Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification
Histone modifications are critical for the regulation of gene expression, cell type specification, and differentiation. However, evolutionary patterns of key modifications that regulate gene expression in differentiating organisms have not been examined. Here we mapped the genomic locations of the r...
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Veröffentlicht in: | Genome research 2014-07, Vol.24 (7), p.1115-1124 |
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description | Histone modifications are critical for the regulation of gene expression, cell type specification, and differentiation. However, evolutionary patterns of key modifications that regulate gene expression in differentiating organisms have not been examined. Here we mapped the genomic locations of the repressive mark histone 3 lysine 27 trimethylation (H3K27me3) in four species of Drosophila, and compared these patterns to those in C. elegans. We found that patterns of H3K27me3 are highly conserved across species, but conservation is substantially weaker among duplicated genes. We further discovered that retropositions are associated with greater evolutionary changes in H3K27me3 and gene expression than tandem duplications, indicating that local chromatin constraints influence duplicated gene evolution. These changes are also associated with concomitant evolution of gene expression. Our findings reveal the strong conservation of genomic architecture governed by an epigenetic mark across distantly related species and the importance of gene duplication in generating novel H3K27me3 profiles. |
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However, evolutionary patterns of key modifications that regulate gene expression in differentiating organisms have not been examined. Here we mapped the genomic locations of the repressive mark histone 3 lysine 27 trimethylation (H3K27me3) in four species of Drosophila, and compared these patterns to those in C. elegans. We found that patterns of H3K27me3 are highly conserved across species, but conservation is substantially weaker among duplicated genes. We further discovered that retropositions are associated with greater evolutionary changes in H3K27me3 and gene expression than tandem duplications, indicating that local chromatin constraints influence duplicated gene evolution. These changes are also associated with concomitant evolution of gene expression. Our findings reveal the strong conservation of genomic architecture governed by an epigenetic mark across distantly related species and the importance of gene duplication in generating novel H3K27me3 profiles.</description><identifier>ISSN: 1088-9051</identifier><identifier>EISSN: 1549-5469</identifier><identifier>DOI: 10.1101/gr.162008.113</identifier><identifier>PMID: 24985914</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Animals ; BASIC BIOLOGICAL SCIENCES ; Biochemistry & Molecular Biology ; Biological Evolution ; Biotechnology & Applied Microbiology ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - metabolism ; Chromatin - genetics ; Chromatin - metabolism ; Drosophila ; Drosophila - genetics ; Drosophila - metabolism ; Evolution, Molecular ; Gene Dosage ; Gene Duplication ; Gene Expression Regulation, Developmental ; Genetics & Heredity ; Histones - metabolism ; Life Sciences ; Translocation, Genetic</subject><ispartof>Genome research, 2014-07, Vol.24 (7), p.1115-1124</ispartof><rights>2014 Arthur et al.; Published by Cold Spring Harbor Laboratory Press.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c481t-4a7aa2d9de4345b5db277f235bc41fdb9d4584e12403cb06cd8ff9535566c4bf3</citedby><cites>FETCH-LOGICAL-c481t-4a7aa2d9de4345b5db277f235bc41fdb9d4584e12403cb06cd8ff9535566c4bf3</cites><orcidid>0000-0001-9727-3416</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4079967/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4079967/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27922,27923,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24985914$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01837273$$DView record in HAL$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1625628$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Arthur, Robert K</creatorcontrib><creatorcontrib>Ma, Lijia</creatorcontrib><creatorcontrib>Slattery, Matthew</creatorcontrib><creatorcontrib>Spokony, Rebecca F</creatorcontrib><creatorcontrib>Ostapenko, Alexander</creatorcontrib><creatorcontrib>Nègre, Nicolas</creatorcontrib><creatorcontrib>White, Kevin P</creatorcontrib><creatorcontrib>Univ. of Chicago, IL (United States)</creatorcontrib><title>Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification</title><title>Genome research</title><addtitle>Genome Res</addtitle><description>Histone modifications are critical for the regulation of gene expression, cell type specification, and differentiation. However, evolutionary patterns of key modifications that regulate gene expression in differentiating organisms have not been examined. Here we mapped the genomic locations of the repressive mark histone 3 lysine 27 trimethylation (H3K27me3) in four species of Drosophila, and compared these patterns to those in C. elegans. We found that patterns of H3K27me3 are highly conserved across species, but conservation is substantially weaker among duplicated genes. We further discovered that retropositions are associated with greater evolutionary changes in H3K27me3 and gene expression than tandem duplications, indicating that local chromatin constraints influence duplicated gene evolution. These changes are also associated with concomitant evolution of gene expression. Our findings reveal the strong conservation of genomic architecture governed by an epigenetic mark across distantly related species and the importance of gene duplication in generating novel H3K27me3 profiles.</description><subject>Animals</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biochemistry & Molecular Biology</subject><subject>Biological Evolution</subject><subject>Biotechnology & Applied Microbiology</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Chromatin - genetics</subject><subject>Chromatin - metabolism</subject><subject>Drosophila</subject><subject>Drosophila - genetics</subject><subject>Drosophila - metabolism</subject><subject>Evolution, Molecular</subject><subject>Gene Dosage</subject><subject>Gene Duplication</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genetics & Heredity</subject><subject>Histones - metabolism</subject><subject>Life Sciences</subject><subject>Translocation, Genetic</subject><issn>1088-9051</issn><issn>1549-5469</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdksFu1DAQQCMEoqVw5IoiTnBIsWM7ti9IVVVYxEq9wNly7MmuIbGD7azgA_jvJs2yoj3ZM35-mtFMUbzG6BJjhD_s4iVuaoTEHJInxTlmVFaMNvLpfEdCVBIxfFa8SOkHQohQIZ4XZzWVgklMz4u_N4fQT9kFX4au3JCvNR-AVIOOP8GWZh_DoLPzpUtl7_ySy6HcgYcSfo8RUlp-wsmh_T0w6pwh-rQ472E7jb0z-sRYd4CYXHfMvSyedbpP8Op4XhTfP918u95U29vPX66vtpWhAueKaq51baUFSihrmW1rzruasNZQ3NlWWsoEBVxTREyLGmNF10lGGGsaQ9uOXBQfV-84tQNYAz5H3asxurnhPypopx6-eLdXu3BQFHEpGz4L3q6CkLJTybgMZm-C92CymufAmlrM0PsV2j9yb662askhLAivOTngmX13rCiGXxOkrAaXDPS99hCmpDBjuCGMMzKj1YqaGFKK0J3cGKllF9QuqnUX5nDh3_zf7In-N3xyBwpisYI</recordid><startdate>20140701</startdate><enddate>20140701</enddate><creator>Arthur, Robert K</creator><creator>Ma, Lijia</creator><creator>Slattery, Matthew</creator><creator>Spokony, Rebecca F</creator><creator>Ostapenko, Alexander</creator><creator>Nègre, Nicolas</creator><creator>White, Kevin P</creator><general>Cold Spring Harbor Laboratory Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>1XC</scope><scope>VOOES</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9727-3416</orcidid></search><sort><creationdate>20140701</creationdate><title>Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification</title><author>Arthur, Robert K ; Ma, Lijia ; Slattery, Matthew ; Spokony, Rebecca F ; Ostapenko, Alexander ; Nègre, Nicolas ; White, Kevin P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c481t-4a7aa2d9de4345b5db277f235bc41fdb9d4584e12403cb06cd8ff9535566c4bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biochemistry & Molecular Biology</topic><topic>Biological Evolution</topic><topic>Biotechnology & Applied Microbiology</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Caenorhabditis elegans - metabolism</topic><topic>Chromatin - genetics</topic><topic>Chromatin - metabolism</topic><topic>Drosophila</topic><topic>Drosophila - genetics</topic><topic>Drosophila - metabolism</topic><topic>Evolution, Molecular</topic><topic>Gene Dosage</topic><topic>Gene Duplication</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Genetics & Heredity</topic><topic>Histones - metabolism</topic><topic>Life Sciences</topic><topic>Translocation, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Arthur, Robert K</creatorcontrib><creatorcontrib>Ma, Lijia</creatorcontrib><creatorcontrib>Slattery, Matthew</creatorcontrib><creatorcontrib>Spokony, Rebecca F</creatorcontrib><creatorcontrib>Ostapenko, Alexander</creatorcontrib><creatorcontrib>Nègre, Nicolas</creatorcontrib><creatorcontrib>White, Kevin P</creatorcontrib><creatorcontrib>Univ. of Chicago, IL (United States)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Arthur, Robert K</au><au>Ma, Lijia</au><au>Slattery, Matthew</au><au>Spokony, Rebecca F</au><au>Ostapenko, Alexander</au><au>Nègre, Nicolas</au><au>White, Kevin P</au><aucorp>Univ. of Chicago, IL (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification</atitle><jtitle>Genome research</jtitle><addtitle>Genome Res</addtitle><date>2014-07-01</date><risdate>2014</risdate><volume>24</volume><issue>7</issue><spage>1115</spage><epage>1124</epage><pages>1115-1124</pages><issn>1088-9051</issn><eissn>1549-5469</eissn><abstract>Histone modifications are critical for the regulation of gene expression, cell type specification, and differentiation. However, evolutionary patterns of key modifications that regulate gene expression in differentiating organisms have not been examined. Here we mapped the genomic locations of the repressive mark histone 3 lysine 27 trimethylation (H3K27me3) in four species of Drosophila, and compared these patterns to those in C. elegans. We found that patterns of H3K27me3 are highly conserved across species, but conservation is substantially weaker among duplicated genes. We further discovered that retropositions are associated with greater evolutionary changes in H3K27me3 and gene expression than tandem duplications, indicating that local chromatin constraints influence duplicated gene evolution. These changes are also associated with concomitant evolution of gene expression. Our findings reveal the strong conservation of genomic architecture governed by an epigenetic mark across distantly related species and the importance of gene duplication in generating novel H3K27me3 profiles.</abstract><cop>United States</cop><pub>Cold Spring Harbor Laboratory Press</pub><pmid>24985914</pmid><doi>10.1101/gr.162008.113</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-9727-3416</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals BASIC BIOLOGICAL SCIENCES Biochemistry & Molecular Biology Biological Evolution Biotechnology & Applied Microbiology Caenorhabditis elegans - genetics Caenorhabditis elegans - metabolism Chromatin - genetics Chromatin - metabolism Drosophila Drosophila - genetics Drosophila - metabolism Evolution, Molecular Gene Dosage Gene Duplication Gene Expression Regulation, Developmental Genetics & Heredity Histones - metabolism Life Sciences Translocation, Genetic |
title | Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification |
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