DURET

Codon usage in animals and plants: new data, new paradox

Laurent Duret and Dominique Mouchiroud

Laboratoire de Biométrie et Biologie Evolutive, Université Claude Bernard, Villeurbanne Cedex, France

We analyzed the expression pattern and codon usage in 8133, 1550, 2917 and 760 genes respectively from Caenorhabditis elegans, Drosophila melanogaster, Arabidopsis thaliana and human. In human, codon usage is correlated to the base composition of the genomic context (isochore) in which the gene is embedded, but not to its expression pattern. Variations of codon usage among human genes probably result of neutral evolution due to mutational biases rather than of selection for optimal gene expression.

Interestingly, in the three other species, we observed a clear correlation between codon usage and gene expression levels, and showed that this correlation is not due to a mutational bias. This provides direct evidence for selection on silent sites in those three distantly related multicellular eukaryotes. Surprisingly, there is a strong negative correlation between codon usage and protein length. This effect is not due to a smaller size of highly expressed proteins. Thus, for a same expression pattern, the selective pressure on codon usage appears to be lower in genes encoding long rather than short proteins. This puzzling observation is not predicted by any of the current models of selection on codon usage and thus raises the question of how translation efficiency affects fitness in multicellular organisms.