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Nature. 2018 Dec;564(7734):64-70. doi: 10.1038/s41586-018-0734-6. Epub 2018 Nov 21.

Amphioxus functional genomics and the origins of vertebrate gene regulation.

Author information

1
Department of Zoology, University of Oxford, Oxford, UK.
2
Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Japan.
3
Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
4
Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain. nacho.maeso@gmail.com.
5
Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
6
St Vincent's Clinical School, Faculty of Medicine, University of New South Wales, Sydney, New South Wales, Australia.
7
Australian Research Council Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Crawley, Western Australia, Australia.
8
Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London, UK.
9
Computational Regulatory Genomics, MRC London Institute of Medical Sciences, London, UK.
10
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain.
11
Universitat Pompeu Fabra (UPF), Barcelona, Spain.
12
Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
13
Department of Genetics, Microbiology and Statistics, Faculty of Biology, and Institut de Biomedicina (IBUB), University of Barcelona, Barcelona, Spain.
14
Department of Molecular Developmental Biology, Faculty of Science, Radboud Institute for Molecular Life Sciences, Radboud University, Nijmegen, The Netherlands.
15
Institute of Molecular Genetics of the Czech Academy of Sciences, Prague, Czech Republic.
16
Institut de Biologie de l'ENS, IBENS, Ecole Normale Supérieure, Paris, France.
17
Inserm, U1024, Paris, France.
18
CNRS, UMR 8197, Paris, France.
19
Genoscope, Institut de biologie François-Jacob, Commissariat à l'Energie Atomique (CEA), Université Paris-Saclay, Evry, France.
20
Génomique Métabolique, Genoscope, Institut de biologie François Jacob, Commissariat à l'Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, Evry, France.
21
Department of Genetics, Microbiology and Statistics, Faculty of Biology and Institut de Recerca de la Biodiversitat (IRBio), University of Barcelona, Barcelona, Spain.
22
Department of Zoology, University of Cambridge, Cambridge, UK.
23
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR) and Faculty of Sciences (FCUP), Department of Biology, University of Porto, Porto, Portugal.
24
Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn Napoli, Naples, Italy.
25
The Scottish Oceans Institute, Gatty Marine Laboratory, University of St Andrews, St Andrews, UK.
26
State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
27
Laboratoire de Biométrie et Biologie Evolutive (UMR 5558), CNRS and Université Lyon 1, Villeurbanne, France.
28
IRD, APHM, Microbe, Evolution, PHylogénie, Infection, IHU Méditerranée Infection and CNRS, Aix Marseille University, Marseille, France.
29
Sorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Institut de la Mer de Villefranche-sur-Mer, Villefranche-sur-Mer, France.
30
UMR 9002 CNRS, Institut de Génétique Humaine, Université de Montpellier, Montpellier, France.
31
Biomedical Sciences Research Complex, School of Biology, University of St Andrews, St Andrews, UK.
32
School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.
33
INSERM U830, Équipe Labellisée LNCC, SIREDO Oncology Centre, Institut Curie, PSL Research University, Paris, France.
34
School of Life Sciences, Beijing University of Chinese Medicine, Beijing, China.
35
Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan.
36
RIKEN Center for Life Science Technologies (Division of Genomic Technologies) (CLST DGT), Yokohama, Japan.
37
Laboratory for Transcriptome Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
38
Center for Autoimmune Genomics and Etiology, Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
39
Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA.
40
Harry Perkins Institute of Medical Research, Nedlands, Western Australia, Australia.
41
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
42
Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France. hescriva@obs-banyuls.fr.
43
Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain. jlgomska@upo.es.
44
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain. mirimia@gmail.com.
45
Universitat Pompeu Fabra (UPF), Barcelona, Spain. mirimia@gmail.com.

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.

PMID:
30464347
DOI:
10.1038/s41586-018-0734-6

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