ArticleNature genetics2022
Multiomic atlas with functional stratification and developmental dynamics of zebrafish cis-regulatory elements.
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Article in Nature genetics, 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 56 papers.
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56citing papers in PubMed
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Who cites it
56 citing papers in PubMed.
- Developmental contexts of gene-regulatory evolution following whole genome duplication in salmonids.Nature ecology & evolution · 2026Article
- Comparative analysis of conserved non-coding elements identifies gene regulatory networks rewired during the water-to-land transition in vertebrates.Biologia futura · 2026Article
- Genomic repeats for single-cell molecular recording.bioRxiv : the preprint server for biology · 2026Article
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- Multiple cis-regulatory elements collaborate to control mdka expression in telencephalic neural stem cells of adult zebrafish during constitutive and regenerative neurogenesis.The FEBS journal · 2026Article
- Single-cell ATAC-seq analysis of human embryoid bodies reveals crucial transcription factor networks involved in early germ layer specification.Cell & bioscience · 2026Article
- Single-cell chromatin profiling reveals dynamic regulatory logic and enhancer elements in brain and retina development.bioRxiv : the preprint server for biology · 2026Article
- Ontogeny Dictates Oncogenic Potential, Lineage Hierarchy, and Therapy Response in Pediatric Leukemia.Cancer discovery · 2026Article
- A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape.Innovation (Cambridge (Mass.)) · 2026Article
- Teleosts as Models for Epigenetic Inheritance.Molecular ecology · 2026Review
- Extrusion fountains are hallmarks of chromosome organization emerging upon zygotic genome activation.Nature communications · 2026Article
- Evaluation of eef1a1l1 expression stability and promoter-driven reporter activity during zebrafish development.microPublication biology · 2026Article
- Recommendations of the Polish Zebrafish Society on the use of the zebrafish (Acta biochimica Polonica · 2026Review
- Impact of dietary composition on behavioural expression and gut microbiome dynamics in zebrafish.Pflugers Archiv : European journal of physiology · 2025Article
- Alternative Vertebrate and Invertebrate Model Organisms Show Similar Sensitivity as Rodents to a Diverse Set of Chemicals.Environmental science & technology · 2025Article
- Systematic enhancer mapping and functional analysis in zebrafish with optimized CRISPR interference.Nucleic acids research · 2025Article
- CompletebioRxiv : the preprint server for biology · 2025Article
- Cell type-independent timekeeping gene modules enable embryonic stage prediction in zebrafish.bioRxiv : the preprint server for biology · 2025Article
- Zebrafish in the spotlight: expanding Frontiers in toxicology and drug discovery.Toxicology research · 2025Review
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Authors and funding
55 authors.
Damir Baranasic *MRC London Institute of Medical Sciences, London, UK.ORCID http://orcid.org/0000-0001-5948-0932
Matthias Hörtenhuber *Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden.ORCID http://orcid.org/0000-0002-5599-5565
Piotr J Balwierz *MRC London Institute of Medical Sciences, London, UK.ORCID http://orcid.org/0000-0002-1548-4605
Tobias Zehnder *MRC London Institute of Medical Sciences, London, UK.ORCID http://orcid.org/0000-0002-4127-2673
Abdul Kadir Mukarram *Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden.
Chirag NepalBiotech Research and Innovation Centre (BRIC), Department of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
Csilla VárnaiInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.ORCID http://orcid.org/0000-0003-0048-9507
Yavor HadzhievInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.ORCID http://orcid.org/0000-0002-1134-4904
Ada Jimenez-GonzalezInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.ORCID http://orcid.org/0000-0001-7702-6135
Nan LiInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.ORCID http://orcid.org/0000-0002-8919-2357
Joseph WraggInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.
Fabio M D'OrazioInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.
Dorde RelicBiozentrum, University of Basel and Swiss Institute of Bioinformatics, Basel, Switzerland.ORCID http://orcid.org/0000-0001-6237-3345
Mikhail PachkovBiozentrum, University of Basel and Swiss Institute of Bioinformatics, Basel, Switzerland.ORCID http://orcid.org/0000-0001-7616-6435
Noelia DíazMax Planck Institute for Molecular Biomedicine, Muenster, Germany.ORCID http://orcid.org/0000-0002-0319-3448
Benjamín Hernández-RodríguezMax Planck Institute for Molecular Biomedicine, Muenster, Germany.ORCID http://orcid.org/0000-0002-5118-8715
Zelin ChenTranslational and Functional Genomics Branch, National Human Genome Research Institute, Bethesda, MD, USA.ORCID http://orcid.org/0000-0002-8376-7367
Marcus StoiberEnvironmental Genomics & Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Michaël DongDepartment of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden.ORCID http://orcid.org/0000-0003-4084-3099
Irene StevensDepartment of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden.ORCID http://orcid.org/0000-0003-3823-1499
Samuel E RossGenomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.
Anne EagleInstitute of Neuroscience, University of Oregon, Eugene, OR, USA.
Ryan MartinInstitute of Neuroscience, University of Oregon, Eugene, OR, USA.
Oluwapelumi ObasajuInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK.ORCID http://orcid.org/0000-0001-5952-3103
Sepand RastegarInstitute of Biological and Chemical Systems - Biological Information Processing (IBCS-BIP), Karlsruhe Institute of Technology, Karlsruhe, Germany.ORCID http://orcid.org/0000-0003-4411-5646
Alison C McGarveyMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany.
Wolfgang KoppMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany.ORCID http://orcid.org/0000-0003-0376-0032
Emily ChambersSheffield Bioinformatics Core, Sheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, UK.ORCID http://orcid.org/0000-0003-1252-8059
Dennis WangSheffield Bioinformatics Core, Sheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, UK.ORCID http://orcid.org/0000-0003-0068-1005
Hyejeong R KimBateson Centre/Biomedical Science, University of Sheffield, Sheffield, UK.
Rafael D AcemelCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.ORCID http://orcid.org/0000-0003-4120-0140
Silvia NaranjoCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.ORCID http://orcid.org/0000-0002-4529-3332
Maciej ŁapińskiInternational Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland.ORCID http://orcid.org/0000-0003-4892-976X
Vanessa ChongMRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK.ORCID http://orcid.org/0000-0002-2547-3694
Sinnakaruppan MathavanVision Research Foundation, Sankara Nethralayas, Chennai, India.
Bernard PeersLaboratory of Zebrafish Development and Disease Models (ZDDM), GIGA-R, SART TILMAN, University of Liège, Liège, Belgium.
Tatjana Sauka-SpenglerMRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK.ORCID http://orcid.org/0000-0001-9289-0263
Martin VingronMax Planck Institute for Molecular Genetics, Department of Computational Molecular Biology, Berlin, Germany.ORCID http://orcid.org/0000-0002-1765-4241
Piero CarninciLaboratory for Transcriptome Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.ORCID http://orcid.org/0000-0001-7202-7243
Uwe OhlerMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany.ORCID http://orcid.org/0000-0002-0881-3116
Scott Allen LacadieMax-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany.
Shawn M BurgessSouthern Marine Science and Engineering Guangdong Laboratory, Guangzhou, China.ORCID http://orcid.org/0000-0003-1147-0596
Cecilia WinataInternational Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland.ORCID http://orcid.org/0000-0002-7718-5248
Freek van EedenBateson Centre/Biomedical Science, University of Sheffield, Sheffield, UK.ORCID http://orcid.org/0000-0003-3483-8269
Juan M VaquerizasMRC London Institute of Medical Sciences, London, UK.ORCID http://orcid.org/0000-0002-6583-6541
José Luis Gómez-SkarmetaCentro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain.ORCID http://orcid.org/0000-0001-5125-4332
Daria OnichtchoukDepartment of Developmental Biology, Signalling Research Centers BIOSS and CIBSS, University of Freiburg, Freiburg, Germany.ORCID http://orcid.org/0000-0001-6497-1445
Ben James BrownEnvironmental Genomics & Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.ORCID http://orcid.org/0000-0002-5898-5848
Ozren BogdanovicGenomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia.ORCID http://orcid.org/0000-0001-5680-0056
Erik van NimwegenBiozentrum, University of Basel and Swiss Institute of Bioinformatics, Basel, Switzerland.ORCID http://orcid.org/0000-0001-6338-1312
Monte WesterfieldInstitute of Neuroscience, University of Oregon, Eugene, OR, USA.ORCID http://orcid.org/0000-0003-1187-7839
Fiona C WardleRandall Centre for Cell & Molecular Biophysics, Guy's Campus, King's College London, London, UK.ORCID http://orcid.org/0000-0001-5444-1889
Carsten O DaubDepartment of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden. carsten.daub@ki.se.ORCID http://orcid.org/0000-0002-3295-8729
Boris LenhardMRC London Institute of Medical Sciences, London, UK. b.lenhard@imperial.ac.uk.ORCID http://orcid.org/0000-0002-1114-1509
Ferenc MüllerInstitute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK. f.mueller@bham.ac.uk.ORCID http://orcid.org/0000-0002-0996-774X
Funding
Zebrafish targeted mutagenesis and functional genomicsZIAHG000183 · NHGRI · NATIONAL HUMAN GENOME RESEARCH INSTITUTE · PI BURGESS, SHAWN M · 2009 to 2025
$16.7MZFIN: The Zebrafish Model Organism DatabaseU24HG002659 · NHGRI · UNIVERSITY OF OREGON · PI WESTERFIELD, MONTE · 2021 to 2025
$10.8MBiotechnology and Biological Sciences Research Council BB/R015457/1Biotechnology and Biological Sciences Research Council P61715Medical Research Council MC_EX_MR/S300007/1Medical Research Council MC_UP_1102/1Medical Research Council MC_UP_1605/10NHGRI NIH HHS U24 HG002659Wellcome Trust 106955
Abstract
Zebrafish, a popular organism for studying embryonic development and for modeling human diseases, has so far lacked a systematic functional annotation program akin to those in other animal models. To address this, we formed the international DANIO-CODE consortium and created a central repository to store and process zebrafish developmental functional genomic data. Our data coordination center ( https://danio-code.zfin.org ) combines a total of 1,802 sets of unpublished and re-analyzed published genomic data, which we used to improve existing annotations and show its utility in experimental design. We identified over 140,000 cis-regulatory elements throughout development, including classes with distinct features dependent on their activity in time and space. We delineated the distinct distance topology and chromatin features between regulatory elements active during zygotic genome activation and those active during organogenesis. Finally, we matched regulatory elements and epigenomic landscapes between zebrafish and mouse and predicted functional relationships between them beyond sequence similarity, thus extending the utility of zebrafish developmental genomics to mammals.
Indexed as
Databases, GeneticGene Expression Regulation, DevelopmentalGenomeGenomicsRegulatory Sequences, Nucleic AcidZebrafishZebrafish ProteinsAnimalsChromatinHumansMiceMolecular Sequence AnnotationOrganogenesisChromatinZebrafish Proteins
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