H3K23me1 is an evolutionarily conserved histone modification associated with CG DNA methylation in Arabidopsis
Summary Amino‐terminal tails of histones are targets for diverse post‐translational modifications whose combinatorial action may constitute a code that will be read and interpreted by cellular proteins to define particular transcriptional states. Here, we describe monomethylation of histone H3 lysin...
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| Veröffentlicht in: | The Plant journal : for cell and molecular biology 2017-04, Vol.90 (2), p.293-303 |
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| creator | Trejo‐Arellano, Minerva S. Mahrez, Walid Nakamura, Miyuki Moreno‐Romero, Jordi Nanni, Paolo Köhler, Claudia Hennig, Lars |
| description | Summary
Amino‐terminal tails of histones are targets for diverse post‐translational modifications whose combinatorial action may constitute a code that will be read and interpreted by cellular proteins to define particular transcriptional states. Here, we describe monomethylation of histone H3 lysine 23 (H3K23me1) as a histone modification not previously described in plants. H3K23me1 is an evolutionarily conserved mark in diverse species of flowering plants. Chromatin immunoprecipitation followed by high‐throughput sequencing in Arabidopsis thaliana showed that H3K23me1 was highly enriched in pericentromeric regions and depleted from chromosome arms. In transposable elements it co‐localized with CG, CHG and CHH DNA methylation as well as with the heterochromatic histone mark H3K9me2. Transposable elements are often rich in H3K23me1 but different families vary in their enrichment: LTR‐Gypsy elements are most enriched and RC/Helitron elements are least enriched. The histone methyltransferase KRYPTONITE and normal DNA methylation were required for normal levels of H3K23me1 on transposable elements. Immunostaining experiments confirmed the pericentromeric localization and also showed mild enrichment in less condensed regions. Accordingly, gene bodies of protein‐coding genes had intermediate H3K23me1 levels, which coexisted with CG DNA methylation. Enrichment of H3K23me1 along gene bodies did not correlate with transcription levels. Together, this work establishes H3K23me1 as a so far undescribed component of the plant histone code.
Significance Statement
Understanding the epigenetic regulation of gene expression requires thorough characterization of chromatin components. Here we used high‐sensitivity mass spectrometry to search for additional post‐translational histone modifications and thereby identified H3K23me1, which is highly enriched in heterochromatin but also found at some euchromatic coding genes. This mark is conserved in gymnosperms and angiosperms. |
| doi_str_mv | 10.1111/tpj.13489 |
| format | Article |
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Amino‐terminal tails of histones are targets for diverse post‐translational modifications whose combinatorial action may constitute a code that will be read and interpreted by cellular proteins to define particular transcriptional states. Here, we describe monomethylation of histone H3 lysine 23 (H3K23me1) as a histone modification not previously described in plants. H3K23me1 is an evolutionarily conserved mark in diverse species of flowering plants. Chromatin immunoprecipitation followed by high‐throughput sequencing in Arabidopsis thaliana showed that H3K23me1 was highly enriched in pericentromeric regions and depleted from chromosome arms. In transposable elements it co‐localized with CG, CHG and CHH DNA methylation as well as with the heterochromatic histone mark H3K9me2. Transposable elements are often rich in H3K23me1 but different families vary in their enrichment: LTR‐Gypsy elements are most enriched and RC/Helitron elements are least enriched. The histone methyltransferase KRYPTONITE and normal DNA methylation were required for normal levels of H3K23me1 on transposable elements. Immunostaining experiments confirmed the pericentromeric localization and also showed mild enrichment in less condensed regions. Accordingly, gene bodies of protein‐coding genes had intermediate H3K23me1 levels, which coexisted with CG DNA methylation. Enrichment of H3K23me1 along gene bodies did not correlate with transcription levels. Together, this work establishes H3K23me1 as a so far undescribed component of the plant histone code.
Significance Statement
Understanding the epigenetic regulation of gene expression requires thorough characterization of chromatin components. Here we used high‐sensitivity mass spectrometry to search for additional post‐translational histone modifications and thereby identified H3K23me1, which is highly enriched in heterochromatin but also found at some euchromatic coding genes. This mark is conserved in gymnosperms and angiosperms.</description><identifier>ISSN: 0960-7412</identifier><identifier>ISSN: 1365-313X</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.13489</identifier><identifier>PMID: 28182313</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Botanik ; Botany ; ChIP‐seq ; Chromatin ; Deoxyribonucleic acid ; DNA ; DNA methylation ; DNA Methylation - genetics ; DNA Methylation - physiology ; Epigenesis, Genetic - genetics ; epigenetics ; Flowering plants ; gene body methylation ; Gene expression ; Gene Expression Regulation, Plant - genetics ; Gene Expression Regulation, Plant - physiology ; heterochromatin ; Heterochromatin - genetics ; histone post‐translational modifications ; Histones - genetics ; Histones - metabolism ; Mass spectrometry ; Protein Processing, Post-Translational - genetics ; Protein Processing, Post-Translational - physiology ; Species diversity</subject><ispartof>The Plant journal : for cell and molecular biology, 2017-04, Vol.90 (2), p.293-303</ispartof><rights>2017 The Authors The Plant Journal © 2017 John Wiley & Sons Ltd</rights><rights>2017 The Authors The Plant Journal © 2017 John Wiley & Sons Ltd.</rights><rights>Copyright © 2017 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4599-1443ee114ada3c44795c2c121171f9de26dd8ed439cf5f4e165ca288b93aa8853</citedby><cites>FETCH-LOGICAL-c4599-1443ee114ada3c44795c2c121171f9de26dd8ed439cf5f4e165ca288b93aa8853</cites><orcidid>0000-0002-1982-3475</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.13489$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.13489$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28182313$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://res.slu.se/id/publ/84359$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Trejo‐Arellano, Minerva S.</creatorcontrib><creatorcontrib>Mahrez, Walid</creatorcontrib><creatorcontrib>Nakamura, Miyuki</creatorcontrib><creatorcontrib>Moreno‐Romero, Jordi</creatorcontrib><creatorcontrib>Nanni, Paolo</creatorcontrib><creatorcontrib>Köhler, Claudia</creatorcontrib><creatorcontrib>Hennig, Lars</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><title>H3K23me1 is an evolutionarily conserved histone modification associated with CG DNA methylation in Arabidopsis</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Amino‐terminal tails of histones are targets for diverse post‐translational modifications whose combinatorial action may constitute a code that will be read and interpreted by cellular proteins to define particular transcriptional states. Here, we describe monomethylation of histone H3 lysine 23 (H3K23me1) as a histone modification not previously described in plants. H3K23me1 is an evolutionarily conserved mark in diverse species of flowering plants. Chromatin immunoprecipitation followed by high‐throughput sequencing in Arabidopsis thaliana showed that H3K23me1 was highly enriched in pericentromeric regions and depleted from chromosome arms. In transposable elements it co‐localized with CG, CHG and CHH DNA methylation as well as with the heterochromatic histone mark H3K9me2. Transposable elements are often rich in H3K23me1 but different families vary in their enrichment: LTR‐Gypsy elements are most enriched and RC/Helitron elements are least enriched. The histone methyltransferase KRYPTONITE and normal DNA methylation were required for normal levels of H3K23me1 on transposable elements. Immunostaining experiments confirmed the pericentromeric localization and also showed mild enrichment in less condensed regions. Accordingly, gene bodies of protein‐coding genes had intermediate H3K23me1 levels, which coexisted with CG DNA methylation. Enrichment of H3K23me1 along gene bodies did not correlate with transcription levels. Together, this work establishes H3K23me1 as a so far undescribed component of the plant histone code.
Significance Statement
Understanding the epigenetic regulation of gene expression requires thorough characterization of chromatin components. Here we used high‐sensitivity mass spectrometry to search for additional post‐translational histone modifications and thereby identified H3K23me1, which is highly enriched in heterochromatin but also found at some euchromatic coding genes. This mark is conserved in gymnosperms and angiosperms.</description><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Botanik</subject><subject>Botany</subject><subject>ChIP‐seq</subject><subject>Chromatin</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>DNA Methylation - genetics</subject><subject>DNA Methylation - physiology</subject><subject>Epigenesis, Genetic - genetics</subject><subject>epigenetics</subject><subject>Flowering plants</subject><subject>gene body methylation</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>Gene Expression Regulation, Plant - physiology</subject><subject>heterochromatin</subject><subject>Heterochromatin - genetics</subject><subject>histone post‐translational modifications</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>Mass spectrometry</subject><subject>Protein Processing, Post-Translational - genetics</subject><subject>Protein Processing, Post-Translational - physiology</subject><subject>Species diversity</subject><issn>0960-7412</issn><issn>1365-313X</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqN0cFu1DAQBmALgeh24cALIEtc6CFtxnYS-7haoAUq4FAkbpbjTLReJXGwk6727fGS0gMSEr7MwZ9-e_QT8gryS0jnahr3l8CFVE_ICnhZZBz4j6dklasyzyoB7Iycx7jPc6h4KZ6TMyZBsoRWZLjhnxnvEaiL1AwU7303T84PJrjuSK0fIoZ7bOjOxckPSHvfuNZZczLUxOitM1O6P7hpR7fX9N2XDe1x2h27hbiBboKpXePH6OIL8qw1XcSXD3NNvn94f7e9yW6_Xn_cbm4zKwqlMhCCIwII0xhuhahUYZkFBlBBqxpkZdNIbARXti1agVAW1jApa8WNkbLga5ItufGA41zrMbjehKP2xunYzbUJp6Ejail4oZJ_u_gx-J8zxkn3LlrsOjOgn6MGqUBWJWfsP2hZlqpkRZ7om7_o3s9hSIsnJYXIWZ6eX5OLRdngYwzYPv4Wcn3qV6d-9e9-k339kDjXPTaP8k-hCVwt4OA6PP47Sd99-7RE_gJGtK8j</recordid><startdate>201704</startdate><enddate>201704</enddate><creator>Trejo‐Arellano, Minerva S.</creator><creator>Mahrez, Walid</creator><creator>Nakamura, Miyuki</creator><creator>Moreno‐Romero, Jordi</creator><creator>Nanni, Paolo</creator><creator>Köhler, Claudia</creator><creator>Hennig, Lars</creator><general>Blackwell Publishing Ltd</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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>ADTPV</scope><scope>AOWAS</scope><orcidid>https://orcid.org/0000-0002-1982-3475</orcidid></search><sort><creationdate>201704</creationdate><title>H3K23me1 is an evolutionarily conserved histone modification associated with CG DNA methylation in Arabidopsis</title><author>Trejo‐Arellano, Minerva S. ; Mahrez, Walid ; Nakamura, Miyuki ; Moreno‐Romero, Jordi ; Nanni, Paolo ; Köhler, Claudia ; Hennig, Lars</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4599-1443ee114ada3c44795c2c121171f9de26dd8ed439cf5f4e165ca288b93aa8853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Botanik</topic><topic>Botany</topic><topic>ChIP‐seq</topic><topic>Chromatin</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>DNA Methylation - genetics</topic><topic>DNA Methylation - physiology</topic><topic>Epigenesis, Genetic - genetics</topic><topic>epigenetics</topic><topic>Flowering plants</topic><topic>gene body methylation</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>Gene Expression Regulation, Plant - physiology</topic><topic>heterochromatin</topic><topic>Heterochromatin - genetics</topic><topic>histone post‐translational modifications</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>Mass spectrometry</topic><topic>Protein Processing, Post-Translational - genetics</topic><topic>Protein Processing, Post-Translational - physiology</topic><topic>Species diversity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Trejo‐Arellano, Minerva S.</creatorcontrib><creatorcontrib>Mahrez, Walid</creatorcontrib><creatorcontrib>Nakamura, Miyuki</creatorcontrib><creatorcontrib>Moreno‐Romero, Jordi</creatorcontrib><creatorcontrib>Nanni, Paolo</creatorcontrib><creatorcontrib>Köhler, Claudia</creatorcontrib><creatorcontrib>Hennig, Lars</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>SwePub</collection><collection>SwePub Articles</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Trejo‐Arellano, Minerva S.</au><au>Mahrez, Walid</au><au>Nakamura, Miyuki</au><au>Moreno‐Romero, Jordi</au><au>Nanni, Paolo</au><au>Köhler, Claudia</au><au>Hennig, Lars</au><aucorp>Sveriges lantbruksuniversitet</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>H3K23me1 is an evolutionarily conserved histone modification associated with CG DNA methylation in Arabidopsis</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2017-04</date><risdate>2017</risdate><volume>90</volume><issue>2</issue><spage>293</spage><epage>303</epage><pages>293-303</pages><issn>0960-7412</issn><issn>1365-313X</issn><eissn>1365-313X</eissn><abstract>Summary
Amino‐terminal tails of histones are targets for diverse post‐translational modifications whose combinatorial action may constitute a code that will be read and interpreted by cellular proteins to define particular transcriptional states. Here, we describe monomethylation of histone H3 lysine 23 (H3K23me1) as a histone modification not previously described in plants. H3K23me1 is an evolutionarily conserved mark in diverse species of flowering plants. Chromatin immunoprecipitation followed by high‐throughput sequencing in Arabidopsis thaliana showed that H3K23me1 was highly enriched in pericentromeric regions and depleted from chromosome arms. In transposable elements it co‐localized with CG, CHG and CHH DNA methylation as well as with the heterochromatic histone mark H3K9me2. Transposable elements are often rich in H3K23me1 but different families vary in their enrichment: LTR‐Gypsy elements are most enriched and RC/Helitron elements are least enriched. The histone methyltransferase KRYPTONITE and normal DNA methylation were required for normal levels of H3K23me1 on transposable elements. Immunostaining experiments confirmed the pericentromeric localization and also showed mild enrichment in less condensed regions. Accordingly, gene bodies of protein‐coding genes had intermediate H3K23me1 levels, which coexisted with CG DNA methylation. Enrichment of H3K23me1 along gene bodies did not correlate with transcription levels. Together, this work establishes H3K23me1 as a so far undescribed component of the plant histone code.
Significance Statement
Understanding the epigenetic regulation of gene expression requires thorough characterization of chromatin components. Here we used high‐sensitivity mass spectrometry to search for additional post‐translational histone modifications and thereby identified H3K23me1, which is highly enriched in heterochromatin but also found at some euchromatic coding genes. This mark is conserved in gymnosperms and angiosperms.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>28182313</pmid><doi>10.1111/tpj.13489</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-1982-3475</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Botanik Botany ChIP‐seq Chromatin Deoxyribonucleic acid DNA DNA methylation DNA Methylation - genetics DNA Methylation - physiology Epigenesis, Genetic - genetics epigenetics Flowering plants gene body methylation Gene expression Gene Expression Regulation, Plant - genetics Gene Expression Regulation, Plant - physiology heterochromatin Heterochromatin - genetics histone post‐translational modifications Histones - genetics Histones - metabolism Mass spectrometry Protein Processing, Post-Translational - genetics Protein Processing, Post-Translational - physiology Species diversity |
| title | H3K23me1 is an evolutionarily conserved histone modification associated with CG DNA methylation in Arabidopsis |
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