An evolutionary perspective on synonymous codon usage in unicellular organisms

Sharp, Paul M.; Li, Wen-Hsiung

doi:10.1007/bf02099948

Cited by 861 publications

(638 citation statements)

References 41 publications

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“…Our data revealed several shared correlations between the X chromosome and the autosomes, with respect to both the magnitude of the correlation and the direction ( Table 2). As previously reported (Bulmer 1988;Duret and Mouchiroud 1999;Hey and Kliman 2002;Sharp and Li 1986), codon bias is significantly positively correlated with expression level (Kendall partial correlation s = 0.234 and 0.221 for autosomes and X, respectively, Bonferroni-corrected p << 0.0001, both comparisons), which likely reflects increased selective benefits of translational efficiency for highly expressed genes. In addition, we confirm the negative correlation between protein length and codon bias (Kendall partial correlation s = )0.315 and )0.321 for autosomes and X, respectively.…”

Section: Additional Relationships Among Codon Bias Correlatessupporting

confidence: 79%

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

2005

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Abstract. The patterns and processes of molecular evolution may differ between the X chromosome and the autosomes in Drosophila melanogaster. This may in part be due to differences in the effective population size between the two chromosome sets and in part to the hemizygosity of the X chromosome in Drosophila males. These and other factors may lead to differences both in the gene complements of the X and the autosomes and in the properties of the genes residing on those chromosomes. Here we show that codon bias and recombination rate are correlated strongly and negatively on the X chromosome, and that this correlation cannot be explained by indirect relationships with other known determinants of codon bias. This is in dramatic contrast to the weak positive correlation found on the autosomes. We explored possible explanations for these patterns, which required a comprehensive analysis of the relationships among multiple genetic properties such as protein length and expression level. This analysis highlights conserved features of coding sequence evolution on the X and the autosomes and illuminates interesting differences between these two chromosome sets.

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Section: Additional Relationships Among Codon Bias Correlatessupporting

confidence: 79%

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

2005

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“…This is highly unlikely, and we argue elsewhere that there is likely a continuum in Drosophila (and other organisms) with codon usage in highly biased genes being primarily affected by selection, whereas other genes may have codon usage controlled primarily by mutation and drift along the lines of models previously proposed (33,34). This is in agreement with Akashi's (35) observation that the selection for optimal codons in D. simulans has been more effective than in D. melanogaster.…”

Section: Resultsmentioning

confidence: 80%

Evolution of codon usage bias in Drosophila

Powell

Moriyama

1997

Proc. Natl. Acad. Sci. U.S.A.

297

196

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We first review what is known about patterns of codon usage bias in Drosophila and make the following points: (i) Drosophila genes are as biased or more biased than those in microorganisms. (vii) Finally, smaller genes tend to be more biased than longer genes. We then examine possible causes of these patterns and discount mutation bias on three bases: there is little evidence of regional mutation bias in Drosophila, mutation bias is likely toward A؉T (the opposite of codon usage bias), and not all amino acids display the preference for the same nucleotide in the wobble position. Two lines of evidence support a selection hypothesis based on tRNA pools: highly biased genes tend to be highly and͞or rapidly expressed, and the preferred codons in highly biased genes optimally bind the most abundant isoaccepting tRNAs. Finally, we examine the effect of bias on DNA evolution and confirm that genes with high codon usage bias have lower rates of synonymous substitution between species than do genes with low codon usage bias. Surprisingly, we find that genes with higher codon usage bias display higher levels of intraspecific synonymous polymorphism. This may be due to opposing effects of recombination.As far as is known, synonymous mutations are truly neutral with respect to natural selection.The above quotation from King and Jukes (1) was one of the major, and more reasonable, tenets of the neutral theory of molecular evolution. With few exceptions (e.g., ref.2), even those researchers who tended toward the selectionist view of molecular evolution were willing to concede synonymous substitutions to the neutralists. After all, such mutations do not affect the structure of the primary gene product and therefore should not be able to affect the phenotype, the level at which natural selection acts. One of the more surprising observations provided by the accumulating DNA sequence data has been the evidence that selection can and does affect synonymous substitutions.

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“…Codon bias. Codon bias is thought to enhance the efficiency and/or accuracy of translation [99][100][101] and seems to be maintained by mutation-selection-drift balance [101][102][103][104] . Across the 12 Drosophila genomes, there is more codon bias in the Sophophora subgenus than in the Drosophila subgenus, and a previously noted [105][106][107][108][109] striking reduction in codon bias in D. willistoni 110,111 (Fig.…”

Section: Articlesmentioning

confidence: 99%

Evolution of genes and genomes on the Drosophila phylogeny

Clark¹,

Eisen²,

Smith³

et al. 2007

Nature

1,831

1,041

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Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.

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An evolutionary perspective on synonymous codon usage in unicellular organisms

Cited by 861 publications

References 41 publications

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

Codon Bias and Noncoding GC Content Correlate Negatively with Recombination Rate on the Drosophila X Chromosome

Evolution of codon usage bias in Drosophila

Evolution of genes and genomes on the Drosophila phylogeny

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