An otx/nodal regulatory signature for posterior neural development in ascidians
In chordates, neural induction is the first step of a complex developmental process through which ectodermal cells acquire a neural identity. In ascidians, FGF-mediated neural induction occurs at the 32-cell stage in two blastomere pairs, precursors respectively of anterior and posterior neural tiss...
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description | In chordates, neural induction is the first step of a complex developmental process through which ectodermal cells acquire a neural identity. In ascidians, FGF-mediated neural induction occurs at the 32-cell stage in two blastomere pairs, precursors respectively of anterior and posterior neural tissue. We combined molecular embryology and cis-regulatory analysis to unveil in the ascidian Ciona intestinalis the remarkably simple proximal genetic network that controls posterior neural fate acquisition downstream of FGF. We report that the combined action of two direct FGF targets, the TGFβ factor Nodal, acting via Smad- and Fox-binding sites, and the transcription factor Otx suffices to trigger ascidian posterior neural tissue formation. Moreover, we found that this strategy is conserved in the distantly related ascidian Phallusia mammillata, in spite of extreme sequence divergence in the cis-regulatory sequences involved. Our results thus highlight that the modes of gene regulatory network evolution differ with the evolutionary scale considered. Within ascidians, developmental regulatory networks are remarkably robust to genome sequence divergence. Between ascidians and vertebrates, major fate determinants, such as Otx and Nodal, can be co-opted into different networks. Comparative developmental studies in ascidians with divergent genomes will thus uncover shared ascidian strategies, and contribute to a better understanding of the diversity of developmental strategies within chordates. |
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In ascidians, FGF-mediated neural induction occurs at the 32-cell stage in two blastomere pairs, precursors respectively of anterior and posterior neural tissue. We combined molecular embryology and cis-regulatory analysis to unveil in the ascidian Ciona intestinalis the remarkably simple proximal genetic network that controls posterior neural fate acquisition downstream of FGF. We report that the combined action of two direct FGF targets, the TGFβ factor Nodal, acting via Smad- and Fox-binding sites, and the transcription factor Otx suffices to trigger ascidian posterior neural tissue formation. Moreover, we found that this strategy is conserved in the distantly related ascidian Phallusia mammillata, in spite of extreme sequence divergence in the cis-regulatory sequences involved. Our results thus highlight that the modes of gene regulatory network evolution differ with the evolutionary scale considered. Within ascidians, developmental regulatory networks are remarkably robust to genome sequence divergence. Between ascidians and vertebrates, major fate determinants, such as Otx and Nodal, can be co-opted into different networks. Comparative developmental studies in ascidians with divergent genomes will thus uncover shared ascidian strategies, and contribute to a better understanding of the diversity of developmental strategies within chordates.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1004548</identifier><identifier>PMID: 25121599</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acquisitions & mergers ; Animals ; Ascidiacea ; Binding Sites ; Biology and life sciences ; Blastomeres ; Central Nervous System - growth & development ; Ciona intestinalis - genetics ; Ciona intestinalis - growth & development ; Embryology ; Evolution, Molecular ; Gastrula - growth & development ; Gene Expression Regulation, Developmental ; Gene Regulatory Networks ; Genes ; Genetic aspects ; Genetic research ; Genetics ; Genomes ; Genomics ; Life Sciences ; Nervous system ; Neurogenesis - genetics ; Nodal Protein - biosynthesis ; Nodal Protein - genetics ; Otx Transcription Factors - biosynthesis ; Otx Transcription Factors - genetics ; Physiological aspects ; Research and Analysis Methods ; Stem cell research ; Transcription factors ; Transforming growth factors ; Vertebrates</subject><ispartof>PLoS genetics, 2014-08, Vol.10 (8), p.e1004548-e1004548</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>Attribution</rights><rights>2014 Roure et al 2014 Roure et al</rights><rights>2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Roure A, Lemaire P, Darras S (2014) An Otx/Nodal Regulatory Signature for Posterior Neural Development in Ascidians. 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In ascidians, FGF-mediated neural induction occurs at the 32-cell stage in two blastomere pairs, precursors respectively of anterior and posterior neural tissue. We combined molecular embryology and cis-regulatory analysis to unveil in the ascidian Ciona intestinalis the remarkably simple proximal genetic network that controls posterior neural fate acquisition downstream of FGF. We report that the combined action of two direct FGF targets, the TGFβ factor Nodal, acting via Smad- and Fox-binding sites, and the transcription factor Otx suffices to trigger ascidian posterior neural tissue formation. Moreover, we found that this strategy is conserved in the distantly related ascidian Phallusia mammillata, in spite of extreme sequence divergence in the cis-regulatory sequences involved. Our results thus highlight that the modes of gene regulatory network evolution differ with the evolutionary scale considered. Within ascidians, developmental regulatory networks are remarkably robust to genome sequence divergence. Between ascidians and vertebrates, major fate determinants, such as Otx and Nodal, can be co-opted into different networks. Comparative developmental studies in ascidians with divergent genomes will thus uncover shared ascidian strategies, and contribute to a better understanding of the diversity of developmental strategies within chordates.</description><subject>Acquisitions & mergers</subject><subject>Animals</subject><subject>Ascidiacea</subject><subject>Binding Sites</subject><subject>Biology and life sciences</subject><subject>Blastomeres</subject><subject>Central Nervous System - growth & development</subject><subject>Ciona intestinalis - genetics</subject><subject>Ciona intestinalis - growth & development</subject><subject>Embryology</subject><subject>Evolution, Molecular</subject><subject>Gastrula - growth & development</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic research</subject><subject>Genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Life Sciences</subject><subject>Nervous system</subject><subject>Neurogenesis - genetics</subject><subject>Nodal Protein - biosynthesis</subject><subject>Nodal Protein - genetics</subject><subject>Otx Transcription Factors - biosynthesis</subject><subject>Otx Transcription Factors - genetics</subject><subject>Physiological aspects</subject><subject>Research and Analysis Methods</subject><subject>Stem cell research</subject><subject>Transcription factors</subject><subject>Transforming growth factors</subject><subject>Vertebrates</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVk12LEzEUhgdR3HX1H4gOCOJetJuP-cqNUBZ1C8WCX7chTU6mKdOkJpmy--_N2O7SES-UuZhw5nnfl3MyJ8teYjTFtMZXG9d7K7rprgU7xQgVZdE8ys5xWdJJXaDi8cn5LHsWwgYhWjasfpqdkRITXDJ2ni1nNnfx9so6JbrcQ9t3Ijp_lwfTWhF7D7l2Pt-5EMGbdLLQ-0Qq2EPndluwMTc2F0EaZYQNz7MnWnQBXhzfF9n3jx--Xd9MFstP8-vZYiJrSuKEipUWSCIGiFaEUoorQdEKNKuYpnpVSNUArhRDooZSk6pWUiu1qhlgWUlML7LXB99d5wI_ziJwXDUlYk2NaCLmB0I5seE7b7bC33EnDP9dcL7lwkcjO-CaEk1Yo1kjaFHXogGhKqGSTcUIIUPa-2Nav9qCkqnrNISR6fiLNWveuj0vMKWoQMng8mCw_kN2M1vwoYYwLUhVsf0Q9u4Y5t3PHkLkWxMkdJ2w4PrUY7rVGjFUNwl9c0BbkdowVruULgecz2hDWImqhiRq-hcqPQq2RjoL2qT6SHA5EiQmwm1sRR8Cn3_98h_s539nlz_G7NsTdg2ii-vguj4aZ8MYLA6g9C4ED_phvhjxYVPu_w4-bAo_bkqSvTq90gfR_WrQX-mSDZ8</recordid><startdate>20140801</startdate><enddate>20140801</enddate><creator>Roure, Agnès</creator><creator>Lemaire, Patrick</creator><creator>Darras, Sébastien</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-0590-0062</orcidid><orcidid>https://orcid.org/0000-0003-4925-2009</orcidid></search><sort><creationdate>20140801</creationdate><title>An otx/nodal regulatory signature for posterior neural development in ascidians</title><author>Roure, Agnès ; 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In ascidians, FGF-mediated neural induction occurs at the 32-cell stage in two blastomere pairs, precursors respectively of anterior and posterior neural tissue. We combined molecular embryology and cis-regulatory analysis to unveil in the ascidian Ciona intestinalis the remarkably simple proximal genetic network that controls posterior neural fate acquisition downstream of FGF. We report that the combined action of two direct FGF targets, the TGFβ factor Nodal, acting via Smad- and Fox-binding sites, and the transcription factor Otx suffices to trigger ascidian posterior neural tissue formation. Moreover, we found that this strategy is conserved in the distantly related ascidian Phallusia mammillata, in spite of extreme sequence divergence in the cis-regulatory sequences involved. Our results thus highlight that the modes of gene regulatory network evolution differ with the evolutionary scale considered. Within ascidians, developmental regulatory networks are remarkably robust to genome sequence divergence. Between ascidians and vertebrates, major fate determinants, such as Otx and Nodal, can be co-opted into different networks. Comparative developmental studies in ascidians with divergent genomes will thus uncover shared ascidian strategies, and contribute to a better understanding of the diversity of developmental strategies within chordates.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25121599</pmid><doi>10.1371/journal.pgen.1004548</doi><orcidid>https://orcid.org/0000-0002-0590-0062</orcidid><orcidid>https://orcid.org/0000-0003-4925-2009</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acquisitions & mergers Animals Ascidiacea Binding Sites Biology and life sciences Blastomeres Central Nervous System - growth & development Ciona intestinalis - genetics Ciona intestinalis - growth & development Embryology Evolution, Molecular Gastrula - growth & development Gene Expression Regulation, Developmental Gene Regulatory Networks Genes Genetic aspects Genetic research Genetics Genomes Genomics Life Sciences Nervous system Neurogenesis - genetics Nodal Protein - biosynthesis Nodal Protein - genetics Otx Transcription Factors - biosynthesis Otx Transcription Factors - genetics Physiological aspects Research and Analysis Methods Stem cell research Transcription factors Transforming growth factors Vertebrates |
title | An otx/nodal regulatory signature for posterior neural development in ascidians |
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