Amphioxus functional genomics and the origins of vertebrate gene regulation

Marlétaz, Ferdinand; Firbas, Panos; Maeso, Ignacio; Tena, Juan J.; Bogdanovic, Ozren; Perry, M.; Wyatt, Christopher D. R.; Calle-Mustienes, Elisa de la; Bertrand, Stephanie; Burguera, Demian; Acemel, Rafael D.; Van Heeringen, Simon J.; Naranjo, Silvia; Herrera-Úbeda, Carlos; Skvortsova, Ksenia; Jiménez-Gancedo, Sandra; Aldea, Daniel; Marquez, Yamile; Buono, Lorena; Kozmikova, Iryna; Permanyer, Jon; Louis, Alexandra; Albuixech-Crespo, Beatriz; Petillon, Yann Le; Leon, Anthony; Subirana, Lucie; Balwierz, Piotr J.; Duckett, Paul Edward; Farahani, Ensieh; Aury, Jean‐Marc; Mangenot, Sophie; Wincker, Patrick; Albalat, Ricard; Benito-Gutiérrez, Èlia; Cañestro, Cristian; Castro, Filipe; D’Aniello, Salvatore; Ferrier, David E. K.; Huang, Shengfeng; Laudet, Vincent; Marais, Gabriel A.B.; Pontarotti, Pierre; Schubert, Michael; Seitz, Hervé; Somorjai, Ildiko; Takahashi, Tokiharu; Mirabeau, Olivier; Xu, Anlong; Yu, Jr-Kai; Carninci, Piero; Martínez-Morales, Juan Ramón; Roest Crollius, Hugues; Kozmik, Zbynek; Weirauch, Matthew T.; Garcia-Fernàndez, Jordi; Lister, Ryan; Lenhard, Boris; Holland, Peter W. H.; Escrivá, Héctor; Gómez-Skarmeta, José Luis; Irimia, 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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Authors:	Marlétaz, Ferdinand, Firbas, Panos, Maeso, Ignacio, Tena, Juan J., Bogdanovic, Ozren, Perry, M., Wyatt, Christopher D. R., Calle-Mustienes, Elisa de la, Bertrand, Stephanie, Burguera, Demian, Acemel, Rafael D., Van Heeringen, Simon J., Naranjo, Silvia, Herrera-Úbeda, Carlos, Skvortsova, Ksenia, Jiménez-Gancedo, Sandra, Aldea, Daniel, Marquez, Yamile, Buono, Lorena, Kozmikova, Iryna, Permanyer, Jon, Louis, Alexandra, Albuixech-Crespo, Beatriz, Petillon, Yann Le, Leon, Anthony, Subirana, Lucie, Balwierz, Piotr J., Duckett, Paul Edward, Farahani, Ensieh, Aury, Jean‐Marc, Mangenot, Sophie, Wincker, Patrick, Albalat, Ricard, Benito-Gutiérrez, Èlia, Cañestro, Cristian, Castro, Filipe, D’Aniello, Salvatore, Ferrier, David E. K., Huang, Shengfeng, Laudet, Vincent, Marais, Gabriel A.B., Pontarotti, Pierre, Schubert, Michael, Seitz, Hervé, Somorjai, Ildiko, Takahashi, Tokiharu, Mirabeau, Olivier, Xu, Anlong, Yu, Jr-Kai, Carninci, Piero, Martínez-Morales, Juan Ramón, Roest Crollius, Hugues, Kozmik, Zbynek, Weirauch, Matthew T., Garcia-Fernàndez, Jordi, Lister, Ryan, Lenhard, Boris, Holland, Peter W. H., Escrivá, Héctor, Gómez-Skarmeta, José Luis, Irimia, Manuel
Format:	article
Status:	Published version
Publication Date:	2018
Country:	España
Institution:	Consejo Superior de Investigaciones Científicas (CSIC)
Repository:	DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:	oai:digital.csic.es:10261/242299
Online Access:	http://hdl.handle.net/10261/242299
Access Level:	Open access
Keyword:	Amphioxus Ancestral expression Whole-genome duplications Phylotypic period Branchiostoma lanceolatum

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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 Amphioxus Ancestral expression Whole-genome duplications Phylotypic period 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 Maeso, Ignacio Tena, Juan J. Bogdanovic, Ozren Perry, M. Wyatt, Christopher D. R. Calle-Mustienes, Elisa de la Bertrand, Stephanie Burguera, Demian Acemel, Rafael D. Van Heeringen, Simon J. Naranjo, Silvia Herrera-Úbeda, Carlos Skvortsova, Ksenia Jiménez-Gancedo, Sandra Aldea, Daniel Marquez, Yamile Buono, Lorena Kozmikova, Iryna Permanyer, Jon Louis, Alexandra Albuixech-Crespo, Beatriz Petillon, Yann Le Leon, Anthony Subirana, Lucie Balwierz, Piotr J. Duckett, Paul Edward Farahani, Ensieh Aury, Jean‐Marc Mangenot, Sophie Wincker, Patrick Albalat, Ricard Benito-Gutiérrez, Èlia Cañestro, Cristian Castro, Filipe D’Aniello, Salvatore Ferrier, David E. K. Huang, Shengfeng Laudet, Vincent Marais, Gabriel A.B. Pontarotti, Pierre Schubert, Michael Seitz, Hervé Somorjai, Ildiko Takahashi, Tokiharu Mirabeau, Olivier Xu, Anlong Yu, Jr-Kai Carninci, Piero Martínez-Morales, Juan Ramón Roest Crollius, Hugues Kozmik, Zbynek Weirauch, Matthew T. Garcia-Fernàndez, Jordi Lister, Ryan Lenhard, Boris Holland, Peter W. H. Escrivá, Héctor Gómez-Skarmeta, José Luis Irimia, Manuel
author	Marlétaz, Ferdinand
author_facet	Marlétaz, Ferdinand Firbas, Panos Maeso, Ignacio Tena, Juan J. Bogdanovic, Ozren Perry, M. Wyatt, Christopher D. R. Calle-Mustienes, Elisa de la Bertrand, Stephanie Burguera, Demian Acemel, Rafael D. Van Heeringen, Simon J. Naranjo, Silvia Herrera-Úbeda, Carlos Skvortsova, Ksenia Jiménez-Gancedo, Sandra Aldea, Daniel Marquez, Yamile Buono, Lorena Kozmikova, Iryna Permanyer, Jon Louis, Alexandra Albuixech-Crespo, Beatriz Petillon, Yann Le Leon, Anthony Subirana, Lucie Balwierz, Piotr J. Duckett, Paul Edward Farahani, Ensieh Aury, Jean‐Marc Mangenot, Sophie Wincker, Patrick Albalat, Ricard Benito-Gutiérrez, Èlia Cañestro, Cristian Castro, Filipe D’Aniello, Salvatore Ferrier, David E. K. Huang, Shengfeng Laudet, Vincent Marais, Gabriel A.B. Pontarotti, Pierre Schubert, Michael Seitz, Hervé Somorjai, Ildiko Takahashi, Tokiharu Mirabeau, Olivier Xu, Anlong Yu, Jr-Kai Carninci, Piero Martínez-Morales, Juan Ramón Roest Crollius, Hugues Kozmik, Zbynek Weirauch, Matthew T. Garcia-Fernàndez, Jordi Lister, Ryan Lenhard, Boris Holland, Peter W. H. Escrivá, Héctor Gómez-Skarmeta, José Luis Irimia, Manuel
author_role	author
author2	Firbas, Panos Maeso, Ignacio Tena, Juan J. Bogdanovic, Ozren Perry, M. Wyatt, Christopher D. R. Calle-Mustienes, Elisa de la Bertrand, Stephanie Burguera, Demian Acemel, Rafael D. Van Heeringen, Simon J. Naranjo, Silvia Herrera-Úbeda, Carlos Skvortsova, Ksenia Jiménez-Gancedo, Sandra Aldea, Daniel Marquez, Yamile Buono, Lorena Kozmikova, Iryna Permanyer, Jon Louis, Alexandra Albuixech-Crespo, Beatriz Petillon, Yann Le Leon, Anthony Subirana, Lucie Balwierz, Piotr J. Duckett, Paul Edward Farahani, Ensieh Aury, Jean‐Marc Mangenot, Sophie Wincker, Patrick Albalat, Ricard Benito-Gutiérrez, Èlia Cañestro, Cristian Castro, Filipe D’Aniello, Salvatore Ferrier, David E. K. Huang, Shengfeng Laudet, Vincent Marais, Gabriel A.B. Pontarotti, Pierre Schubert, Michael Seitz, Hervé Somorjai, Ildiko Takahashi, Tokiharu Mirabeau, Olivier Xu, Anlong Yu, Jr-Kai Carninci, Piero Martínez-Morales, Juan Ramón Roest Crollius, Hugues Kozmik, Zbynek Weirauch, Matthew T. Garcia-Fernàndez, Jordi Lister, Ryan Lenhard, Boris Holland, Peter W. H. Escrivá, Héctor Gómez-Skarmeta, José Luis Irimia, 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
dc.contributor.none.fl_str_mv	European Research Council European Commission Ministerio de Economía y Competitividad (España) Australian Research Council Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv	Amphioxus Ancestral expression Whole-genome duplications Phylotypic period Branchiostoma lanceolatum
topic	Amphioxus Ancestral expression Whole-genome duplications Phylotypic period 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 http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion
format	article
status_str	publishedVersion
dc.identifier.none.fl_str_mv	http://hdl.handle.net/10261/242299
url	http://hdl.handle.net/10261/242299
dc.language.none.fl_str_mv	Inglés
language_invalid_str_mv	Inglés
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dc.rights.none.fl_str_mv	info:eu-repo/semantics/openAccess
eu_rights_str_mv	openAccess
dc.publisher.none.fl_str_mv	Springer Nature
publisher.none.fl_str_mv	Springer Nature
dc.source.none.fl_str_mv	reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str	Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str	DIGITAL.CSIC. Repositorio Institucional del CSIC
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repository.mail.fl_str_mv
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spelling	Amphioxus functional genomics and the origins of vertebrate gene regulationMarlétaz, FerdinandFirbas, PanosMaeso, IgnacioTena, Juan J.Bogdanovic, OzrenPerry, M.Wyatt, Christopher D. R.Calle-Mustienes, Elisa de laBertrand, StephanieBurguera, DemianAcemel, Rafael D.Van Heeringen, Simon J.Naranjo, SilviaHerrera-Úbeda, CarlosSkvortsova, KseniaJiménez-Gancedo, SandraAldea, DanielMarquez, YamileBuono, LorenaKozmikova, IrynaPermanyer, JonLouis, AlexandraAlbuixech-Crespo, BeatrizPetillon, Yann LeLeon, AnthonySubirana, LucieBalwierz, Piotr J.Duckett, Paul EdwardFarahani, EnsiehAury, Jean‐MarcMangenot, SophieWincker, PatrickAlbalat, RicardBenito-Gutiérrez, ÈliaCañestro, CristianCastro, FilipeD’Aniello, SalvatoreFerrier, David E. K.Huang, ShengfengLaudet, VincentMarais, Gabriel A.B.Pontarotti, PierreSchubert, MichaelSeitz, HervéSomorjai, IldikoTakahashi, TokiharuMirabeau, OlivierXu, AnlongYu, Jr-KaiCarninci, PieroMartínez-Morales, Juan RamónRoest Crollius, HuguesKozmik, ZbynekWeirauch, Matthew T.Garcia-Fernàndez, JordiLister, RyanLenhard, BorisHolland, Peter W. H.Escrivá, HéctorGómez-Skarmeta, José LuisIrimia, ManuelAmphioxusAncestral expressionWhole-genome duplicationsPhylotypic periodBranchiostoma 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.This research was funded primarily by the European Research Council (ERC) under the European Union’s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Economía y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208), the ‘Unidad de Excelencia María de Maetzu 2017-2021’(MDM-2016-0687), the People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program FP7 under REA grant agreement number 607142 (DevCom) to J.L.G.-S., and the CNRS and the ANR (ANR16-CE12-0008-01) to H.E. O.B. was supported by an Australian Research Council Discovery Early Career Researcher Award (DECRA; DE140101962).Springer NatureEuropean Research CouncilEuropean CommissionMinisterio de Economía y Competitividad (España)Australian Research CouncilConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2021202120182021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/242299reponame:DIGITAL.CSIC. 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Amphioxus functional genomics and the origins of vertebrate gene regulation

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