Abstract
BackgroundSurprisingly, in several multi-cellular eukaryotes optimal codon use correlates negatively with gene length. This contrasts with the expectation under selection for translational accuracy. While suggested explanations focus on variation in strength and efficiency of translational selection, it has rarely been noticed that the negative correlation is reported only in organisms whose optimal codons are biased towards codons that end with G or C (-GC). This raises the question whether forces that affect base composition - such as GC-biased gene conversion - contribute to the negative correlation between optimal codon use and gene length.ResultsYeast is a good organism to study this as equal numbers of optimal codons end in -GC and -AT and one may hence compare frequencies of optimal GC- with optimal AT-ending codons to disentangle the forces. Results of this study demonstrate in yeast frequencies of GC-ending (optimal AND non-optimal) codons decrease with gene length and increase with recombination. A decrease of GC-ending codons along genes contributes to the negative correlation with gene length. Correlations with recombination and gene expression differentiate between GC-ending and optimal codons, and also substitution patterns support effects of GC-biased gene conversion.ConclusionWhile the general effect of GC-biased gene conversion is well known, the negative correlation of optimal codon use with gene length has not been considered in this context before. Initiation of gene conversion events in promoter regions and the presence of a gene conversion gradient most likely explain the observed decrease of GC-ending codons with gene length and gene position.
Highlights
In several multi-cellular eukaryotes optimal codon use correlates negatively with gene length
Results of this study demonstrate in S. cerevisiae the frequency of GC-ending codons decreases with gene length and increases with recombination
Difference between optimal codons depending on whether they end with -AT or -GC To disentangle forces affecting base compositions from translational selection on optimal codons, one can compare optimal GC-ending and optimal AT-ending codons
Summary
In several multi-cellular eukaryotes optimal codon use correlates negatively with gene length This contrasts with the expectation under selection for translational accuracy. While suggested explanations focus on variation in strength and efficiency of translational selection, it has rarely been noticed that the negative correlation is reported only in organisms whose optimal codons are biased towards codons that end with G or C (-GC). Under translational selection for accuracy one may expect higher optimal codon frequencies at conserved than at non-conserved amino acid sites This is the case in D. melanogaster, C. elegans, E. coli [12,13,14]; a recent study [15] indicates this pattern may apply to mouse and human using a modified measure of optimal codons
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