Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, Arabidopsis

We measured the expression pattern and analyzed codon usage in 8,133, 1,550 , and 2,917 genes, respectively, from Caenorhabditis elegans, Drosophila me lanogaster, and Arabidopsis thaliana. In those three species, we observed a clear correlation between codon usage and gene expression levels and showe d that this correlation is not due to a mutational bias. This provides dire ct evidence for selection on silent sites in those three distantly related multicellular eukaryotes. Surprisingly, there is a strong negative correlat ion between codon usage and protein length. This effect is not due to a sma ller size of highly expressed proteins. Thus, for a same-expression pattern , the selective pressure on codon usage appears to be lower in genes encodi ng long rather than short proteins. This puzzling observation is not predic ted by any of the current models of selection on codon usage and thus raise s the question of how translation efficiency affects fitness in multicellul ar organisms.