ArticleNature2018
Amphioxus functional genomics and the origins of vertebrate gene regulation.
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Article in Nature, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 171 papers.
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171citing papers in PubMed
13.2field-weighted citation impact, top 1% of its field
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171 citing papers in PubMed, 321 citations in OpenAlex.
- Developmental contexts of gene-regulatory evolution following whole genome duplication in salmonids.Nature ecology & evolution · 2026Article
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- Internalized Evolutionary Inertia on Body Plan Evolution.Evolution & development · 2026Review
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- Insights into cephalochordate genome and gene evolution from the early-diverging amphioxusProceedings of the National Academy of Sciences of the United States of America · 2026Article
- A cellular basis for the hourglass pattern in vertebrate embryogenesis.Nature communications · 2026Review
- A comprehensive evaluation of long-read de novo transcriptome assembly.Genome biology · 2026Article
- Germline de novo mutation rate of the highly heterozygous amphioxus genome.Molecular biology and evolution · 2026Article
- Expanding the fly eye gene regulatory network: From Drosophila to the hoverfly Episyrphus balteatus.PLoS genetics · 2026Article
- Deep conservation of cis-regulatory elements and chromatin organization in echinoderms uncover ancestral regulatory features of animal genomes.Nature ecology & evolution · 2026Article
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- Evolutionary dynamics of sex determination in Branchiostoma belcheri driven by repeated transposition of a single novel gene.Nature communications · 2026Article
- Decoding cnidarian cell type gene regulation.Nature ecology & evolution · 2026Article
- Evolutionary dynamics of FoxQ2 transcription factors across metazoans reveals three ancient paralogs.Communications biology · 2025Article
- Double stranded RNA sensing is silenced during early embryonic development.Nature communications · 2025Article
- Toward mechanisms underlying the developmental hourglass: evolvability and phylotypic conservation.EvoDevo · 2025Review
- Assessing the Impact of Whole Genome Duplication on Gene Expression and Regulation During Arachnid Development.Genome biology and evolution · 2025Article
- Phenotypic impact of individual conserved neuronal microexons and their master regulators in zebrafish.eLife · 2025Article
- Developmental system drift and modular gene regulatory networks shape gastrulation inLife science alliance · 2025Article
- Cell fate specification modes shape transcriptome evolution in the highly conserved spiral cleavage.EMBO reports · 2025Article
111 more citing papers are in PubMed but not listed here.
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Authors and funding
61 authors at 20 institutions in 13 countries.
Ferdinand MarlétazDepartment of Zoology, University of Oxford, Oxford, UK.
Panos N FirbasCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Ignacio MaesoCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain. nacho.maeso@gmail.com.
Juan J TenaCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Ozren BogdanovicGenomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
Malcolm PerryInstitute of Clinical Sciences, Faculty of Medicine, Imperial College London, London, UK.
Christopher D R WyattCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain.
Elisa de la Calle-MustienesCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Stephanie BertrandBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
Demian BurgueraCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain.
Rafael D AcemelCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Simon J van HeeringenDepartment of Molecular Developmental Biology, Faculty of Science, Radboud Institute for Molecular Life Sciences, Radboud University, Nijmegen, The Netherlands.
Silvia NaranjoCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Carlos Herrera-UbedaDepartment of Genetics, Microbiology and Statistics, Faculty of Biology, and Institut de Biomedicina (IBUB), University of Barcelona, Barcelona, Spain.
Ksenia SkvortsovaGenomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
Sandra Jimenez-GancedoCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Daniel AldeaBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
Yamile MarquezCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain.
Lorena BuonoCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Iryna KozmikovaInstitute of Molecular Genetics of the Czech Academy of Sciences, Prague, Czech Republic.
Jon PermanyerCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain.
Alexandra LouisInstitut de Biologie de l'ENS, IBENS, Ecole Normale Supérieure, Paris, France.
Beatriz Albuixech-CrespoDepartment of Genetics, Microbiology and Statistics, Faculty of Biology, and Institut de Biomedicina (IBUB), University of Barcelona, Barcelona, Spain.
Yann Le PetillonBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
Anthony LeonBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
Lucie SubiranaBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
Piotr J BalwierzInstitute of Clinical Sciences, Faculty of Medicine, Imperial College London, London, UK.
Paul Edward DuckettGenomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
Ensieh FarahaniCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Jean-Marc AuryGenoscope, Institut de biologie François-Jacob, Commissariat à l'Energie Atomique (CEA), Université Paris-Saclay, Evry, France.
Sophie MangenotGenoscope, Institut de biologie François-Jacob, Commissariat à l'Energie Atomique (CEA), Université Paris-Saclay, Evry, France.
Patrick WinckerGénomique Métabolique, Genoscope, Institut de biologie François Jacob, Commissariat à l'Energie Atomique (CEA), CNRS, Université Evry, Université Paris-Saclay, Evry, France.
Ricard AlbalatDepartment of Genetics, Microbiology and Statistics, Faculty of Biology and Institut de Recerca de la Biodiversitat (IRBio), University of Barcelona, Barcelona, Spain.
Èlia Benito-GutiérrezDepartment of Zoology, University of Cambridge, Cambridge, UK.
Cristian CañestroDepartment of Genetics, Microbiology and Statistics, Faculty of Biology and Institut de Recerca de la Biodiversitat (IRBio), University of Barcelona, Barcelona, Spain.
Filipe CastroInterdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR) and Faculty of Sciences (FCUP), Department of Biology, University of Porto, Porto, Portugal.
Salvatore D'AnielloBiology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn Napoli, Naples, Italy.
David E K FerrierThe Scottish Oceans Institute, Gatty Marine Laboratory, University of St Andrews, St Andrews, UK.
Shengfeng HuangState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
Vincent LaudetBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France.
Gabriel A B MaraisLaboratoire de Biométrie et Biologie Evolutive (UMR 5558), CNRS and Université Lyon 1, Villeurbanne, France.
Pierre PontarottiIRD, APHM, Microbe, Evolution, PHylogénie, Infection, IHU Méditerranée Infection and CNRS, Aix Marseille University, Marseille, France.
Michael SchubertSorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Institut de la Mer de Villefranche-sur-Mer, Villefranche-sur-Mer, France.
Hervé SeitzUMR 9002 CNRS, Institut de Génétique Humaine, Université de Montpellier, Montpellier, France.
Ildiko SomorjaiBiomedical Sciences Research Complex, School of Biology, University of St Andrews, St Andrews, UK.
Tokiharu TakahashiSchool of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.
Olivier MirabeauINSERM U830, Équipe Labellisée LNCC, SIREDO Oncology Centre, Institut Curie, PSL Research University, Paris, France.
Anlong XuState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
Jr-Kai YuInstitute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan.
Piero CarninciRIKEN Center for Life Science Technologies (Division of Genomic Technologies) (CLST DGT), Yokohama, Japan.
Juan Ramon Martinez-MoralesCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.
Hugues Roest CrolliusInstitut de Biologie de l'ENS, IBENS, Ecole Normale Supérieure, Paris, France.
Zbynek KozmikInstitute of Molecular Genetics of the Czech Academy of Sciences, Prague, Czech Republic.
Matthew T WeirauchCenter for Autoimmune Genomics and Etiology, Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Jordi Garcia-FernàndezDepartment of Genetics, Microbiology and Statistics, Faculty of Biology, and Institut de Biomedicina (IBUB), University of Barcelona, Barcelona, Spain.
Ryan ListerAustralian Research Council Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Crawley, Western Australia, Australia.
Boris LenhardInstitute of Clinical Sciences, Faculty of Medicine, Imperial College London, London, UK.
Peter W H HollandDepartment of Zoology, University of Oxford, Oxford, UK.
Hector EscrivaBiologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, CNRS and Sorbonne Université, Banyuls sur Mer, France. hescriva@obs-banyuls.fr.
Jose Luis Gómez-SkarmetaCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain. jlgomska@upo.es.
Manuel IrimiaCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, Spain. mirimia@gmail.com.
Universidad Pablo de Olavide · ESUniversitat de Barcelona · ESCentro Andaluz de Biología del Desarrollo · ESBiologie Intégrative des Organismes Marins · FRCentre for Genomic Regulation · ESCentre National de la Recherche Scientifique · FRSorbonne Université · FRCEA Paris-Saclay · FRCzech Academy of Sciences, Institute of Molecular Genetics · CZGarvan Institute of Medical Research · AUInserm · FRUniversitat Pompeu Fabra · ESUniversity of Oxford · GBUniversity of St Andrews · GBBeijing University of Chinese Medicine · CNGenomics (United Kingdom) · GBGenoscope · FRHarry Perkins Institute of Medical Research · AUImperial College London · GBInstitut de Génétique Humaine · FR
Funding
Medical Research Council MC_UP_1102/1
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.
Indexed as
Gene Expression RegulationGenomicsAnimalsBody PatterningDNA MethylationHumansLanceletsMolecular Sequence AnnotationPromoter Regions, GeneticTranscriptomeVertebrates
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