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Publication . Article . 2018

Amphioxus functional genomics and the origins of vertebrate gene regulation.

Ferdinand Marlétaz; Panos N. Firbas; Ignacio Maeso; Juan J. Tena; Ozren Bogdanovic; Malcolm Perry; Christopher D. R. Wyatt; +54 Authors
Open Access
English
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.

This research was funded primarily by the European Research Council (ERC) under the European Union’s Horizon 2020 and Seventh Framework Program FP7 research and innovation programs (ERC-AdG-LS8-740041 to J.L.G.-S., ERC-StG-LS2-637591 to M.I., a Marie Sklodowska-Curie Grant (658521) to I.M. and a FP7/2007-2013-ERC-268513 to P.W.H.H.), the Spanish Ministerio de Economía y Competitividad (BFU2016-74961-P to J.L.G.-S., RYC-2016-20089 to I.M., BFU2014-55076-P and BFU2017-89201-P to M.I. and BFU2014-55738-REDT to J.L.G.-S, M.I. and J.R.M.-M), the ‘Centro de Excelencia Severo Ochoa 2013-2017’(SEV-2012-0208), the ‘Unidad de Excelencia María de Maetzu 2017-2021’(MDM-2016-0687), the People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program FP7 under REA grant agreement number 607142 (DevCom) to J.L.G.-S., and the CNRS and the ANR (ANR16-CE12-0008-01) to H.E. O.B. was supported by an Australian Research Council Discovery Early Career Researcher Award (DECRA; DE140101962).

Subjects by Vocabulary

ACM Computing Classification System: ComputingMilieux_MISCELLANEOUS

Microsoft Academic Graph classification: Genomics Functional genomics Gene duplication Biology Regulation of gene expression Subfunctionalization Vertebrate biology.animal Branchiostoma biology.organism_classification Evolutionary biology Genome

Subjects

Animals, Vertebrates, Humans, Genomics, DNA Methylation, Gene Expression Regulation, Body Patterning, Promoter Regions, Genetic, Molecular Sequence Annotation, Transcriptome, Lancelets, [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases, [SDV.BDD.EO]Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis, Vertebrats, Amfiox, Branchiostoma lanceolatum, Amphioxus, Ancestral expression, Whole-genome Duplication (WGD), Phylotypic Period, Multidisciplinary, Epigenomics, Functional genomics, Molecular evolution, Article, whole genome duplication, regulatory genomics, transcriptomics, DDC model, hourglass model, chordate evolution, comparative study, developmental stage, evolution, gene, gene expression, genetic analysis, innovation, invertebrate, specialization, vertebrate, adult, animal cell, animal tissue, Article, Branchiostoma, chromatin, controlled study, embryo, embryo development, female, gene control, gene duplication, gene sequence, genome, histone modification, male, molecular genetics, mouse, multigene family, nonhuman, priority journal, zebra fish, Vertebrata, Amphioxus, Ancestral expression, Whole-genome Duplication (WGD), Phylotypic Period, Branchiostoma Lanceolatum, Animals, Vertebrates, Humans, Genomics, DNA Methylation, Gene Expression Regulation, Body Patterning, Promoter Regions, Genetic, Molecular Sequence Annotation, Transcriptome, Lancelets, Epigenomics, Functional genomics, Molecular evolution, QH426 Genetics, DAS, QH426, Science & Technology, Multidisciplinary Sciences, Science & Technology - Other Topics, BRANCHIOSTOMA-LANCEOLATUM, DNA DEMETHYLATION, CHROMATIN, EVOLUTION, SEQ, CONSERVATION, LANDSCAPES, ZEBRAFISH, PLURIPOTENCY, TRANSGENESIS, General Science & Technology

Funded byView all
EC| Evoland
Project
Evoland
Evolution of regulatory landscapes at multiple timescales
  • Funder: European Commission (EC)
  • Project Code: 740041
  • Funding stream: H2020 | ERC | ERC-ADG
Validated by funder
,
EC| BLUEandGREEN
Project
BLUEandGREEN
Boosting scientific excellence and innovation capacity in biorefineries based on marine resources
  • Funder: European Commission (EC)
  • Project Code: 692419
  • Funding stream: H2020 | CSA
Validated by funder
,
EC| GENEVA
Project
GENEVA
Genome Evolution in the Animal Kingdom
  • Funder: European Commission (EC)
  • Project Code: 268513
  • Funding stream: FP7 | SP2 | ERC
,
EC| DEVCOM
Project
DEVCOM
European Initial Training Network on Developmental and Computational Biology
  • Funder: European Commission (EC)
  • Project Code: 607142
  • Funding stream: FP7 | SP3 | PEOPLE
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