Recombination, meiotic expression and human codon usage

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Abstract

Synonymous codon usage (SCU) varies widely among human genes. In particular, genes involved in different functional categories display a distinct codon usage, which was interpreted as evidence that SCU is adaptively constrained to optimize translation efficiency in distinct cellular states. We demonstrate here that SCU is not driven by constraints on tRNA abundance, but by large-scale variation in GC-content, caused by meiotic recombination, via the non-adaptive process of GC-biased gene conversion (gBGC). Expression in meiotic cells is associated with a strong decrease in recombination within genes. Differences SCU among functional categories reflect differences in levels of meiotic transcription, which is linked to variation in recombination and therefore in gBGC. Overall, the gBGC model explains 70% of the variance in SCU among genes. We argue that the strong heterogeneity of SCU induced by gBGC in mammalian genomes precludes any optimization of the tRNA pool to the demand in codon usage.

Data availability

The following previously published data sets were used

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Article and author information

Author details

Fanny Pouyet

Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Claude Bernard, CNRS UMR 5558, Villeurbanne, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5614-6998
Dominique Mouchiroud

Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Claude Bernard, CNRS UMR 5558, Villeurbanne, France

Competing interests
The authors declare that no competing interests exist.
Laurent Duret

Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Claude Bernard, CNRS UMR 5558, Villeurbanne, France

For correspondence
Laurent.Duret@univ-lyon1.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2836-3463
Marie Sémon

Laboratory of Biology and Modelling of the Cell, Université de Lyon, Université Claude Bernard, CNRS UMR 5239, INSERM U1210, Lyon, France

For correspondence
marie.semon@ens-lyon.fr

Competing interests
The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR-530 15-CE12-0010-01/DaSiRe)

Laurent Duret

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.