Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas

Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Genes 2019-09, Vol.10 (9), p.695
Hauptverfasser: Fellous, Alexandre, Lefranc, Lorane, Jouaux, Aude, Goux, Didier, Favrel, Pascal, Rivière, Guillaume
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 9
container_start_page 695
container_title Genes
container_volume 10
creator Fellous, Alexandre
Lefranc, Lorane
Jouaux, Aude
Goux, Didier
Favrel, Pascal
Rivière, Guillaume
description Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster is under the strong epigenetic influence of DNA methylation, and histone-demethylase orthologues are highly expressed during . early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.
doi_str_mv 10.3390/genes10090695
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6771004</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2289571879</sourcerecordid><originalsourceid>FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</originalsourceid><addsrcrecordid>eNqFkrFv3CAUxq2qVROlGbtWSF3awSkYjGGpFF2TXKWrkqGdEcbPPiIfuIBPua1_erlcGiVZygLi-_G9p49XFO8JPqNU4i8DOIgEY4m5rF8VxxVuaMlYVb9-cj4qTmO8xXkxXGFcvy2OKKmxlKI-Lv4sbUzeAfoBab0bdbLeoRsdkjV20gkisg5d5TLo4m4KEONeX3iXgh9RNwfrBpTWWdVh3KFvsIXRTxtwCfn-XrjRxvbWoOtdTBDQIugYfUwBNBrsoOO74k2vxwinD_tJ8evy4udiWa6ur74vzlel4USkkncNbTvDhSSNFITInggKpBaVxLIirZamAcaYpIbIDgTrQAreVi2RhDSE0pPi68F3mtsNdCa3GPSopmA3OuyU11Y9V5xdq8FvFW-anDDLBp8PBusXz5bnK7W_w6y-J7cks58eigX_e4aY1MZGA-OoHfg5qoqx_GOcYfF_tBIy-4pGZvTjC_TWz8Hl1FRVM1ETxgXPVHmgTPAxBugfmyVY7adGPZuazH94Gswj_W9G6F9lTb2w</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2548514686</pqid></control><display><type>article</type><title>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</title><source>MDPI - Multidisciplinary Digital Publishing Institute</source><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><source>PubMed Central Open Access</source><creator>Fellous, Alexandre ; Lefranc, Lorane ; Jouaux, Aude ; Goux, Didier ; Favrel, Pascal ; Rivière, Guillaume</creator><creatorcontrib>Fellous, Alexandre ; Lefranc, Lorane ; Jouaux, Aude ; Goux, Didier ; Favrel, Pascal ; Rivière, Guillaume</creatorcontrib><description>Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster is under the strong epigenetic influence of DNA methylation, and histone-demethylase orthologues are highly expressed during . early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.</description><identifier>ISSN: 2073-4425</identifier><identifier>EISSN: 2073-4425</identifier><identifier>DOI: 10.3390/genes10090695</identifier><identifier>PMID: 31509985</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Animals ; Cell cycle ; Cell differentiation ; chromatin ; Chromatin remodeling ; Crassostrea - genetics ; Crassostrea - growth &amp; development ; Crassostrea gigas ; DNA methylation ; DNA microarrays ; early development ; Embryo, Nonmammalian - metabolism ; Embryo, Nonmammalian - ultrastructure ; Embryogenesis ; Embryos ; enzyme-linked immunosorbent assay ; Enzymes ; Epigenesis, Genetic ; Epigenetics ; fluorescence ; Gene expression ; gene expression regulation ; Gene Expression Regulation, Developmental ; gene ontology ; genes ; Histone Code ; histone demethylases ; Histone H3 ; Histones ; Histones - genetics ; Histones - metabolism ; larvae ; Life Sciences ; Lysine ; mammals ; Methylation ; microarray technology ; oysters ; Physiology ; Pluripotency ; principal component analysis ; Protein Processing, Post-Translational ; Proteins ; Scanning electron microscopy ; Stem cells ; Sucrose ; Transcription ; transcription (genetics)</subject><ispartof>Genes, 2019-09, Vol.10 (9), p.695</ispartof><rights>2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2019 by the authors. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</citedby><cites>FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</cites><orcidid>0000-0001-8372-8715 ; 0000-0002-4051-4415</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/PMC6771004/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6771004/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31509985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04571004$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Fellous, Alexandre</creatorcontrib><creatorcontrib>Lefranc, Lorane</creatorcontrib><creatorcontrib>Jouaux, Aude</creatorcontrib><creatorcontrib>Goux, Didier</creatorcontrib><creatorcontrib>Favrel, Pascal</creatorcontrib><creatorcontrib>Rivière, Guillaume</creatorcontrib><title>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</title><title>Genes</title><addtitle>Genes (Basel)</addtitle><description>Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster is under the strong epigenetic influence of DNA methylation, and histone-demethylase orthologues are highly expressed during . early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.</description><subject>Animals</subject><subject>Cell cycle</subject><subject>Cell differentiation</subject><subject>chromatin</subject><subject>Chromatin remodeling</subject><subject>Crassostrea - genetics</subject><subject>Crassostrea - growth &amp; development</subject><subject>Crassostrea gigas</subject><subject>DNA methylation</subject><subject>DNA microarrays</subject><subject>early development</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryo, Nonmammalian - ultrastructure</subject><subject>Embryogenesis</subject><subject>Embryos</subject><subject>enzyme-linked immunosorbent assay</subject><subject>Enzymes</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>fluorescence</subject><subject>Gene expression</subject><subject>gene expression regulation</subject><subject>Gene Expression Regulation, Developmental</subject><subject>gene ontology</subject><subject>genes</subject><subject>Histone Code</subject><subject>histone demethylases</subject><subject>Histone H3</subject><subject>Histones</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>larvae</subject><subject>Life Sciences</subject><subject>Lysine</subject><subject>mammals</subject><subject>Methylation</subject><subject>microarray technology</subject><subject>oysters</subject><subject>Physiology</subject><subject>Pluripotency</subject><subject>principal component analysis</subject><subject>Protein Processing, Post-Translational</subject><subject>Proteins</subject><subject>Scanning electron microscopy</subject><subject>Stem cells</subject><subject>Sucrose</subject><subject>Transcription</subject><subject>transcription (genetics)</subject><issn>2073-4425</issn><issn>2073-4425</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFkrFv3CAUxq2qVROlGbtWSF3awSkYjGGpFF2TXKWrkqGdEcbPPiIfuIBPua1_erlcGiVZygLi-_G9p49XFO8JPqNU4i8DOIgEY4m5rF8VxxVuaMlYVb9-cj4qTmO8xXkxXGFcvy2OKKmxlKI-Lv4sbUzeAfoBab0bdbLeoRsdkjV20gkisg5d5TLo4m4KEONeX3iXgh9RNwfrBpTWWdVh3KFvsIXRTxtwCfn-XrjRxvbWoOtdTBDQIugYfUwBNBrsoOO74k2vxwinD_tJ8evy4udiWa6ur74vzlel4USkkncNbTvDhSSNFITInggKpBaVxLIirZamAcaYpIbIDgTrQAreVi2RhDSE0pPi68F3mtsNdCa3GPSopmA3OuyU11Y9V5xdq8FvFW-anDDLBp8PBusXz5bnK7W_w6y-J7cks58eigX_e4aY1MZGA-OoHfg5qoqx_GOcYfF_tBIy-4pGZvTjC_TWz8Hl1FRVM1ETxgXPVHmgTPAxBugfmyVY7adGPZuazH94Gswj_W9G6F9lTb2w</recordid><startdate>20190910</startdate><enddate>20190910</enddate><creator>Fellous, Alexandre</creator><creator>Lefranc, Lorane</creator><creator>Jouaux, Aude</creator><creator>Goux, Didier</creator><creator>Favrel, Pascal</creator><creator>Rivière, Guillaume</creator><general>MDPI AG</general><general>MDPI</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>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8372-8715</orcidid><orcidid>https://orcid.org/0000-0002-4051-4415</orcidid></search><sort><creationdate>20190910</creationdate><title>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</title><author>Fellous, Alexandre ; Lefranc, Lorane ; Jouaux, Aude ; Goux, Didier ; Favrel, Pascal ; Rivière, Guillaume</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c618t-6d73bdc6891798119f183e158290921ba9c7e44493c19de84de986b2b19117133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Cell cycle</topic><topic>Cell differentiation</topic><topic>chromatin</topic><topic>Chromatin remodeling</topic><topic>Crassostrea - genetics</topic><topic>Crassostrea - growth &amp; development</topic><topic>Crassostrea gigas</topic><topic>DNA methylation</topic><topic>DNA microarrays</topic><topic>early development</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryo, Nonmammalian - ultrastructure</topic><topic>Embryogenesis</topic><topic>Embryos</topic><topic>enzyme-linked immunosorbent assay</topic><topic>Enzymes</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetics</topic><topic>fluorescence</topic><topic>Gene expression</topic><topic>gene expression regulation</topic><topic>Gene Expression Regulation, Developmental</topic><topic>gene ontology</topic><topic>genes</topic><topic>Histone Code</topic><topic>histone demethylases</topic><topic>Histone H3</topic><topic>Histones</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>larvae</topic><topic>Life Sciences</topic><topic>Lysine</topic><topic>mammals</topic><topic>Methylation</topic><topic>microarray technology</topic><topic>oysters</topic><topic>Physiology</topic><topic>Pluripotency</topic><topic>principal component analysis</topic><topic>Protein Processing, Post-Translational</topic><topic>Proteins</topic><topic>Scanning electron microscopy</topic><topic>Stem cells</topic><topic>Sucrose</topic><topic>Transcription</topic><topic>transcription (genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fellous, Alexandre</creatorcontrib><creatorcontrib>Lefranc, Lorane</creatorcontrib><creatorcontrib>Jouaux, Aude</creatorcontrib><creatorcontrib>Goux, Didier</creatorcontrib><creatorcontrib>Favrel, Pascal</creatorcontrib><creatorcontrib>Rivière, Guillaume</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fellous, Alexandre</au><au>Lefranc, Lorane</au><au>Jouaux, Aude</au><au>Goux, Didier</au><au>Favrel, Pascal</au><au>Rivière, Guillaume</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas</atitle><jtitle>Genes</jtitle><addtitle>Genes (Basel)</addtitle><date>2019-09-10</date><risdate>2019</risdate><volume>10</volume><issue>9</issue><spage>695</spage><pages>695-</pages><issn>2073-4425</issn><eissn>2073-4425</eissn><abstract>Histone methylation patterns are important epigenetic regulators of mammalian development, notably through stem cell identity maintenance by chromatin remodeling and transcriptional control of pluripotency genes. But, the implications of histone marks are poorly understood in distant groups outside vertebrates and ecdysozoan models. However, the development of the Pacific oyster is under the strong epigenetic influence of DNA methylation, and histone-demethylase orthologues are highly expressed during . early life. This suggests a physiological relevance of histone methylation regulation in oyster development, raising the question of functional conservation of this epigenetic pathway in lophotrochozoan. Quantification of histone methylation using fluorescent ELISAs during oyster early life indicated significant variations in monomethyl histone H3 lysine 4 (H3K4me), an overall decrease in H3K9 mono- and tri-methylations, and in H3K36 methylations, respectively, whereas no significant modification could be detected in H3K27 methylation. Early in vivo treatment with the JmjC-specific inhibitor Methylstat induced hypermethylation of all the examined histone H3 lysines and developmental alterations as revealed by scanning electronic microscopy. Using microarrays, we identified 376 genes that were differentially expressed under methylstat treatment, which expression patterns could discriminate between samples as indicated by principal component analysis. Furthermore, Gene Ontology revealed that these genes were related to processes potentially important for embryonic stages such as binding, cell differentiation and development. These results suggest an important physiological significance of histone methylation in the oyster embryonic and larval life, providing, to our knowledge, the first insights into epigenetic regulation by histone methylation in lophotrochozoan development.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>31509985</pmid><doi>10.3390/genes10090695</doi><orcidid>https://orcid.org/0000-0001-8372-8715</orcidid><orcidid>https://orcid.org/0000-0002-4051-4415</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2073-4425
ispartof Genes, 2019-09, Vol.10 (9), p.695
issn 2073-4425
2073-4425
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6771004
source MDPI - Multidisciplinary Digital Publishing Institute; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central; PubMed Central Open Access
subjects Animals
Cell cycle
Cell differentiation
chromatin
Chromatin remodeling
Crassostrea - genetics
Crassostrea - growth & development
Crassostrea gigas
DNA methylation
DNA microarrays
early development
Embryo, Nonmammalian - metabolism
Embryo, Nonmammalian - ultrastructure
Embryogenesis
Embryos
enzyme-linked immunosorbent assay
Enzymes
Epigenesis, Genetic
Epigenetics
fluorescence
Gene expression
gene expression regulation
Gene Expression Regulation, Developmental
gene ontology
genes
Histone Code
histone demethylases
Histone H3
Histones
Histones - genetics
Histones - metabolism
larvae
Life Sciences
Lysine
mammals
Methylation
microarray technology
oysters
Physiology
Pluripotency
principal component analysis
Protein Processing, Post-Translational
Proteins
Scanning electron microscopy
Stem cells
Sucrose
Transcription
transcription (genetics)
title Histone Methylation Participates in Gene Expression Control during the Early Development of the Pacific Oyster Crassostrea gigas
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-27T08%3A17%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Histone%20Methylation%20Participates%20in%20Gene%20Expression%20Control%20during%20the%20Early%20Development%20of%20the%20Pacific%20Oyster%20Crassostrea%20gigas&rft.jtitle=Genes&rft.au=Fellous,%20Alexandre&rft.date=2019-09-10&rft.volume=10&rft.issue=9&rft.spage=695&rft.pages=695-&rft.issn=2073-4425&rft.eissn=2073-4425&rft_id=info:doi/10.3390/genes10090695&rft_dat=%3Cproquest_pubme%3E2289571879%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2548514686&rft_id=info:pmid/31509985&rfr_iscdi=true