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Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marletaz 1, 2 Panos N. Firbas 3 Ignacio Maeso 3 Juan J. Tena 3 Ozren Bogdanovic 4, 5 Malcolm Perry 6 Christopher D. R. Wyatt 7 Elisa Calle-Mustienes 3 Stephanie Bertrand 8 Demian Burguera 9 Rafael D. Acemel 10 Simon J. Heeringen 11 Silvia Naranjo 10 Carlos Herrera-Ubeda 12 Ksenia Skvortsova 13 Sandra Jimenez-Gancedo 10 Daniel Aldea 8 Yamile Marquez 9 Lorena Buono 10 Iryna Kozmikova 14 Jon Permanyer 9 Alexandra Louis 15 Beatriz Albuixech-Crespo 12 Yann Le Petillon 8 Anthony Leon 8 Lucie Subirana 8 Piotr J. Balwierz 6 Paul Edward Duckett 13 Ensieh Farahani 10 Jean-Marc Aury 16 Sophie Mangenot 16 Patrick Wincker 16 Ricard Albalat 17 Elia Benito-Gutierrez 18 Cristian Canestro 17 Filipe Castro 19 Salvatore d'Aniello 20 David E. K. Ferrier 21 Shengfeng Huang 22 Vincent Laudet 8 Gabriel A. B. Marais 23 Pierre Pontarotti 24 Michael Schubert 25 Herve Seitz 26 Ildiko Somorjai 21 Tokiharu Takahashi 27 Olivier Mirabeau 28 Anlong Xu 22 Jr-Kai Yu 29 Piero Carninci 30 Juan Ramon Martinez-Morales 10 Hugues Roest Crollius 15 Zbynek Kozmik 14 Matthew T. Weirauch 31 Jordi Garcia-Fernandez 12 Ryan Lister 5 Boris Lenhard 6, 32 Peter W. H. Holland 33 Hector Escriva 8 Jose Luis Gomez-Skarmeta 10 Manuel Irimia 9, 7
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.
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Ferdinand Marletaz, Panos N. Firbas, Ignacio Maeso, Juan J. Tena, Ozren Bogdanovic, et al.. Amphioxus functional genomics and the origins of vertebrate gene regulation. Nature, Nature Publishing Group, 2018, 564 (7734), pp.64-70. ⟨10.1038/s41586-018-0734-6⟩. ⟨hal-02000511⟩

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