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

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 showe...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 1999-04, Vol.96 (8), p.4482-4487
Main Authors: Duret, L, Mouchiroud, D
Format: Article
Language:English
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
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Summary: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.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.96.8.4482