Recombination, meiotic expression and human codon usage
- Université de Lyon, Université Claude Bernard, CNRS UMR 5558, France
- Université de Lyon, Université Claude Bernard, CNRS UMR 5239, INSERM U1210, France
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
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The transcriptome and DNA methylome landscapes of human primordial germ cells.Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE63818).
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Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomicsPublicly available at ArrayExpress (accession no. E-MTAB-1733).
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Parallel evolution of male germline epigenetic poising and somatic development in animals.Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE68507).
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A second generation human haplotype map of over 3.1 million SNPs.Publicly available at the NCBI ftp site for HapMap.
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Refined genetic maps reveal sexual dimorphism in human meiotic recombinationPublicly available at Github (https://github.com/).
Article and author information
Author details
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.
Reviewing Editor
- Molly Przeworski, Columbia University, United States
Version history
- Received: March 31, 2017
- Accepted: August 14, 2017
- Accepted Manuscript published: August 15, 2017 (version 1)
- Version of Record published: August 30, 2017 (version 2)
Copyright
© 2017, Pouyet et al.
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.
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Recombination, meiotic expression and human codon usage
eLife 6:e27344.
https://doi.org/10.7554/eLife.27344
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