Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.

Whether codon usage fine-tunes mRNA translation in mammals remains controversial, with recent papers suggesting that production of proteins in specific Gene Ontological (GO) pathways can be regulated by actively modifying the codon and anticodon pools in different cellular conditions. In this work,...

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Main Authors: Konrad L M Rudolph, Bianca M Schmitt, Diego Villar, Robert J White, John C Marioni, Claudia Kutter, Duncan T Odom
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-05-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1006024&type=printable
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author Konrad L M Rudolph
Bianca M Schmitt
Diego Villar
Robert J White
John C Marioni
Claudia Kutter
Duncan T Odom
author_facet Konrad L M Rudolph
Bianca M Schmitt
Diego Villar
Robert J White
John C Marioni
Claudia Kutter
Duncan T Odom
author_sort Konrad L M Rudolph
collection DOAJ
description Whether codon usage fine-tunes mRNA translation in mammals remains controversial, with recent papers suggesting that production of proteins in specific Gene Ontological (GO) pathways can be regulated by actively modifying the codon and anticodon pools in different cellular conditions. In this work, we compared the sequence content of genes in specific GO categories with the exonic genome background. Although a substantial fraction of variability in codon usage could be explained by random sampling, almost half of GO sets showed more variability in codon usage than expected by chance. Nevertheless, by quantifying translational efficiency in healthy and cancerous tissues in human and mouse, we demonstrated that a given tRNA pool can equally well translate many different sets of mRNAs, irrespective of their cell-type specificity. This disconnect between variations in codon usage and the stability of translational efficiency is best explained by differences in GC content between gene sets. GC variation across the mammalian genome is most likely a result of the interplay between genome repair and gene duplication mechanisms, rather than selective pressures caused by codon-driven translational rates. Consequently, codon usage differences in mammalian transcriptomes are most easily explained by well-understood mutational biases acting on the underlying genome.
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institution OA Journals
issn 1553-7390
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language English
publishDate 2016-05-01
publisher Public Library of Science (PLoS)
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series PLoS Genetics
spelling doaj-art-779b25bbe2bb4d289cd3281bdcc0c1842025-08-20T02:31:59ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042016-05-01125e100602410.1371/journal.pgen.1006024Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.Konrad L M RudolphBianca M SchmittDiego VillarRobert J WhiteJohn C MarioniClaudia KutterDuncan T OdomWhether codon usage fine-tunes mRNA translation in mammals remains controversial, with recent papers suggesting that production of proteins in specific Gene Ontological (GO) pathways can be regulated by actively modifying the codon and anticodon pools in different cellular conditions. In this work, we compared the sequence content of genes in specific GO categories with the exonic genome background. Although a substantial fraction of variability in codon usage could be explained by random sampling, almost half of GO sets showed more variability in codon usage than expected by chance. Nevertheless, by quantifying translational efficiency in healthy and cancerous tissues in human and mouse, we demonstrated that a given tRNA pool can equally well translate many different sets of mRNAs, irrespective of their cell-type specificity. This disconnect between variations in codon usage and the stability of translational efficiency is best explained by differences in GC content between gene sets. GC variation across the mammalian genome is most likely a result of the interplay between genome repair and gene duplication mechanisms, rather than selective pressures caused by codon-driven translational rates. Consequently, codon usage differences in mammalian transcriptomes are most easily explained by well-understood mutational biases acting on the underlying genome.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1006024&type=printable
spellingShingle Konrad L M Rudolph
Bianca M Schmitt
Diego Villar
Robert J White
John C Marioni
Claudia Kutter
Duncan T Odom
Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.
PLoS Genetics
title Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.
title_full Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.
title_fullStr Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.
title_full_unstemmed Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.
title_short Codon-Driven Translational Efficiency Is Stable across Diverse Mammalian Cell States.
title_sort codon driven translational efficiency is stable across diverse mammalian cell states
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1006024&type=printable
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