Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marletaz, Panos Firbas, Ignacio Maeso, Juan Tena, Ozren Bogdanovic, Malcolm Perry, Chris Wyatt, Elisa de la Calle-Mustienes, Stephanie Bertrand, Demian Burguera, Rafael Acemel, Simon van Heeringen, Silvia Naranjo, Carlos Herrera-Ubeda, Ksenia Skvortsova, Sandra Jimenez-Gancedo, Daniel Aldea, Yamile Marquez, Lorena Buono, Iryna KozmikovaJon Permanyer, Alexandra Louis, Beatriz Albuixech-Crespo, Yann Le Petillon, Anthony Leon Florian, Lucie Subirana, Piotr J. Balwierz, Paul Duckett, Ensieh Farahani, Jean Marc Aury, Sophie Mangenot, Patrick Wincker, Ricard Albalat, Elia Benito-Gutierrez, Cristian Canestro, Filipe Castro, Salvatore D'Aniello, David Ellard Keith Ferrier, Shengfeng Huang, Vincent Laudet, Gabriel Marais, Pierre Pontarotti, Michael Schubert, Herve Seitz, Ildiko Maureen Lara Somorjai, Tokiharu Takahashi, Olivier Mirabeau, Anlong Xu, Jr-Kai Yu, Piero Carninci, Juan Martinez-Morales, Hugues Crollius, Zbynek Kozmik, Matt Weirauch, Jordi Garcia-Fernandez, Ryan Lister, Boris Lenhard, Peter Holland, Hector Escriva, Jose Luis Gomez-Skarmeta, Manuel Irimia

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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.
Original languageEnglish
Pages (from-to)64-70
Number of pages29
JournalNature
Volume564
Issue number7734
DOIs
Publication statusPublished - 21 Nov 2018

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  • Amphioxus functional genomics and the origins of vertebrate gene regulation (Raw genome sequencing data)

    Marletaz, F. (Creator), Firbas, P. (Creator), Maeso, I. (Creator), Tena, J. (Creator), Bogdanovic, O. (Creator), Perry, M. (Creator), Wyatt, C. (Creator), de la Calle-Mustienes, E. (Creator), Bertrand, S. (Creator), Burguera, D. (Creator), Acemel, R. (Creator), van Heeringen, S. (Creator), Naranjo, S. (Creator), Herrera-Ubeda, C. (Creator), Skvortsova, K. (Creator), Jimenez-Gancedo, S. (Creator), Aldea, D. (Creator), Marquez, Y. (Creator), Buono, L. (Creator), Kozmikova, I. (Creator), Permanyer, J. (Creator), Louis, A. (Creator), Albuixech-Crespo, B. (Creator), Le Petillon, Y. (Creator), Leon Florian, A. (Creator), Subirana, L. (Creator), Balwierz, P. J. (Creator), Duckett, P. (Creator), Farahani, E. (Creator), Aury, J. M. (Creator), Mangenot, S. (Creator), Wincker, P. (Creator), Albalat, R. (Creator), Benito-Gutierrez, E. (Creator), Canestro, C. (Creator), Castro, F. (Creator), D'Aniello, S. (Creator), Ferrier, D. E. K. (Creator), Huang, S. (Creator), Laudet, V. (Creator), Marais, G. (Creator), Pontarotti, P. (Creator), Schubert, M. (Creator), Seitz, H. (Creator), Somorjai, I. M. L. (Creator), Takahashi, T. (Creator), Mirabeau, O. (Creator), Xu, A. (Creator), Yu, J. (Creator), Carninci, P. (Creator), Martinez-Morales, J. (Creator), Crollius, H. (Creator), Kozmik, Z. (Creator), Weirauch, M. (Creator), Garcia-Fernandez, J. (Creator), Lister, R. (Creator), Lenhard, B. (Creator), Holland, P. (Creator), Escriva, H. (Creator), Gomez-Skarmeta, J. L. (Creator) & Irimia, M. (Creator), European Nucleotide Archive (ENA), 2018

    Dataset

  • Amphioxus functional genomics and the origins of vertebrate gene regulation (next-generation sequencing data)

    Marletaz, F. (Creator), Firbas, P. (Creator), Maeso, I. (Creator), Tena, J. (Creator), Bogdanovic, O. (Creator), Perry, M. (Creator), Wyatt, C. (Creator), de la Calle-Mustienes, E. (Creator), Bertrand, S. (Creator), Burguera, D. (Creator), Acemel, R. (Creator), van Heeringen, S. (Creator), Naranjo, S. (Creator), Herrera-Ubeda, C. (Creator), Skvortsova, K. (Creator), Jimenez-Gancedo, S. (Creator), Aldea, D. (Creator), Marquez, Y. (Creator), Buono, L. (Creator), Kozmikova, I. (Creator), Permanyer, J. (Creator), Louis, A. (Creator), Albuixech-Crespo, B. (Creator), Le Petillon, Y. (Creator), Leon Florian, A. (Creator), Subirana, L. (Creator), Balwierz, P. J. (Creator), Duckett, P. (Creator), Farahani, E. (Creator), Aury, J. M. (Creator), Mangenot, S. (Creator), Wincker, P. (Creator), Albalat, R. (Creator), Benito-Gutierrez, E. (Creator), Canestro, C. (Creator), Castro, F. (Creator), D'Aniello, S. (Creator), Ferrier, D. E. K. (Creator), Huang, S. (Creator), Laudet, V. (Creator), Marais, G. (Creator), Pontarotti, P. (Creator), Schubert, M. (Creator), Seitz, H. (Creator), Somorjai, I. M. L. (Creator), Takahashi, T. (Creator), Mirabeau, O. (Creator), Xu, A. (Creator), Yu, J. (Creator), Carninci, P. (Creator), Martinez-Morales, J. (Creator), Crollius, H. (Creator), Kozmik, Z. (Creator), Weirauch, M. (Creator), Garcia-Fernandez, J. (Creator), Lister, R. (Creator), Lenhard, B. (Creator), Holland, P. (Creator), Escriva, H. (Creator), Gomez-Skarmeta, J. L. (Creator) & Irimia, M. (Creator), Gene Expression Omnibus (GEO), 15 Aug 2018

    Dataset

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