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Cited by 101Genomics and Chromatin DynamicsZebrafish Biomedical Research ApplicationsDevelopmental Biology and Gene Regulation

Multiomic atlas with functional stratification and developmental dynamics of zebrafish cis-regulatory elements

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Baranasic, Damir, Hörtenhuber, Matthias, Balwierz, Piotr J., Zehnder, Tobias, Mukarram, Abdul Kadir, Nepal, Chirag, Várnai, Csilla, Hadzhiev, Yavor +47 more·2022·Nature Genetics
DOI 10.1038/s41588-022-01089-wPMC PMC9279159

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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 Our data coordination center ( https://danio-code.zfin.org ) combines a total of 1,802 sets of unpublished and re-analyzed published genomic data, which we used to improve existing annotations and show its utility in experimental design.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.

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Authors
Baranasic, D., Hörtenhuber, M., Balwierz, P. J., Zehnder, T., Mukarram, A. K., Nepal, C., Várnai, C., Hadzhiev, Y., Jimenez-Gonzalez, A., Li, N., Wragg, J., D’Orazio, F. M., Relic, D., Pachkov, M., Díaz, N., Hernández-Rodríguez, B., Chen, Z., Stoiber, M., Dong, M., Stevens, I., Ross, S. E., Eagle, A., Martin, R., Obasaju, O., Rastegar, S., McGarvey, A. C., Kopp, W., Chambers, E., Wang, D., Kim, H. R., Acemel, R. D., Naranjo, S., Łapiński, M., Chong, V., Mathavan, S., Peers, B., Sauka-Spengler, T., Vingron, M., Carninci, P., Ohler, U., Lacadie, S. A., Burgess, S. M., Winata, C., van Eeden, F., Vaquerizas, J. M., Gómez-Skarmeta, J. L., Onichtchouk, D., Brown, B. J., Bogdanovic, O., van Nimwegen, E., Westerfield, M., Wardle, F. C., Daub, C. O., Lenhard, B., & Müller, F.
Affiliations
  • Karolinska Institutet (SE)
  • Hammersmith Hospital (GB)
  • University of Copenhagen (DK)
  • University of Birmingham (GB)
  • SIB Swiss Institute of Bioinformatics (CH)
  • Max Planck Institute for Molecular Biomedicine (DE)
  • Chinese Academy of Sciences (CN)
  • Lawrence Berkeley National Laboratory (US)
  • Garvan Institute of Medical Research (AU)
  • University of Oregon (US)
  • Karlsruhe Institute of Technology (DE)
  • Max Delbrück Center (DE)
  • University of Sheffield (GB)
  • Singapore Institute for Clinical Sciences (SG)
  • Centro Andaluz de Biología del Desarrollo (ES)
  • International Institute of Molecular and Cell Biology (PL)
  • Sankara Nethralaya (IN)
  • University of Liège (BE)
  • Max Planck Institute for Molecular Genetics (DE)
  • Human Technopole (IT)
  • Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (CN)
  • University of Freiburg (DE)
  • King's College London (GB)
  • Science for Life Laboratory (SE)
Corresponding author
  • Daub, Carsten O.
  • Lenhard, Boris
  • Müller, Ferenc
ORCID
Venue
Nature Genetics
Publisher
Springer Science and Business Media LLC
Published
2022-07
Volume
54
Issue
7
Pages
1037-1050
ISSN
  • 1061-4036 (ISSN-L)
  • 1546-1718
DOI
10.1038/s41588-022-01089-w
PMC
PMC9279159
OpenAlex
W4283789731
Cited by
101
References
12
Citations by year
2026: 19 · 2025: 28 · 2024: 26 · 2023: 15 · 2022: 11 · 2021: 2
FWCI
6.53
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research Portal (King's College London) (publishedVersion, other-oa)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
  • University of Birmingham Research Portal (University of Birmingham) (publishedVersion, cc-by)
  • edoc (University of Basel) (acceptedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
  • MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
  • Repository KITopen (Karlsruhe Institute of Technology) (submittedVersion, cc-by)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • ORBi (University of Liège) (submittedVersion, other-oa)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • KITopen (cc-by)
Funders
  • RCUK | Biotechnology and Biological Sciences Research Council (P61715)
  • EC | Horizon 2020 Framework Programme (643062)
  • Wellcome Trust (106955/Z/15/Z)
  • Rutherford Fund
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
zebrafish, cis-regulatory elements, zygotic genome activation, organogenesis, epigenomic landscape, embryonic development
MeSH terms
Animals, Chromatin, Humans, Regulatory Sequences, Nucleic Acid, Zebrafish, Genome, Gene Expression Regulation, Developmental, Genomics, Zebrafish Proteins, Databases, Genetic, Organogenesis, Mice, Molecular Sequence Annotation

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