Genome-Wide microRNA Binding Site Variation between Extinct Wild Aurochs and Modern Cattle Identifies Candidate microRNA-Regulated Domestication Genes
The domestication of cattle from the now-extinct wild aurochs ( ) involved selection for physiological and behavioral traits, with underlying genetic factors that remain largely unknown. Non-coding microRNAs have emerged as key regulators of the spatio-temporal expression of target genes controlling...
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| Published in: | Frontiers in genetics Vol. 8; p. 3 |
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| Main Authors: | , , , , , , |
| Format: | Journal Article |
| Language: | English |
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31.01.2017
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| ISSN: | 1664-8021, 1664-8021 |
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| Abstract | The domestication of cattle from the now-extinct wild aurochs (
) involved selection for physiological and behavioral traits, with underlying genetic factors that remain largely unknown. Non-coding microRNAs have emerged as key regulators of the spatio-temporal expression of target genes controlling mammalian growth and development, including in livestock species. During the domestication process, selection of mutational changes in miRNAs and/or miRNA binding sites could have provided a mechanism to generate some of the traits that differentiate domesticated cattle from wild aurochs. To investigate this, we analyzed the open reading frame DNA sequence of 19,994 orthologous protein-coding gene pairs from extant
genomes and a single extinct
genome. We identified miRNA binding site polymorphisms in the 3' UTRs of 1,620 of these orthologous genes. These 1,620 genes with altered miRNA binding sites between the
and
lineages represent candidate domestication genes. Using a novel Score Site ratio metric we have ranked these miRNA-regulated genes according to the extent of divergence between miRNA binding site presence, frequency and copy number between the orthologous genes from
and
This provides an unbiased approach to identify cattle genes that have undergone the most changes in miRNA binding (i.e., regulation) between the wild aurochs and modern-day cattle breeds. In addition, we demonstrate that these 1,620 candidate domestication genes are enriched for roles in pigmentation, fertility, neurobiology, metabolism, immunity and production traits (including milk quality and feed efficiency). Our findings suggest that directional selection of miRNA regulatory variants was important in the domestication and subsequent artificial selection that gave rise to modern taurine cattle. |
|---|---|
| AbstractList | The domestication of cattle from the now-extinct wild aurochs (
) involved selection for physiological and behavioral traits, with underlying genetic factors that remain largely unknown. Non-coding microRNAs have emerged as key regulators of the spatio-temporal expression of target genes controlling mammalian growth and development, including in livestock species. During the domestication process, selection of mutational changes in miRNAs and/or miRNA binding sites could have provided a mechanism to generate some of the traits that differentiate domesticated cattle from wild aurochs. To investigate this, we analyzed the open reading frame DNA sequence of 19,994 orthologous protein-coding gene pairs from extant
genomes and a single extinct
genome. We identified miRNA binding site polymorphisms in the 3' UTRs of 1,620 of these orthologous genes. These 1,620 genes with altered miRNA binding sites between the
and
lineages represent candidate domestication genes. Using a novel Score Site ratio metric we have ranked these miRNA-regulated genes according to the extent of divergence between miRNA binding site presence, frequency and copy number between the orthologous genes from
and
This provides an unbiased approach to identify cattle genes that have undergone the most changes in miRNA binding (i.e., regulation) between the wild aurochs and modern-day cattle breeds. In addition, we demonstrate that these 1,620 candidate domestication genes are enriched for roles in pigmentation, fertility, neurobiology, metabolism, immunity and production traits (including milk quality and feed efficiency). Our findings suggest that directional selection of miRNA regulatory variants was important in the domestication and subsequent artificial selection that gave rise to modern taurine cattle. The domestication of cattle from the now-extinct wild aurochs (Bos primigenius) involved selection for physiological and behavioral traits, with underlying genetic factors that remain largely unknown. Non-coding microRNAs have emerged as key regulators of the spatio-temporal expression of target genes controlling mammalian growth and development, including in livestock species. During the domestication process, selection of mutational changes in miRNAs and/or miRNA binding sites could have provided a mechanism to generate some of the traits that differentiate domesticated cattle from wild aurochs. To investigate this, we analyzed the open reading frame DNA sequence of 19,994 orthologous protein-coding gene pairs from extant Bos taurus genomes and a single extinct B. primigenius genome. We identified miRNA binding site polymorphisms in the 3′ UTRs of 1,620 of these orthologous genes. These 1,620 genes with altered miRNA binding sites between the B. taurus and B. primigenius lineages represent candidate domestication genes. Using a novel Score Site ratio metric we have ranked these miRNA-regulated genes according to the extent of divergence between miRNA binding site presence, frequency and copy number between the orthologous genes from B. taurus and B. primigenius. This provides an unbiased approach to identify cattle genes that have undergone the most changes in miRNA binding (i.e., regulation) between the wild aurochs and modern-day cattle breeds. In addition, we demonstrate that these 1,620 candidate domestication genes are enriched for roles in pigmentation, fertility, neurobiology, metabolism, immunity and production traits (including milk quality and feed efficiency). Our findings suggest that directional selection of miRNA regulatory variants was important in the domestication and subsequent artificial selection that gave rise to modern taurine cattle. The domestication of cattle from the now-extinct wild aurochs (Bos primigenius) involved selection for physiological and behavioral traits, with underlying genetic factors that remain largely unknown. Non-coding microRNAs have emerged as key regulators of the spatio-temporal expression of target genes controlling mammalian growth and development, including in livestock species. During the domestication process, selection of mutational changes in miRNAs and/or miRNA binding sites could have provided a mechanism to generate some of the traits that differentiate domesticated cattle from wild aurochs. To investigate this, we analyzed the open reading frame DNA sequence of 19,994 orthologous protein-coding gene pairs from extant Bos taurus genomes and a single extinct B. primigenius genome. We identified miRNA binding site polymorphisms in the 3' UTRs of 1,620 of these orthologous genes. These 1,620 genes with altered miRNA binding sites between the B. taurus and B. primigenius lineages represent candidate domestication genes. Using a novel Score Site ratio metric we have ranked these miRNA-regulated genes according to the extent of divergence between miRNA binding site presence, frequency and copy number between the orthologous genes from B. taurus and B. primigenius. This provides an unbiased approach to identify cattle genes that have undergone the most changes in miRNA binding (i.e., regulation) between the wild aurochs and modern-day cattle breeds. In addition, we demonstrate that these 1,620 candidate domestication genes are enriched for roles in pigmentation, fertility, neurobiology, metabolism, immunity and production traits (including milk quality and feed efficiency). Our findings suggest that directional selection of miRNA regulatory variants was important in the domestication and subsequent artificial selection that gave rise to modern taurine cattle.The domestication of cattle from the now-extinct wild aurochs (Bos primigenius) involved selection for physiological and behavioral traits, with underlying genetic factors that remain largely unknown. Non-coding microRNAs have emerged as key regulators of the spatio-temporal expression of target genes controlling mammalian growth and development, including in livestock species. During the domestication process, selection of mutational changes in miRNAs and/or miRNA binding sites could have provided a mechanism to generate some of the traits that differentiate domesticated cattle from wild aurochs. To investigate this, we analyzed the open reading frame DNA sequence of 19,994 orthologous protein-coding gene pairs from extant Bos taurus genomes and a single extinct B. primigenius genome. We identified miRNA binding site polymorphisms in the 3' UTRs of 1,620 of these orthologous genes. These 1,620 genes with altered miRNA binding sites between the B. taurus and B. primigenius lineages represent candidate domestication genes. Using a novel Score Site ratio metric we have ranked these miRNA-regulated genes according to the extent of divergence between miRNA binding site presence, frequency and copy number between the orthologous genes from B. taurus and B. primigenius. This provides an unbiased approach to identify cattle genes that have undergone the most changes in miRNA binding (i.e., regulation) between the wild aurochs and modern-day cattle breeds. In addition, we demonstrate that these 1,620 candidate domestication genes are enriched for roles in pigmentation, fertility, neurobiology, metabolism, immunity and production traits (including milk quality and feed efficiency). Our findings suggest that directional selection of miRNA regulatory variants was important in the domestication and subsequent artificial selection that gave rise to modern taurine cattle. |
| Author | MacHugh, David E. Park, Stephen D. E. Spillane, Charles Waters, Sinead M. Magee, David A. Braud, Martin Sonstegard, Tad S. |
| AuthorAffiliation | 2 Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin Dublin, Ireland 5 Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre, Teagasc Dunsany, Ireland 1 Genetics and Biotechnology Lab, Plant and AgriBiosciences Research Centre, School of Natural Sciences, National University of Ireland Galway, University Road Galway, Ireland 6 UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin Dublin, Ireland 3 IdentiGEN Ltd, Unit 2, Trinity Enterprise Centre Dublin, Ireland 4 Recombinetics, Inc., St. Paul MN, USA |
| AuthorAffiliation_xml | – name: 4 Recombinetics, Inc., St. Paul MN, USA – name: 1 Genetics and Biotechnology Lab, Plant and AgriBiosciences Research Centre, School of Natural Sciences, National University of Ireland Galway, University Road Galway, Ireland – name: 3 IdentiGEN Ltd, Unit 2, Trinity Enterprise Centre Dublin, Ireland – name: 6 UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin Dublin, Ireland – name: 2 Animal Genomics Laboratory, UCD School of Agriculture and Food Science, University College Dublin Dublin, Ireland – name: 5 Animal and Bioscience Research Department, Animal and Grassland Research and Innovation Centre, Teagasc Dunsany, Ireland |
| Author_xml | – sequence: 1 givenname: Martin surname: Braud fullname: Braud, Martin – sequence: 2 givenname: David A. surname: Magee fullname: Magee, David A. – sequence: 3 givenname: Stephen D. E. surname: Park fullname: Park, Stephen D. E. – sequence: 4 givenname: Tad S. surname: Sonstegard fullname: Sonstegard, Tad S. – sequence: 5 givenname: Sinead M. surname: Waters fullname: Waters, Sinead M. – sequence: 6 givenname: David E. surname: MacHugh fullname: MacHugh, David E. – sequence: 7 givenname: Charles surname: Spillane fullname: Spillane, Charles |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28197171$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2017 Braud, Magee, Park, Sonstegard, Waters, MacHugh and Spillane. 2017 Braud, Magee, Park, Sonstegard, Waters, MacHugh and Spillane |
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| Keywords | agriculture Bos primigenius domestication microRNA ancient DNA polymorphism Bos taurus evolution |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Martien Groenen, Wageningen University and Research Centre, Netherlands Reviewed by: Dan Nonneman, Agricultural Research Service (USDA), USA; Laurent Frantz, University of Oxford, UK This article was submitted to Livestock Genomics, a section of the journal Frontiers in Genetics |
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) involved selection for physiological and behavioral traits, with underlying genetic factors... The domestication of cattle from the now-extinct wild aurochs (Bos primigenius) involved selection for physiological and behavioral traits, with underlying... |
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| Title | Genome-Wide microRNA Binding Site Variation between Extinct Wild Aurochs and Modern Cattle Identifies Candidate microRNA-Regulated Domestication Genes |
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