Amphioxus functional genomics and the origins of vertebrate gene regulation

Ferdinand Marlétaz Panos Firbas Ignacio Maeso 1 Juan Tena 2 Ozren Bogdanovic Malcolm Perry Christopher Wyatt Elisa de la Calle-Mustienes Stéphanie Bertrand Demian Burguera Rafael Acemel Simon van Heeringen Silvia Naranjo Carlos Herrera-Úbeda 3 Ksenia Skvortsova Sandra Jimenez-Gancedo Daniel Aldea 4 Yamile Marquez 5 Lorena Buono Iryna Kozmikova Jon Permanyer 1 Alexandra Louis 6 Beatriz Albuixech-Crespo Yann Le Pétillon 7 Anthony Léon 8 Lucie Subirana 4 Piotr Balwierz Paul Edward Duckett Ensieh Farahani Jean-Marc Aury 9 Sophie Mangenot 10 Patrick Wincker 11 Ricard Albalat 1 Èlia Benito-Gutiérrez Cristian Cañestro 12 Filipe Castro 13 Salvatore D’aniello David Ferrier Shengfeng Huang 14 Vincent Laudet 15 Gabriel Marais 16 Pierre Pontarotti 17 Michael Schubert 18 Hervé Seitz 19 Ildikó Somorjai 20 Tokiharu Takahashi Olivier Mirabeau 21 Anlong Xu 22 Jr-Kai Yu 23 Piero Carninci 24 Juan Martínez-Morales 2 Hugues Roest Crollius 6 Zbynek Kozmik Matthew Weirauch Jordi Garcia-Fernàndez 3 Ryan Lister 25 Boris Lenhard 26 Peter Holland Hector Escriva 27 José Luis Gomez-Skarmeta 2 Manuel Irimia
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 Marlétaz, Panos Firbas, Ignacio Maeso, Juan 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-02145578⟩

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