Enhancer evolution across 20 mammalian species

Diego Villar; Camille Berthelot; Sarah Aldridge; Tim F. Rayner; Margus Lukk; Miguel Pignatelli; Thomas J. Park; Robert Deaville; Jonathan T. Erichsen; Anna J. Jasinska; James M. A. Turner; Mads Frost Bertelsen; Elizabeth P. Murchison; Paul Flicek; Duncan T. Odom

doi:10.1016/j.cell.2015.01.006

Enhancer evolution across 20 mammalian species

Diego Villar, Camille Berthelot, Sarah Aldridge, Tim F. Rayner, Margus Lukk, Miguel Pignatelli, Thomas J. Park, Robert Deaville, Jonathan T. Erichsen, Anna J. Jasinska, James M. A. Turner, Mads Frost Bertelsen, Elizabeth P. Murchison, Paul Flicek, Duncan T. Odom

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Abstract

The mammalian radiation has corresponded with rapid changes in noncoding regions of the genome, but we lack a comprehensive understanding of regulatory evolution in mammals. Here, we track the evolution of promoters and enhancers active in liver across 20 mammalian species from six diverse orders by profiling genomic enrichment of H3K27 acetylation and H3K4 trimethylation. We report that rapid evolution of enhancers is a universal feature of mammalian genomes. Most of the recently evolved enhancers arise from ancestral DNA exaptation, rather than lineage-specific expansions of repeat elements. In contrast, almost all liver promoters are partially or fully conserved across these species. Our data further reveal that recently evolved enhancers can be associated with genes under positive selection, demonstrating the power of this approach for annotating regulatory adaptations in genomic sequences. These results provide important insight into the functional genetics underpinning mammalian regulatory evolution.

Original language	English
Journal	Cell
Volume	160
Issue number	3
Pages (from-to)	554-566
Number of pages	13
ISSN	0092-8674
DOIs	https://doi.org/10.1016/j.cell.2015.01.006
Publication status	Published - 29 Jan 2015

Keywords

Animals
Enhancer Elements, Genetic
Evolution, Molecular
Histone Code
Humans
Liver
Mammals
Promoter Regions, Genetic
Transcription Factors

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title = "Enhancer evolution across 20 mammalian species",

abstract = "The mammalian radiation has corresponded with rapid changes in noncoding regions of the genome, but we lack a comprehensive understanding of regulatory evolution in mammals. Here, we track the evolution of promoters and enhancers active in liver across 20 mammalian species from six diverse orders by profiling genomic enrichment of H3K27 acetylation and H3K4 trimethylation. We report that rapid evolution of enhancers is a universal feature of mammalian genomes. Most of the recently evolved enhancers arise from ancestral DNA exaptation, rather than lineage-specific expansions of repeat elements. In contrast, almost all liver promoters are partially or fully conserved across these species. Our data further reveal that recently evolved enhancers can be associated with genes under positive selection, demonstrating the power of this approach for annotating regulatory adaptations in genomic sequences. These results provide important insight into the functional genetics underpinning mammalian regulatory evolution.",

keywords = "Animals, Enhancer Elements, Genetic, Evolution, Molecular, Histone Code, Humans, Liver, Mammals, Promoter Regions, Genetic, Transcription Factors",

author = "Diego Villar and Camille Berthelot and Sarah Aldridge and Rayner, {Tim F.} and Margus Lukk and Miguel Pignatelli and Park, {Thomas J.} and Robert Deaville and Erichsen, {Jonathan T.} and Jasinska, {Anna J.} and Turner, {James M. A.} and Bertelsen, {Mads Frost} and Murchison, {Elizabeth P.} and Paul Flicek and Odom, {Duncan T.}",

year = "2015",

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doi = "10.1016/j.cell.2015.01.006",

language = "English",

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journal = "Cell",

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T1 - Enhancer evolution across 20 mammalian species

AU - Villar, Diego

AU - Berthelot, Camille

AU - Aldridge, Sarah

AU - Rayner, Tim F.

AU - Lukk, Margus

AU - Pignatelli, Miguel

AU - Park, Thomas J.

AU - Deaville, Robert

AU - Erichsen, Jonathan T.

AU - Jasinska, Anna J.

AU - Turner, James M. A.

AU - Bertelsen, Mads Frost

AU - Murchison, Elizabeth P.

AU - Flicek, Paul

AU - Odom, Duncan T.

PY - 2015/1/29

Y1 - 2015/1/29

N2 - The mammalian radiation has corresponded with rapid changes in noncoding regions of the genome, but we lack a comprehensive understanding of regulatory evolution in mammals. Here, we track the evolution of promoters and enhancers active in liver across 20 mammalian species from six diverse orders by profiling genomic enrichment of H3K27 acetylation and H3K4 trimethylation. We report that rapid evolution of enhancers is a universal feature of mammalian genomes. Most of the recently evolved enhancers arise from ancestral DNA exaptation, rather than lineage-specific expansions of repeat elements. In contrast, almost all liver promoters are partially or fully conserved across these species. Our data further reveal that recently evolved enhancers can be associated with genes under positive selection, demonstrating the power of this approach for annotating regulatory adaptations in genomic sequences. These results provide important insight into the functional genetics underpinning mammalian regulatory evolution.

AB - The mammalian radiation has corresponded with rapid changes in noncoding regions of the genome, but we lack a comprehensive understanding of regulatory evolution in mammals. Here, we track the evolution of promoters and enhancers active in liver across 20 mammalian species from six diverse orders by profiling genomic enrichment of H3K27 acetylation and H3K4 trimethylation. We report that rapid evolution of enhancers is a universal feature of mammalian genomes. Most of the recently evolved enhancers arise from ancestral DNA exaptation, rather than lineage-specific expansions of repeat elements. In contrast, almost all liver promoters are partially or fully conserved across these species. Our data further reveal that recently evolved enhancers can be associated with genes under positive selection, demonstrating the power of this approach for annotating regulatory adaptations in genomic sequences. These results provide important insight into the functional genetics underpinning mammalian regulatory evolution.

KW - Animals

KW - Enhancer Elements, Genetic

KW - Evolution, Molecular

KW - Histone Code

KW - Humans

KW - Liver

KW - Mammals

KW - Promoter Regions, Genetic

KW - Transcription Factors

U2 - 10.1016/j.cell.2015.01.006

DO - 10.1016/j.cell.2015.01.006

M3 - Journal article

C2 - 25635462

SN - 0092-8674

VL - 160

SP - 554

EP - 566

JO - Cell

JF - Cell

IS - 3

ER -

Enhancer evolution across 20 mammalian species

Abstract

Keywords

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