MBE Advance Access published online on September 28, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm210
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Research Article |
Evidence for a Trade-Off between Translational Efficiency and Splicing Regulation in Determining Synonymous Codon Usage in Drosophila melanogaster
* Department of Biology and Biochemistry, University of Bath, Bath, BA2 7AY, UK
Corresponding author: Laurence D. Hurst, University of Bath, Claverton Down, Bath, BA2 7AY, United Kingdom, Tel: + 44 (0)1225 386424, Fax: + 44 (0)1225 386779, email: l.d.hurst{at}bath.ac.uk
Received for publication August 13, 2007. Revision received September 20, 2007. Accepted for publication September 24, 2007.
In Drosophila melanogaster synonymous codons corresponding to the most abundant cognate tRNAs are used more frequently, especially in highly expressed genes. Increased use of such "optimal" codons is considered an adaptation for translational efficiency. Need it always be the case that selection should favour the use of a translationally optimal codon? Here we investigate one possible confounding factor, namely the need to specify information in exons necessary to enable correct splicing. As expected from such a model, in Drosophila many codons show different usage near intron-exon boundaries versus exon core regions. However, this finding is in principle also consistent with Hill-Robertson effects modulating usage of translationally optimal codons. However, several results support the splice model over the translational selection model: 1) the trends in codon usage are strikingly similar to those in mammals in which codon usage near boundaries correlates with abundance in exonic splice enhancers, 2) codons preferred near boundaries tend to be enriched for A and avoid C (conversely those avoided near boundaries prefer C rather than A), as expected were exonic splice enhancers involved, and 3) codons preferred near boundaries are typically not translationally optimal. We conclude that usage of translationally optimal codon usage is compromised in the vicinity of splice junctions in intron-containing genes, to the effect that we observe higher levels of usage of translationally optimal codons at the centre of exons. On the gene level, however, controlling for known correlates of codon bias the impact on codon usage patterns is quantitatively small. These results have implications for inferring aspects of the mechanism of splicing given nothing more than a well-annotated genome.
Key Words: Splicing • codon usage bias • Hill-Robertson interference • ESE • Drosophila melanogaster
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