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Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marlétaz, Panos N. Firbas, Ignacio Maeso (), Juan J. Tena, Ozren Bogdanovic, Malcolm Perry, Christopher D. R. Wyatt, Elisa Calle-Mustienes, Stephanie Bertrand, Demian Burguera, Rafael D. Acemel, Simon J. Heeringen, Silvia Naranjo, Carlos Herrera-Ubeda, Ksenia Skvortsova, Sandra Jimenez-Gancedo, Daniel Aldea, Yamile Marquez, Lorena Buono, Iryna Kozmikova, Jon Permanyer, Alexandra Louis, Beatriz Albuixech-Crespo, Yann Petillon, Anthony Leon, Lucie Subirana, Piotr J. Balwierz, Paul Edward Duckett, Ensieh Farahani, Jean-Marc Aury, Sophie Mangenot, Patrick Wincker, Ricard Albalat, Èlia Benito-Gutiérrez, Cristian Cañestro, Filipe Castro, Salvatore D’Aniello, David E. K. Ferrier, Shengfeng Huang, Vincent Laudet, Gabriel A. B. Marais, Pierre Pontarotti, Michael Schubert, Hervé Seitz, Ildiko Somorjai, Tokiharu Takahashi, Olivier Mirabeau, Anlong Xu, Jr-Kai Yu, Piero Carninci, Juan Ramon Martinez-Morales, Hugues Roest Crollius, Zbynek Kozmik, Matthew T. Weirauch, Jordi Garcia-Fernàndez, Ryan Lister, Boris Lenhard, Peter W. H. Holland, Hector Escriva (), Jose Luis Gómez-Skarmeta () and Manuel Irimia ()
Additional contact information
Ferdinand Marlétaz: University of Oxford
Panos N. Firbas: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Ignacio Maeso: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Juan J. Tena: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Ozren Bogdanovic: Genomics and Epigenetics Division, Garvan Institute of Medical Research
Malcolm Perry: Imperial College London
Christopher D. R. Wyatt: Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Elisa Calle-Mustienes: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Stephanie Bertrand: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Demian Burguera: Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Rafael D. Acemel: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Simon J. Heeringen: Radboud University
Silvia Naranjo: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Carlos Herrera-Ubeda: University of Barcelona
Ksenia Skvortsova: Genomics and Epigenetics Division, Garvan Institute of Medical Research
Sandra Jimenez-Gancedo: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Daniel Aldea: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Yamile Marquez: Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Lorena Buono: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Iryna Kozmikova: Institute of Molecular Genetics of the Czech Academy of Sciences
Jon Permanyer: Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
Alexandra Louis: Institut de Biologie de l’ENS, IBENS, Ecole Normale Supérieure
Beatriz Albuixech-Crespo: University of Barcelona
Yann Petillon: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Anthony Leon: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Lucie Subirana: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Piotr J. Balwierz: Imperial College London
Paul Edward Duckett: Genomics and Epigenetics Division, Garvan Institute of Medical Research
Ensieh Farahani: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Jean-Marc Aury: Genoscope, Institut de biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay
Sophie Mangenot: Genoscope, Institut de biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay
Patrick Wincker: Génomique Métabolique, Genoscope, Institut de biologie François Jacob, Commissariat à l’Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay
Ricard Albalat: University of Barcelona
Èlia Benito-Gutiérrez: University of Cambridge
Cristian Cañestro: University of Barcelona
Filipe Castro: University of Porto
Salvatore D’Aniello: Stazione Zoologica Anton Dohrn Napoli
David E. K. Ferrier: University of St Andrews
Shengfeng Huang: Sun Yat-sen University
Vincent Laudet: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Gabriel A. B. Marais: Laboratoire de Biométrie et Biologie Evolutive (UMR 5558), CNRS and Université Lyon 1
Pierre Pontarotti: IRD, APHM, Microbe, Evolution, PHylogénie, Infection, IHU Méditerranée Infection and CNRS, Aix Marseille University
Michael Schubert: Institut de la Mer de Villefranche-sur-Mer
Hervé Seitz: UMR 9002 CNRS, Institut de Génétique Humaine, Université de Montpellier
Ildiko Somorjai: University of St Andrews
Tokiharu Takahashi: University of Manchester
Olivier Mirabeau: INSERM U830, Équipe Labellisée LNCC, SIREDO Oncology Centre, Institut Curie, PSL Research University
Anlong Xu: Sun Yat-sen University
Jr-Kai Yu: Academia Sinica
Piero Carninci: RIKEN Center for Life Science Technologies (Division of Genomic Technologies) (CLST DGT)
Juan Ramon Martinez-Morales: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Hugues Roest Crollius: Institut de Biologie de l’ENS, IBENS, Ecole Normale Supérieure
Zbynek Kozmik: Institute of Molecular Genetics of the Czech Academy of Sciences
Matthew T. Weirauch: Cincinnati Children’s Hospital Medical Center
Jordi Garcia-Fernàndez: University of Barcelona
Ryan Lister: The University of Western Australia
Boris Lenhard: Imperial College London
Peter W. H. Holland: University of Oxford
Hector Escriva: Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université
Jose Luis Gómez-Skarmeta: Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía
Manuel Irimia: Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)

Nature, 2018, vol. 564, issue 7734, 64-70

Abstract: Abstract 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.

Keywords: Amphioxus; Ancestral Expression; Whole-genome Duplication (WGD); Phylotypic Period; Branchiostoma Lanceolatum (search for similar items in EconPapers)
Date: 2018
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Citations: View citations in EconPapers (2)

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DOI: 10.1038/s41586-018-0734-6

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