DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus
In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we i...
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description | In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we investigated global DNA methylation and mRNA expression of the methylation‐associated enzymes during embryonic development and in adult tissues of one natural isogenic lineage of mangrove rivulus fish, Kryptolebias marmoratus. Being the best‐known self‐fertilizing hermaphroditic vertebrate affords the opportunity to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. Using the LUminometric Methylation Assay (LUMA), we described variable global DNA methylation at CpG sites in adult tissues, which differed significantly between hermaphrodite ovotestes and male testes (79.6% and 87.2%, respectively). After fertilization, an immediate decrease in DNA methylation occurred to 15.8% in gastrula followed by re‐establishment to 70.0% by stage 26 (liver formation). Compared to zebrafish, at the same embryonic stages, this reprogramming event seems later, deeper, and longer. Furthermore, genes putatively encoding DNA methyltransferases (DNMTs), Ten‐Eleven Translocation (TET), and MeCP2 proteins showed specific regulation in adult gonad and brain, and also during early embryogenesis. Their conserved domains and expression profiles suggest that these proteins play important roles during reproduction and development. This study raises questions about mangrove rivulus’ peculiar reprogramming period in terms of epigenetic transmission and physiological adaptation of individuals to highly variable environments. In accordance with the general‐purpose genotype model, epigenetic mechanisms might allow for the expression of diverse phenotypes among genetically identical individuals. Such phenotypes might help to overcome environmental challenges, making the mangrove rivulus a valuable vertebrate model for ecological epigenetic studies. The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of D |
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The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.</description><identifier>ISSN: 2045-7758</identifier><identifier>EISSN: 2045-7758</identifier><identifier>DOI: 10.1002/ece3.4141</identifier><identifier>PMID: 29988456</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Adults ; Brain ; CpG islands ; Deoxyribonucleic acid ; development ; DNA ; DNA methylation ; Ecological monitoring ; Embryogenesis ; Embryonic growth stage ; Epigenetics ; Evolutionary conservation ; Fertilization ; Gametogenesis ; Gene expression ; Genetic diversity ; Genotypes ; Hermaphrodites ; Hermaphroditism ; Kryptolebias marmoratus ; Liver ; LUMA ; MeCP2 protein ; Methyl-CpG binding protein ; Original Research ; Phenotypes ; Phenotypic variations ; Proteins ; reprogramming ; Self-fertilization ; Testes ; Tissues ; Translocation ; Variance ; Vertebrates ; Zebrafish</subject><ispartof>Ecology and evolution, 2018-06, Vol.8 (12), p.6016-6033</ispartof><rights>2018 The Authors. published by John Wiley & Sons Ltd.</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4431-8f7bf8a7eaf84b45bbf32ed5b069443ee653a509ac89f3838069a5fc89c5878f3</citedby><cites>FETCH-LOGICAL-c4431-8f7bf8a7eaf84b45bbf32ed5b069443ee653a509ac89f3838069a5fc89c5878f3</cites><orcidid>0000-0002-6573-8108</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/PMC6024129/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6024129/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1416,11561,27923,27924,45573,45574,46051,46475,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29988456$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fellous, Alexandre</creatorcontrib><creatorcontrib>Labed‐Veydert, Tiphaine</creatorcontrib><creatorcontrib>Locrel, Mélodie</creatorcontrib><creatorcontrib>Voisin, Anne‐Sophie</creatorcontrib><creatorcontrib>Earley, Ryan L.</creatorcontrib><creatorcontrib>Silvestre, Frederic</creatorcontrib><title>DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus</title><title>Ecology and evolution</title><addtitle>Ecol Evol</addtitle><description>In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we investigated global DNA methylation and mRNA expression of the methylation‐associated enzymes during embryonic development and in adult tissues of one natural isogenic lineage of mangrove rivulus fish, Kryptolebias marmoratus. Being the best‐known self‐fertilizing hermaphroditic vertebrate affords the opportunity to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. Using the LUminometric Methylation Assay (LUMA), we described variable global DNA methylation at CpG sites in adult tissues, which differed significantly between hermaphrodite ovotestes and male testes (79.6% and 87.2%, respectively). After fertilization, an immediate decrease in DNA methylation occurred to 15.8% in gastrula followed by re‐establishment to 70.0% by stage 26 (liver formation). Compared to zebrafish, at the same embryonic stages, this reprogramming event seems later, deeper, and longer. Furthermore, genes putatively encoding DNA methyltransferases (DNMTs), Ten‐Eleven Translocation (TET), and MeCP2 proteins showed specific regulation in adult gonad and brain, and also during early embryogenesis. Their conserved domains and expression profiles suggest that these proteins play important roles during reproduction and development. This study raises questions about mangrove rivulus’ peculiar reprogramming period in terms of epigenetic transmission and physiological adaptation of individuals to highly variable environments. In accordance with the general‐purpose genotype model, epigenetic mechanisms might allow for the expression of diverse phenotypes among genetically identical individuals. Such phenotypes might help to overcome environmental challenges, making the mangrove rivulus a valuable vertebrate model for ecological epigenetic studies. The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.
The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.</description><subject>Adults</subject><subject>Brain</subject><subject>CpG islands</subject><subject>Deoxyribonucleic acid</subject><subject>development</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>Ecological monitoring</subject><subject>Embryogenesis</subject><subject>Embryonic growth stage</subject><subject>Epigenetics</subject><subject>Evolutionary conservation</subject><subject>Fertilization</subject><subject>Gametogenesis</subject><subject>Gene expression</subject><subject>Genetic diversity</subject><subject>Genotypes</subject><subject>Hermaphrodites</subject><subject>Hermaphroditism</subject><subject>Kryptolebias marmoratus</subject><subject>Liver</subject><subject>LUMA</subject><subject>MeCP2 protein</subject><subject>Methyl-CpG binding protein</subject><subject>Original Research</subject><subject>Phenotypes</subject><subject>Phenotypic variations</subject><subject>Proteins</subject><subject>reprogramming</subject><subject>Self-fertilization</subject><subject>Testes</subject><subject>Tissues</subject><subject>Translocation</subject><subject>Variance</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>2045-7758</issn><issn>2045-7758</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kc1u1DAUhSMEolXpghdAltiA1Gmd2I6dDVI1DD-igg2sLSe5nnHl2IN_Bg2rPgLPyJPgMKUqSNyN7_X9dHTsU1VPa3xeY9xcwADknNa0flAdN5iyBedMPLzXH1WnMV7jUi1uKOaPq6Om64SgrD2u0uuPl2iCtNlblYx3yDikxmxTRMqNaMzBuDUaYQfWbydwCXmN0gZQBKt_3vzQEJKx5vtMTcqtg98BCmaXbY5n6EPYb5O30BsVyzpMPqiU45PqkVY2wunteVJ9ebP6vHy3uPr09v3y8moxUErqhdC810JxUFrQnrK-16SBkfW47QoA0DKiGO7UIDpNBBHlXjFdpoEJLjQ5qV4ddLe5n2Aciv2grNwGU7zspVdG_r1xZiPXfifnj6qbrgi8uBUI_muGmORk4gDWKgc-R9nglouO1ZQX9Pk_6LXPwZXnFarDhBEuSKFeHqgh-BgD6DszNZZznHKOU85xFvbZffd35J_wCnBxAL4ZC_v_K8nVckV-S_4Cqwis6A</recordid><startdate>201806</startdate><enddate>201806</enddate><creator>Fellous, Alexandre</creator><creator>Labed‐Veydert, Tiphaine</creator><creator>Locrel, Mélodie</creator><creator>Voisin, Anne‐Sophie</creator><creator>Earley, Ryan L.</creator><creator>Silvestre, Frederic</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7X2</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</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>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6573-8108</orcidid></search><sort><creationdate>201806</creationdate><title>DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus</title><author>Fellous, Alexandre ; Labed‐Veydert, Tiphaine ; Locrel, Mélodie ; Voisin, Anne‐Sophie ; Earley, Ryan L. ; Silvestre, Frederic</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4431-8f7bf8a7eaf84b45bbf32ed5b069443ee653a509ac89f3838069a5fc89c5878f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adults</topic><topic>Brain</topic><topic>CpG islands</topic><topic>Deoxyribonucleic acid</topic><topic>development</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>Ecological monitoring</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Epigenetics</topic><topic>Evolutionary conservation</topic><topic>Fertilization</topic><topic>Gametogenesis</topic><topic>Gene expression</topic><topic>Genetic diversity</topic><topic>Genotypes</topic><topic>Hermaphrodites</topic><topic>Hermaphroditism</topic><topic>Kryptolebias marmoratus</topic><topic>Liver</topic><topic>LUMA</topic><topic>MeCP2 protein</topic><topic>Methyl-CpG binding protein</topic><topic>Original Research</topic><topic>Phenotypes</topic><topic>Phenotypic variations</topic><topic>Proteins</topic><topic>reprogramming</topic><topic>Self-fertilization</topic><topic>Testes</topic><topic>Tissues</topic><topic>Translocation</topic><topic>Variance</topic><topic>Vertebrates</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fellous, Alexandre</creatorcontrib><creatorcontrib>Labed‐Veydert, Tiphaine</creatorcontrib><creatorcontrib>Locrel, Mélodie</creatorcontrib><creatorcontrib>Voisin, Anne‐Sophie</creatorcontrib><creatorcontrib>Earley, Ryan L.</creatorcontrib><creatorcontrib>Silvestre, Frederic</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</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>Agricultural Science Database</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>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Ecology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fellous, Alexandre</au><au>Labed‐Veydert, Tiphaine</au><au>Locrel, Mélodie</au><au>Voisin, Anne‐Sophie</au><au>Earley, Ryan L.</au><au>Silvestre, Frederic</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus</atitle><jtitle>Ecology and evolution</jtitle><addtitle>Ecol Evol</addtitle><date>2018-06</date><risdate>2018</risdate><volume>8</volume><issue>12</issue><spage>6016</spage><epage>6033</epage><pages>6016-6033</pages><issn>2045-7758</issn><eissn>2045-7758</eissn><abstract>In addition to genetic variation, epigenetic mechanisms such as DNA methylation might make important contributions to heritable phenotypic diversity in populations. However, it is often difficult to disentangle the contributions of genetic and epigenetic variation to phenotypic diversity. Here, we investigated global DNA methylation and mRNA expression of the methylation‐associated enzymes during embryonic development and in adult tissues of one natural isogenic lineage of mangrove rivulus fish, Kryptolebias marmoratus. Being the best‐known self‐fertilizing hermaphroditic vertebrate affords the opportunity to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. Using the LUminometric Methylation Assay (LUMA), we described variable global DNA methylation at CpG sites in adult tissues, which differed significantly between hermaphrodite ovotestes and male testes (79.6% and 87.2%, respectively). After fertilization, an immediate decrease in DNA methylation occurred to 15.8% in gastrula followed by re‐establishment to 70.0% by stage 26 (liver formation). Compared to zebrafish, at the same embryonic stages, this reprogramming event seems later, deeper, and longer. Furthermore, genes putatively encoding DNA methyltransferases (DNMTs), Ten‐Eleven Translocation (TET), and MeCP2 proteins showed specific regulation in adult gonad and brain, and also during early embryogenesis. Their conserved domains and expression profiles suggest that these proteins play important roles during reproduction and development. This study raises questions about mangrove rivulus’ peculiar reprogramming period in terms of epigenetic transmission and physiological adaptation of individuals to highly variable environments. In accordance with the general‐purpose genotype model, epigenetic mechanisms might allow for the expression of diverse phenotypes among genetically identical individuals. Such phenotypes might help to overcome environmental challenges, making the mangrove rivulus a valuable vertebrate model for ecological epigenetic studies. The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.
The mangrove rivulus, Kryptolebias marmoratus, is the best‐known self‐fertilizing hermaphroditic vertebrate that allows to work with genetically identical individuals to examine, explicitly, the phenotypic effects of epigenetic variance. The reprogramming event is later, more dramatic and longer than in other described vertebrates. High evolutionary conservation and expression patterns of DNMT, TET, and MeCP2 proteins in K. marmoratus suggest biological roles for each member in gametogenesis and development.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>29988456</pmid><doi>10.1002/ece3.4141</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-6573-8108</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adults Brain CpG islands Deoxyribonucleic acid development DNA DNA methylation Ecological monitoring Embryogenesis Embryonic growth stage Epigenetics Evolutionary conservation Fertilization Gametogenesis Gene expression Genetic diversity Genotypes Hermaphrodites Hermaphroditism Kryptolebias marmoratus Liver LUMA MeCP2 protein Methyl-CpG binding protein Original Research Phenotypes Phenotypic variations Proteins reprogramming Self-fertilization Testes Tissues Translocation Variance Vertebrates Zebrafish |
title | DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus |
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