Amphioxus functional genomics and the origins of vertebrate gene regulation

Marlétaz, Ferdinand; Firbas, Panos N.; Maeso, Ignacio; Tena, Juan J.; Bogdanovic, Ozren; Perry, Malcolm; Wyatt, Christopher D.R.; de la Calle-Mustienes, Elisa; Bertrand, Stephanie; Burguera, Demian; Acemel, Rafael D.; van Heeringen, Simon J.; Naranjo, Silvia; Herrera Úbeda, Carlos; Skvortsova, Ksenia; Jimenez-Gancedo, Sandra; Aldea, Daniel; Marquez, Yamile; Buono, Lorena; Kozmikova, Iryna; Permanyer, Jon; Louis, Alexandra; Albuixech Crespo, Beatriz; Le Petillon, Yann Lee; Leon, Anthony; Subirana, Lucie; Balwierz, Piotr J.; Duckett, Paul E.; Farahani, Ensieh; Aury, Jean-Marc; Mangenot, Sophie; Wincker, Patrick; Albalat Rodríguez, Ricard; Benito Gutiérrez, Èlia; Cañestro García, Cristian; Castro, Felipe; D'Aniello, Salvatore; Ferrier, David EK.; Huang, Shengfeng; Laudet, Vincent; Marais, Gabriel A. B.; Pontarotti, Pierre; Schubert, Michael; Seitz, Hervé; Somorjai, Ildikó M. L.; Takahash, Tokiharu; Mirabeau, Olivier; Xu, Anlong; Yu, Jr-Kai; Carninci, Piero; Martinez-Morales, Juan Ramon; Roest Crollius, Hugues; Kozmik, Zbynek; Weirauch, Matthew T.; Garcia Fernández, Jordi; Lister, Ryan; Lenhard, Boris; Holland, Peter W. H.; Escriva, Hector; Gómez-Skarmeta, Jose Luis; Irimia Martínez, Manuel

Amphioxus functional genomics and the origins of vertebrate gene regulation

Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessi...

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Autores:	Marlétaz, Ferdinand, Firbas, Panos N., Maeso, Ignacio, Tena, Juan J., Bogdanovic, Ozren, Perry, Malcolm, Wyatt, Christopher D.R., de la Calle-Mustienes, Elisa, Bertrand, Stephanie, Burguera, Demian, Acemel, Rafael D., van Heeringen, Simon J., Naranjo, Silvia, Herrera Úbeda, Carlos, Skvortsova, Ksenia, Jimenez-Gancedo, Sandra, Aldea, Daniel, Marquez, Yamile, Buono, Lorena, Kozmikova, Iryna, Permanyer, Jon, Louis, Alexandra, Albuixech Crespo, Beatriz, Le Petillon, Yann Lee, Leon, Anthony, Subirana, Lucie, Balwierz, Piotr J., Duckett, Paul E., Farahani, Ensieh, Aury, Jean-Marc, Mangenot, Sophie, Wincker, Patrick, Albalat Rodríguez, Ricard, Benito Gutiérrez, Èlia, Cañestro García, Cristian, Castro, Felipe, D'Aniello, Salvatore, Ferrier, David EK., Huang, Shengfeng, Laudet, Vincent, Marais, Gabriel A. B., Pontarotti, Pierre, Schubert, Michael, Seitz, Hervé, Somorjai, Ildikó M. L., Takahash, Tokiharu, Mirabeau, Olivier, Xu, Anlong, Yu, Jr-Kai, Carninci, Piero, Martinez-Morales, Juan Ramon, Roest Crollius, Hugues, Kozmik, Zbynek, Weirauch, Matthew T., Garcia Fernández, Jordi, Lister, Ryan, Lenhard, Boris, Holland, Peter W. H., Escriva, Hector, Gómez-Skarmeta, Jose Luis, Irimia Martínez, Manuel
Tipo de recurso:	artículo
Estado:	Versión aceptada para publicación
Fecha de publicación:	2018
País:	España
Institución:	Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:	Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:	oai:recercat.cat:2445/175730
Acceso en línea:	https://hdl.handle.net/2445/175730
Access Level:	acceso abierto
Palabra clave:	Vertebrats Amfiox Vertebrates Branchiostoma lanceolatum

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spelling	Amphioxus functional genomics and the origins of vertebrate gene regulationMarlétaz, FerdinandFirbas, Panos N.Maeso, IgnacioTena, Juan J.Bogdanovic, OzrenPerry, MalcolmWyatt, Christopher D.R.de la Calle-Mustienes, ElisaBertrand, StephanieBurguera, DemianAcemel, Rafael D.van Heeringen, Simon J.Naranjo, SilviaHerrera Úbeda, CarlosSkvortsova, KseniaJimenez-Gancedo, SandraAldea, DanielMarquez, YamileBuono, LorenaKozmikova, IrynaPermanyer, JonLouis, AlexandraAlbuixech Crespo, BeatrizLe Petillon, Yann LeeLeon, AnthonySubirana, LucieBalwierz, Piotr J.Duckett, Paul E.Farahani, EnsiehAury, Jean-MarcMangenot, SophieWincker, PatrickAlbalat Rodríguez, RicardBenito Gutiérrez, ÈliaCañestro García, CristianCastro, FelipeD'Aniello, SalvatoreFerrier, David EK.Huang, ShengfengLaudet, VincentMarais, Gabriel A. B.Pontarotti, PierreSchubert, MichaelSeitz, HervéSomorjai, Ildikó M. L.Takahash, TokiharuMirabeau, OlivierXu, AnlongYu, Jr-KaiCarninci, PieroMartinez-Morales, Juan RamonRoest Crollius, HuguesKozmik, ZbynekWeirauch, Matthew T.Kozmik, ZbynekWeirauch, Matthew T.Garcia Fernández, JordiLister, RyanLenhard, BorisHolland, Peter W. H.Escriva, HectorGómez-Skarmeta, Jose LuisIrimia Martínez, ManuelVertebratsAmfioxVertebratesBranchiostoma lanceolatumVertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that-in vertebrates-over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.Nature Publishing Group2021202120182021info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersioninfo:eu-repo/semantics/publishedVersion7 p.application/pdfhttps://hdl.handle.net/2445/175730Articles publicats en revistes (Genètica, Microbiologia i Estadística)reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésReproducció del document publicat a: https://doi.org/10.1038/s41586-018-0734-6Nature, 2018, vol. 564, p. 64-70https://doi.org/10.1038/s41586-018-0734-6info:eu-repo/grantAgreement/EC/H2020/740041info:eu-repo/grantAgreement/EC/FP7/607142info:eu-repo/grantAgreement/EC/H2020/692419info:eu-repo/grantAgreement/EC/H2020/637591info:eu-repo/grantAgreement/EC/H2020/658521info:eu-repo/grantAgreement/EC/FP7/268513(c) cc-by Marlétaz et. al., 2018http://creativecommons.org/licenses/by/3.0/es/info:eu-repo/semantics/openAccessoai:recercat.cat:2445/1757302026-05-29T05:05:01Z
dc.title.none.fl_str_mv	Amphioxus functional genomics and the origins of vertebrate gene regulation
title	Amphioxus functional genomics and the origins of vertebrate gene regulation
spellingShingle	Amphioxus functional genomics and the origins of vertebrate gene regulation Marlétaz, Ferdinand Vertebrats Amfiox Vertebrates Branchiostoma lanceolatum
title_short	Amphioxus functional genomics and the origins of vertebrate gene regulation
title_full	Amphioxus functional genomics and the origins of vertebrate gene regulation
title_fullStr	Amphioxus functional genomics and the origins of vertebrate gene regulation
title_full_unstemmed	Amphioxus functional genomics and the origins of vertebrate gene regulation
title_sort	Amphioxus functional genomics and the origins of vertebrate gene regulation
dc.creator.none.fl_str_mv	Marlétaz, Ferdinand Firbas, Panos N. Maeso, Ignacio Tena, Juan J. Bogdanovic, Ozren Perry, Malcolm Wyatt, Christopher D.R. de la Calle-Mustienes, Elisa Bertrand, Stephanie Burguera, Demian Acemel, Rafael D. van Heeringen, Simon J. Naranjo, Silvia Herrera Úbeda, Carlos Skvortsova, Ksenia Jimenez-Gancedo, Sandra Aldea, Daniel Marquez, Yamile Buono, Lorena Kozmikova, Iryna Permanyer, Jon Louis, Alexandra Albuixech Crespo, Beatriz Le Petillon, Yann Lee Leon, Anthony Subirana, Lucie Balwierz, Piotr J. Duckett, Paul E. Farahani, Ensieh Aury, Jean-Marc Mangenot, Sophie Wincker, Patrick Albalat Rodríguez, Ricard Benito Gutiérrez, Èlia Cañestro García, Cristian Castro, Felipe D'Aniello, Salvatore Ferrier, David EK. Huang, Shengfeng Laudet, Vincent Marais, Gabriel A. B. Pontarotti, Pierre Schubert, Michael Seitz, Hervé Somorjai, Ildikó M. L. Takahash, Tokiharu Mirabeau, Olivier Xu, Anlong Yu, Jr-Kai Carninci, Piero Martinez-Morales, Juan Ramon Roest Crollius, Hugues Kozmik, Zbynek Weirauch, Matthew T. Kozmik, Zbynek Weirauch, Matthew T. Garcia Fernández, Jordi Lister, Ryan Lenhard, Boris Holland, Peter W. H. Escriva, Hector Gómez-Skarmeta, Jose Luis Irimia Martínez, Manuel
author	Marlétaz, Ferdinand
author_facet	Marlétaz, Ferdinand Firbas, Panos N. Maeso, Ignacio Tena, Juan J. Bogdanovic, Ozren Perry, Malcolm Wyatt, Christopher D.R. de la Calle-Mustienes, Elisa Bertrand, Stephanie Burguera, Demian Acemel, Rafael D. van Heeringen, Simon J. Naranjo, Silvia Herrera Úbeda, Carlos Skvortsova, Ksenia Jimenez-Gancedo, Sandra Aldea, Daniel Marquez, Yamile Buono, Lorena Kozmikova, Iryna Permanyer, Jon Louis, Alexandra Albuixech Crespo, Beatriz Le Petillon, Yann Lee Leon, Anthony Subirana, Lucie Balwierz, Piotr J. Duckett, Paul E. Farahani, Ensieh Aury, Jean-Marc Mangenot, Sophie Wincker, Patrick Albalat Rodríguez, Ricard Benito Gutiérrez, Èlia Cañestro García, Cristian Castro, Felipe D'Aniello, Salvatore Ferrier, David EK. Huang, Shengfeng Laudet, Vincent Marais, Gabriel A. B. Pontarotti, Pierre Schubert, Michael Seitz, Hervé Somorjai, Ildikó M. L. Takahash, Tokiharu Mirabeau, Olivier Xu, Anlong Yu, Jr-Kai Carninci, Piero Martinez-Morales, Juan Ramon Roest Crollius, Hugues Kozmik, Zbynek Weirauch, Matthew T. Kozmik, Zbynek Garcia Fernández, Jordi Lister, Ryan Lenhard, Boris Holland, Peter W. H. Escriva, Hector Gómez-Skarmeta, Jose Luis Irimia Martínez, Manuel
author_role	author
author2	Firbas, Panos N. Maeso, Ignacio Tena, Juan J. Bogdanovic, Ozren Perry, Malcolm Wyatt, Christopher D.R. de la Calle-Mustienes, Elisa Bertrand, Stephanie Burguera, Demian Acemel, Rafael D. van Heeringen, Simon J. Naranjo, Silvia Herrera Úbeda, Carlos Skvortsova, Ksenia Jimenez-Gancedo, Sandra Aldea, Daniel Marquez, Yamile Buono, Lorena Kozmikova, Iryna Permanyer, Jon Louis, Alexandra Albuixech Crespo, Beatriz Le Petillon, Yann Lee Leon, Anthony Subirana, Lucie Balwierz, Piotr J. Duckett, Paul E. Farahani, Ensieh Aury, Jean-Marc Mangenot, Sophie Wincker, Patrick Albalat Rodríguez, Ricard Benito Gutiérrez, Èlia Cañestro García, Cristian Castro, Felipe D'Aniello, Salvatore Ferrier, David EK. Huang, Shengfeng Laudet, Vincent Marais, Gabriel A. B. Pontarotti, Pierre Schubert, Michael Seitz, Hervé Somorjai, Ildikó M. L. Takahash, Tokiharu Mirabeau, Olivier Xu, Anlong Yu, Jr-Kai Carninci, Piero Martinez-Morales, Juan Ramon Roest Crollius, Hugues Kozmik, Zbynek Weirauch, Matthew T. Kozmik, Zbynek Garcia Fernández, Jordi Lister, Ryan Lenhard, Boris Holland, Peter W. H. Escriva, Hector Gómez-Skarmeta, Jose Luis Irimia Martínez, Manuel
author2_role	author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author
dc.subject.none.fl_str_mv	Vertebrats Amfiox Vertebrates Branchiostoma lanceolatum
topic	Vertebrats Amfiox Vertebrates Branchiostoma lanceolatum
description	Vertebrates have greatly elaborated the basic chordate body plan and evolved highly distinctive genomes that have been sculpted by two whole-genome duplications. Here we sequence the genome of the Mediterranean amphioxus (Branchiostoma lanceolatum) and characterize DNA methylation, chromatin accessibility, histone modifications and transcriptomes across multiple developmental stages and adult tissues to investigate the evolution of the regulation of the chordate genome. Comparisons with vertebrates identify an intermediate stage in the evolution of differentially methylated enhancers, and a high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates that occurs maximally at an earlier mid-embryonic phylotypic period. We analyse regulatory evolution after whole-genome duplications, and find that-in vertebrates-over 80% of broadly expressed gene families with multiple paralogues derived from whole-genome duplications have members that restricted their ancestral expression, and underwent specialization rather than subfunctionalization. Counter-intuitively, paralogues that restricted their expression increased the complexity of their regulatory landscapes. These data pave the way for a better understanding of the regulatory principles that underlie key vertebrate innovations.
publishDate	2018
dc.date.none.fl_str_mv	2018 2021 2021 2021
dc.type.none.fl_str_mv	info:eu-repo/semantics/article info:eu-repo/semantics/acceptedVersion info:eu-repo/semantics/publishedVersion
format	article
status_str	acceptedVersion
dc.identifier.none.fl_str_mv	https://hdl.handle.net/2445/175730
url	https://hdl.handle.net/2445/175730
dc.language.none.fl_str_mv	Inglés
language_invalid_str_mv	Inglés
dc.relation.none.fl_str_mv	Reproducció del document publicat a: https://doi.org/10.1038/s41586-018-0734-6 Nature, 2018, vol. 564, p. 64-70 https://doi.org/10.1038/s41586-018-0734-6 info:eu-repo/grantAgreement/EC/H2020/740041 info:eu-repo/grantAgreement/EC/FP7/607142 info:eu-repo/grantAgreement/EC/H2020/692419 info:eu-repo/grantAgreement/EC/H2020/637591 info:eu-repo/grantAgreement/EC/H2020/658521 info:eu-repo/grantAgreement/EC/FP7/268513
dc.rights.none.fl_str_mv	(c) cc-by Marlétaz et. al., 2018 http://creativecommons.org/licenses/by/3.0/es/ info:eu-repo/semantics/openAccess
rights_invalid_str_mv	(c) cc-by Marlétaz et. al., 2018 http://creativecommons.org/licenses/by/3.0/es/
eu_rights_str_mv	openAccess
dc.format.none.fl_str_mv	7 p. application/pdf
dc.publisher.none.fl_str_mv	Nature Publishing Group
publisher.none.fl_str_mv	Nature Publishing Group
dc.source.none.fl_str_mv	Articles publicats en revistes (Genètica, Microbiologia i Estadística) reponame:Recercat. Dipósit de la Recerca de Catalunya instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str	Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str	Recercat. Dipósit de la Recerca de Catalunya
collection	Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score	15.81155

Amphioxus functional genomics and the origins of vertebrate gene regulation

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