Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marletaz; Panos N. Firbas; Ignacio Maeso; Juan J. Tena; Ozren Bogdanovic; Malcolm Perry; Christopher D. R. Wyatt; Elisa de La Calle-Mustienes; Stephanie Bertrand; Demian Burguera; Rafael D. Acemel; Simon J. Van 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 Le Petillon; Anthony Leon; Lucie Subirana; Piotr J. Balwierz; Paul Edward Duckett; Ensieh Farahani; Jean-Marc Aury; Sophie Mangenot; Patrick Wincker; Ricard Albalat; Elia Benito-Gutierrez; Cristian Canestro; Filipe Castro; Salvatore d'Aniello; David E. K. Ferrier; Shengfeng Huang; Vincent Laudet; Gabriel A. B. Marais; Pierre Pontarotti; Michael Schubert; Herve 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-Fernandez; Ryan Lister; Boris Lenhard; Peter W. H. Holland; Hector Escriva; Jose Luis Gomez-Skarmeta; Manuel Irimia

doi:10.1038/s41586-018-0734-6

Back

Amphioxus functional genomics and the origins of vertebrate gene regulation

Journal article

Open access

Peer reviewed

Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marletaz, Panos N. Firbas, Ignacio Maeso, Juan J. Tena, Ozren Bogdanovic, Malcolm Perry, Christopher D. R. Wyatt, Elisa de La Calle-Mustienes, Stephanie Bertrand, Demian Burguera, …

Nature, Vol.564(7734), pp.64-70

05/12/2018

DOI: https://doi.org/10.1038/s41586-018-0734-6

PMCID: PMC6292497

PMID: 30464347

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.

Files and links (2)

url

Find in HALView

url

https://doi.org/10.1038/s41586-018-0734-6View

Published (Version of record) Open

Metrics

1 Record Views

Details

Title: Amphioxus functional genomics and the origins of vertebrate gene regulation
Creators - without role: Ferdinand Marletaz - University of Oxford
Panos N. Firbas - Centro Andaluz de Biología del Desarrollo
Ignacio Maeso - Centro Andaluz de Biología del Desarrollo
Juan J. Tena - Centro Andaluz de Biología del Desarrollo
Ozren Bogdanovic - Garvan Institute of Medical Research
Malcolm Perry - Imperial College London
Christopher D. R. Wyatt - Centre for Genomic Regulation
Elisa de La Calle-Mustienes - Centro Andaluz de Biología del Desarrollo
Stephanie Bertrand - Sorbonne Université
Demian Burguera - Centre for Genomic Regulation
Rafael D. Acemel - Centro Andaluz de Biología del Desarrollo
Simon J. Van Heeringen - Radboud University [Nijmegen]
Silvia Naranjo - Centro Andaluz de Biología del Desarrollo
Carlos Herrera-Ubeda - Universitat de Barcelona
Ksenia Skvortsova - Garvan Institute of Medical Research
Sandra Jimenez-Gancedo - Universidad Pablo de Olavide
Daniel Aldea - Biologie Intégrative des Organismes Marins
Yamile Marquez - Centre for Genomic Regulation
Lorena Buono - Junta de Andalucía
Iryna Kozmikova - Czech Academy of Sciences, Institute of Molecular Genetics
Jon Permanyer - Centre for Genomic Regulation
Alexandra Louis - Institut de Biologie de l'École Normale Supérieure
Beatriz Albuixech-Crespo - Universitat de Barcelona
Yann Le Petillon - Biologie Intégrative des Organismes Marins
Anthony Leon - Biologie Intégrative des Organismes Marins
Lucie Subirana - Biologie Intégrative des Organismes Marins
Piotr J. Balwierz - MRC London Institute of Medical Sciences
Paul Edward Duckett - Garvan Institute of Medical Research
Ensieh Farahani - Centro Andaluz de Biología del Desarrollo
Jean-Marc Aury - Laboratoire de Bioinformatique pour la Génomique et la Biodiversité
Sophie Mangenot - Commissariat à l'Énergie Atomique et aux Énergies Alternatives
Patrick Wincker - Université Paris-Saclay
Ricard Albalat - Universitat de Barcelona
Elia Benito-Gutierrez - University of Cambridge
Cristian Canestro - Universitat de Barcelona
Filipe Castro - Universidade do Porto
Salvatore d'Aniello - Stazione Zoologica Anton Dohrn
David E. K. Ferrier - University of St Andrews
Shengfeng Huang - Sun Yat-sen University
Vincent Laudet - Sorbonne Université
Gabriel A. B. Marais - Laboratoire de Biométrie et Biologie Evolutive
Pierre Pontarotti - Méditerranée Infection Foundation
Michael Schubert - Sorbonne Université
Herve Seitz - Université de Montpellier, Institut de Génétique Humaine - IGH
Ildiko Somorjai - University of St Andrews
Tokiharu Takahashi - University of Manchester
Olivier Mirabeau - Université Paris Sciences et Lettres
Anlong Xu - Sun Yat-sen University
Jr-Kai Yu - Academia Sinica
Piero Carninci - RIKEN
Juan Ramon Martinez-Morales - Universidad Pablo de Olavide
Hugues Roest Crollius - Centre National de la Recherche Scientifique
Zbynek Kozmik - Czech Academy of Sciences, Institute of Molecular Genetics
Matthew T. Weirauch - Cincinnati Children's Hospital Medical Center
Jordi Garcia-Fernandez - Universitat de Barcelona
Ryan Lister - Harry Perkins Institute of Medical Research
Boris Lenhard - University of Bergen
Peter W. H. Holland - University of Oxford
Hector Escriva - Sorbonne Université
Jose Luis Gomez-Skarmeta - Universidad Pablo de Olavide
Manuel Irimia - Pompeu Fabra University
Publication Details: Nature, Vol.564(7734), pp.64-70
Identifiers: 9933880009311
Academic Unit: Institut de Génétique Humaine - IGH
Language: English
Resource Type: Journal article
Local Fields: hal-02000511