibly different in the two lineages, corrected for multiple and parallel substitutions at the same site. J Mol Evol 22:69–81
Buskin JN, Jaynes JB, Chamberlain JS, Hauschka SD (1985) The mouse muscle creatine kinase cDNA and deduced amino acid sequences: comparison to evolutionarily related enzymes. J Mol Evol 22:334–341
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, 4:242–253
Chessel D, Gautier C (1977) Des statistiques non paramétriques pour l'analyse des données binaires. Rev Stat Appl 25:57–73
Erba HP, Gunning P, Kedes L (1986) Nucleotide sequence of the human γ cytoskeletal actin mRNA: anomalous evolution of vertebrate nonmuscle actin genes. Nucleic Acids Res 14: 5275–5294
Garel JP, Mandel P, Chavancy G, Daillie J (1970) Functional adaptation of tRNAs to fibroin biosynthesis in the silkgland ofBombyx mori. FEBS Lett 7:327–329
Gautier C (1987) Codon usage changes during evolution: animal mitochondria example. C R Acad Sci (Paris) 304:123–128
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. CABIOS 1:167–172
Grantham R, Gautier C, Gouy M (1980) Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res 8:1893–1912
Hanai R, Wada A (1988) The effects of guanine and cytosine variation on dinucleotide frequency and amino acid composition in the human genome. J Mol Evol 27:321–325
Ikemura T, Aota S (1988) Global variation in C+G content along vertebrate genome DNA. Possible correlation with chromosome band structures. J Mol Biol 203:1–13
Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20:86–93
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
Li WH, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342
Luo CC, Li WH (1986) Structure and evolution of the apolipoprotein multigene family. J Mol Biol 187:325–340
Minghetti HP, Simon WL, Dugaiczyk A (1985) The rate of molecular evolution of α-fetoprotein approaches that of pseudogenes. Mol Biol Evol 2:347–358
Mouchiroud D, Gautier C (1988) High codon usage change in mammalian genes. Mol Biol Evol 5:192–194
Mouchiroud D, Fichant G, Bernardi G (1987) Compositional compartmentalization and gene composition in the genome of vertebrates. J Mol Evol 26:198–204
Mouchiroud D, Gautier C, Bernardi G (1988) The compositional distribution of coding sequences and DNA molecules in humans and murids. J. Mol Evol 27:311–320
Preparata G, Saccone C (1987) A simple quantitative model of the molecular clock. J Mol Evol 26:7–15
Saccone C, Pesole G, Preparata G (1989) DNA microenvironments and the molecular clock. J Mol Evol 29:407–411
Sakakibara M, Mukai T, Yatsuki H, Hori K (1985) Human aldolase isozyme gene: the structure of multispecies aldolase B mRNAs. Nucleic Acids Res 13:5055–5069
Smith TF, Waterman MS, Fitch WM (1981) Comparative biosequence metrics. J Mol Evol 18:36–46
Ticher A, Graur D (1989) Nucleic acid composition, codon usage, and the rate of synonymous substitution in proteincoding genes. J Mol Evol 28:286–298
Wolfe KH, Sharp PM, Li WH (1989) Mutation rates differ among regions of the mammalian genome. Nature 337:283–285
Wu CI, Li WH (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Mouchiroud, D., Gautier, C. Codon usage changes and sequence dissimilarity between human and rat. J Mol Evol 31, 81–91 (1990). https://doi.org/10.1007/BF02109477
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02109477