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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 96; no. 8; pp. 4482 - 4487
• Main Authors: Duret, L, Mouchiroud, D
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences of the United States of America 13.04.1999; National Acad Sciences; National Academy of Sciences; The National Academy of Sciences
• Subjects: Amino acids; animal proteins; Animals; Arabidopsis - genetics; Arabidopsis thaliana; Biological Evolution; Biological Sciences; Caenorhabditis elegans; Caenorhabditis elegans - embryology; Caenorhabditis elegans - genetics; Caenorhabditis elegans - growth & development; CDNA libraries; Codon - genetics; Codons; Correlations; Drosophila; Drosophila melanogaster; Drosophila melanogaster - genetics; Embryos; Expressed Sequence Tags; favored codons; Gene expression; Gene Expression Regulation; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; genes; genetic code; Genetic mutation; Genetics; Insects; length; Life Sciences; Messenger RNA; Mutation; Other; plant proteins; Proteins; relationships; relative synonymous codon usage; RNA, Messenger - analysis; Selection, Genetic; Transfer RNA; Worms
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.96.8.4482

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.