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Mutation bias shapes gene evolution in Arabidopsis thaliana

View ORCID ProfileJ. Grey Monroe, Thanvi Srikant, Pablo Carbonell-Bejerano, View ORCID ProfileMoises Exposito-Alonso, Mao-Lun Weng, Matthew T. Rutter, Charles B. Fenster, Detlef Weigel
doi: https://doi.org/10.1101/2020.06.17.156752
J. Grey Monroe
1Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany
2Department of Plant Sciences, University of California Davis, Davis, CA 95616, USA
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  • ORCID record for J. Grey Monroe
  • For correspondence: greymonroe@gmail.com weigel@weigelworld.org
Thanvi Srikant
1Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany
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Pablo Carbonell-Bejerano
1Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany
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Moises Exposito-Alonso
3Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA
4Department of Biology, Stanford University, Stanford, CA 94305, USA
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Mao-Lun Weng
5Department of Biology, Westfield State University, Westfield, MA 01086, USA
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Matthew T. Rutter
6Department of Biology, College of Charleston, SC 29401, USA
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Charles B. Fenster
7Department of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USA
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Detlef Weigel
1Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany
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  • For correspondence: greymonroe@gmail.com weigel@weigelworld.org
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Abstract

Classical evolutionary theory maintains that mutation rate variation between genes should be random with respect to fitness 1–4 and evolutionary optimization of genic mutation rates remains controversial 3,5. However, it has now become known that cytogenetic (DNA sequence + epigenomic) features influence local mutation probabilities 6, which is predicted by more recent theory to be a prerequisite for beneficial mutation rates between different classes of genes to readily evolve 7. To test this possibility, we used de novo mutations in Arabidopsis thaliana to create a high resolution predictive model of mutation rates as a function of cytogenetic features across the genome. As expected, mutation rates are significantly predicted by features such as GC content, histone modifications, and chromatin accessibility. Deeper analyses of predicted mutation rates reveal effects of introns and untranslated exon regions in distancing coding sequences from mutational hotspots at the start and end of transcribed regions in A. thaliana. Finally, predicted coding region mutation rates are significantly lower in genes where mutations are more likely to be deleterious, supported by numerous estimates of evolutionary and functional constraint. These findings contradict neutral expectations that mutation probabilities are independent of fitness consequences. Instead they are consistent with the evolution of lower mutation rates in functionally constrained loci due to cytogenetic features, with important implications for evolutionary biology8.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted June 18, 2020.
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Mutation bias shapes gene evolution in Arabidopsis thaliana
J. Grey Monroe, Thanvi Srikant, Pablo Carbonell-Bejerano, Moises Exposito-Alonso, Mao-Lun Weng, Matthew T. Rutter, Charles B. Fenster, Detlef Weigel
bioRxiv 2020.06.17.156752; doi: https://doi.org/10.1101/2020.06.17.156752
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Mutation bias shapes gene evolution in Arabidopsis thaliana
J. Grey Monroe, Thanvi Srikant, Pablo Carbonell-Bejerano, Moises Exposito-Alonso, Mao-Lun Weng, Matthew T. Rutter, Charles B. Fenster, Detlef Weigel
bioRxiv 2020.06.17.156752; doi: https://doi.org/10.1101/2020.06.17.156752

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