Synonymous codon usage in Drosophila melanogaster: Natural selection and translational accuracy
Open accessAbstract
I present evidence that natural selection biases synonymous codon usage to enhance the accuracy of protein synthesis in Drosophila melanogaster. Since the fitness cost of a translational misincorporation will depend on how the amino acid substitution affects protein function, selection for translational accuracy predicts an association between codon usage in DNA and functional constraint at the protein level. The frequency of preferred codons is significantly higher at codons conserved for amino acids than at nonconserved codons in 38 genes compared between D. melanogaster and Drosophila virilis or Drosophila pseudoobscura (Z = 5.93, P < 10(-6)). Preferred codon usage is also significantly higher in putative zinc-finger and homeodomain regions than in the rest of 28 D. melanogaster transcription factor encoding genes (Z = 8.38, P < 10(-6)). Mutational alternatives (within-gene differences in mutation rates, amino acid changes altering codon preference states, and doublet mutations at adjacent bases) do not appear to explain this association between synonymous codon usage and amino acid constraint.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The codon optimization in the previous section suffers from the lack of consideration for translation accuracy.
“The codon optimization in the previous section suffers from the lack of consideration for translation accuracy [36,37].”
From Detailed Dissection and Critical Evaluation of the Pfizer/BioNTech and Moderna mRNA Vaccines (2021) · cites this paper as [37]
Akashi found greater codon adaptation in conserved amino acid sites than in variable amino acid sites.
“He found greater codon adaptation in conserved amino acid sites than in variable amino acid sites.”
From Detailed Dissection and Critical Evaluation of the Pfizer/BioNTech and Moderna mRNA Vaccines (2021) · cites this paper as [37]
The difference between conserved and variable sites has resulted from selection for accuracy.
“This is consistent with his inference that the difference between the conserved and variable sites has resulted from selection for accuracy.”
From Detailed Dissection and Critical Evaluation of the Pfizer/BioNTech and Moderna mRNA Vaccines (2021) · cites this paper as [37]
Cites
Statistical Aspects of the Analysis of Data From Retrospective Studies of Disease
(1959) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/22.4.719 · Cited by 14,689 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Coding-Sequence Determinants of Gene Expression in <i>Escherichia coli</i>
Kudla, G., Murray, A. W., Tollervey, D., & Plotkin, J. B. (2009) · Science · doi:10.1126/science.1170160 · Cited by 1,458 · see citing works
Codon Optimality Is a Major Determinant of mRNA Stability
Presnyak, V., Alhusaini, N., Chen, Y.-H., Martin, S., Morris, N., Kline, N., Olson, S., Weinberg, D., Baker, K. E., Graveley, B. R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.02.029 · Cited by 1,078 · see citing works
Why highly expressed proteins evolve slowly
Drummond, D. A., Bloom, J. D., Adami, C., Wilke, C. O., & Arnold, F. H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504070102 · Cited by 815 · see citing works
Codon optimality, bias and usage in translation and mRNA decay
Hanson, G., & Coller, J. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.91 · Cited by 825 · see citing works
The evolutionary consequences of erroneous protein synthesis
Allan Drummond, D., & Wilke, C. O. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2662 · Cited by 515 · see citing works
Gu, W., Zhou, T., & Wilke, C. O. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000664 · Cited by 313 · see citing works
On the origin and evolution of SARS-CoV-2
Singh, D., & Yi, S. V. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00604-z · Cited by 281 · see citing works
Detailed Dissection and Critical Evaluation of the Pfizer/BioNTech and Moderna mRNA Vaccines
Xia, X. (2021) · Vaccines · doi:10.3390/vaccines9070734 · Cited by 201 · see citing works
Zhao, F., Yu, C.-H., & Liu, Y. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx501 · Cited by 120 · see citing works
Moura, G., Pinheiro, M., Arrais, J., Gomes, A. C., Carreto, L., Freitas, A., Oliveira, J. L., & Santos, M. A. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000847 · Cited by 107 · see citing works
Comparative context analysis of codon pairs on an ORFeome scale
Moura, G., Pinheiro, M., Silva, R., Miranda, I., Afreixo, V., Dias, G., Freitas, A., Oliveira, J. L., & Santos, M. A. (2005) · Genome Biology · doi:10.1186/gb-2005-6-3-r28 · Cited by 90 · see citing works
Estimating selection on synonymous codon usage from noisy experimental data
Wallace, E. W. J., Airoldi, E. M., & Drummond, D. A. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst051 · Cited by 48 · see citing works
Rosenberg, A. A., Marx, A., & Bronstein, A. M. (2022) · Nature Communications · doi:10.1038/s41467-022-30390-9 · Cited by 48 · see citing works
- Authors
- Akashi, H.
- Affiliations
- University of Chicago (US)
- Corresponding author
- Akashi, H
- ORCID
- Akashi, H
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 1994-03-01
- Volume
- 136
- Issue
- 3
- Pages
- 927-935
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- OpenAlex
- W2147126179
- Cited by
- 742
- References
- 1
- Citations by year
- 2026: 20 · 2025: 15 · 2024: 23 · 2023: 12 · 2022: 24 · 2021: 22 · 2020: 19 · 2019: 19 · 2018: 39 · 2017: 26 · 2016: 32 · 2015: 27 · 2014: 50 · 2013: 31 · 2012: 36
- FWCI
- 3.36
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- synonymous codon usage, Drosophila melanogaster, translational accuracy, natural selection, amino acid conservation, zinc finger proteins, homeodomain transcription factor, transcription factors, mutational bias, Drosophila virilis, Drosophila pseudoobscura
- MeSH terms
- Animals, Base Sequence, Codon, Drosophila, Drosophila melanogaster, Selection, Genetic, Species Specificity, Transcription Factors, Protein Biosynthesis, Genes, Insect
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review