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

Abstract

We measured the expression pattern and analyzed codon usage in 8,133, 1,550, and 2,917 genes, respectively, from Caenorhabditis elegans, Drosophila melanogaster, and Arabidopsis thaliana. In those three 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.

Figure 1

Frequency of favored codons and gene expression in C. elegans, D. melanogaster, and A. thaliana. Average Fav values have been computed for different expression levels and protein lengths. Error bars indicate the 95% confidence interval.

Figure 2

Frequency of favored codons and development stage expression in C. elegans. Average Fav values have been computed for different patterns of expression and protein lengths. Error bars indicate the 95% confidence interval.

Figure 3

Frequency of favored codons in C. elegans genes expressed at high level having a neighbor expressed at high level less than 5 kb from their 5′ or 3′ end. Average Fav values have been computed for different protein lengths. Error bars indicate the 95% confidence interval.