- Published Version
Official URL: http://dx.doi.org/10.1186/1471-2148-7-S1-S6
Synonymous codon usage varies widely between genomes, and also between genes within genomes. Although there is now a large body of data on variations in codon usage, it is still not clear if the observed patterns reflect the effects of positive Darwinian selection acting at the level of translational efficiency or whether these patterns are due simply to the effects of mutational bias. In this study, we have included both intra-genomic and inter-genomic comparisons of codon usage. This allows us to distinguish more efficiently between the effects of nucleotide bias and translational selection.
We show that there is an extreme degree of heterogeneity in codon usage patterns within the rice genome, and that this heterogeneity is highly correlated with differences in nucleotide content (particularly GC content) between the genes. In contrast to the situation observed within the rice genome, Arabidopsis genes show relatively little variation in both codon usage and nucleotide content. By exploiting a combination of intra-genomic and inter-genomic comparisons, we provide evidence that the differences in codon usage among the rice genes reflect a relatively rapid evolutionary increase in the GC content of some rice genes. We also noted that the degree of codon bias was negatively correlated with gene length.
Our results show that mutational bias can cause a dramatic evolutionary divergence in codon usage patterns within a period of approximately two hundred million years.
The heterogeneity of codon usage patterns within the rice genome can be explained by a balance between genome-wide mutational biases and negative selection against these biased mutations. The strength of the negative selection is proportional to the length of the coding sequences. Our results indicate that the large variations in synonymous codon usage are not related to selection acting on the translational efficiency of synonymous codons.
|Divisions:||Concordia University > Faculty of Arts and Science > Biology|
|Authors:||Wang, Huai-Chun and Hickey, Donal A.|
|Journal or Publication:||BMC Evolutionary Biology|
|Date:||8 February 2007|
|Deposited By:||DANIELLE DENNIE|
|Deposited On:||11 May 2011 22:10|
|Last Modified:||24 Aug 2016 21:26|
1.Grantham R, Gautier C, Gouy C: Codon frequencies in 119 individual genes confirm consistent choices of degenerate bases according to genome type. Nucleic Acids Res 1980, 8:1893-1912.
2.Peden JF: Analysis of Codon Usage. In PhD Thesis. University of Nottingham; 1999.
3.Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F: Codon usage in Escherichia coli, Bacillussubtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res 1988, 16:8207-8211.
4.Wang HC, Badger J, Kearney P, Li M: Analysis of codon usage patterns of bacterial genomes using the self-organizing map. Mol Biol Evol 2001, 18:792-800.
5.Gouy M, Gautier C: Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 1982, 10:7055-7074.
6.Sharp PM, Matassi G: Codon usage and genome evolution. Curr Opin Genet Dev 1994, 4:851-860.
7.Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE: Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 2005, 33:1141-1153.
8.Ikemura T: Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 1981, 146:1-21.
9.Kanaya S, Yamada Y, Kudo Y, Ikemura T: Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 1999, 238:143-155.
10.Shields DC, Sharp PM, Higgins D, Wright F: "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 1988, 5:704-716.
11.Stenico M, Lloyd AT, Sharp PM: Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucleic Acids Res 1994, 22:2437-2446.
12.Li WH: Molecular Evolution. Sunderland, MA: Sinauer Associates, Inc; 1997.
13.Kudla G, Lipinski L, Caffin F, Helwak A, Zylicz M: High guanine and cytosine content increases mRNA levels in mammalian cells. PLoS Biol 2006, 4:e180.
14.Fennoy SL, Bailey-serres J: Synonymous codon usage in Zea mays L. nuclear genes is varied by levels of C and G-ending codons. Nucleic Acids Res 1993, 21:5294-5300.
15.Carels N, Bernardi G: Two classes of genes in plants. Genetics 2000, 154:1819-1825.
16.Ware D, Jaiswal P, Ni J, Pan X, Chang K, Clark K, Teytelman L, Schmidt S, Zhao W, Cartinhour S, et al.: Gramene: a resource for comparative grass genomics. Nucleic Acids Res 2002, 30:103-105.
17.Wang HC, Singer GAC, Hickey DA: Mutational bias affects protein evolution in flowering plants. Mol Biol Evol 2004, 21:90-96.
18.Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
19.Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43.
20.Wright F: The 'effective number of codons' used in a gene. Gene 1990, 87:23-29.
21.Greenacre MJ: Theory and Applications of Correspondence Analysis. London: Academic Press; 1984.
22.Perriere G, Thioulouse J: Use and misuse of correspondence analysis in codon usgae studies. Nucl Acids Res 2002, 30:4548-4555.
23.Banerjee T, Gupta SK, Ghosh TC: Compositional transitions between Oryza sativa and Arabidopsis thaliana genes are linked to the functional change of encoded proteins. Plant Sci 2006, 170:267-273.
24.Novembre JA: Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol 2002, 19:1390-1394.
25.Duret L, Mouchiroud D: Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA 1999, 96:4482-4487.
26.Liu Q, Dou S, Ji Z, Xue Q: Synonymous codon usage and gene function are strongly related in Oryza sativa. Biosystems 2005, 80:123-131.
27.Mathe C, Peresetsky A, Dehais P, Van Montagu M, Rouze P: Classification of Arabidopsis thaliana gene sequences: clustering of coding sequences into two groups according to codon usage improves gene prediction. J Mol Biol 1999, 285:1977-1991.
28.Dos Reis M, Savva R, Wernisch L: Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res 2004, 32:5036-5044.
29.Urrutia AO, Hurst LD: The signature of selection mediated by expression on human genes. Genome Res 2003, 13:2260-2264.
30.Sharp PM, Li WH: The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 1987, 4:222-230.
31.Powell JR, Moriyama EN: Evolution of codon usage bias in Drosophila. Proc Natl Acad Sci USA 1997, 94:7784-7790.
32.Xia X, Wang H, Xie Z, Carullo M, Huang H, Hickey D: Cytosine Usage Modulates the Correlation between CDS Length and CG Content in Prokaryotic Genomes. Mol Biol Evol 2006, 23:1450-1454.
Repository Staff Only: item control page