[en] 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 Our data coordination center ( https://danio-code.zfin.org ) combines a total of 1,802 sets of unpublished and re-analyzed published genomic data, which we used to improve existing annotations and show its utility in experimental design.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.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Baranasic, Damir ; MRC London Institute of Medical Sciences, London, UK ; Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, London, UK
Hörtenhuber, Matthias ; Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden
Balwierz, Piotr J ; MRC London Institute of Medical Sciences, London, UK ; Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, London, UK ; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
Zehnder, Tobias ; MRC London Institute of Medical Sciences, London, UK ; Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, London, UK ; Max Planck Institute for Molecular Genetics, Department of Computational Molecular Biology, Berlin, Germany
Mukarram, Abdul Kadir; Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden
Nepal, Chirag; Biotech Research and Innovation Centre (BRIC), Department of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Várnai, Csilla ; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK ; Centre for Computational Biology, University of Birmingham, Birmingham, UK
Hadzhiev, Yavor ; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
Jimenez-Gonzalez, Ada ; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
Li, Nan ; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
Wragg, Joseph; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
D'Orazio, Fabio M; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
Relic, Dorde ; Biozentrum, University of Basel and Swiss Institute of Bioinformatics, Basel, Switzerland
Pachkov, Mikhail ; Biozentrum, University of Basel and Swiss Institute of Bioinformatics, Basel, Switzerland
Díaz, Noelia ; Max Planck Institute for Molecular Biomedicine, Muenster, Germany ; Institute of Marine Sciences, Barcelona, Spain
Hernández-Rodríguez, Benjamín ; Max Planck Institute for Molecular Biomedicine, Muenster, Germany
Chen, Zelin ; Translational and Functional Genomics Branch, National Human Genome Research Institute, Bethesda, MD, USA ; Southern Marine Science and Engineering Guangdong Laboratory, Guangzhou, China ; CAS Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China
Stoiber, Marcus; Environmental Genomics & Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Dong, Michaël ; Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden
Stevens, Irene ; Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden
Ross, Samuel E; Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia
Eagle, Anne; Institute of Neuroscience, University of Oregon, Eugene, OR, USA
Martin, Ryan; Institute of Neuroscience, University of Oregon, Eugene, OR, USA
Obasaju, Oluwapelumi ; Institute of Cancer and Genomic Sciences, Birmingham Centre for Genome Biology, College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
Rastegar, Sepand ; Institute of Biological and Chemical Systems - Biological Information Processing (IBCS-BIP), Karlsruhe Institute of Technology, Karlsruhe, Germany
McGarvey, Alison C; Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany
Kopp, Wolfgang ; Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany
Chambers, Emily ; Sheffield Bioinformatics Core, Sheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, UK
Wang, Dennis ; Sheffield Bioinformatics Core, Sheffield Institute of Translational Neuroscience, University of Sheffield, Sheffield, UK ; Singapore Institute for Clinical Sciences, Singapore, Singapore
Kim, Hyejeong R; Bateson Centre/Biomedical Science, University of Sheffield, Sheffield, UK
Acemel, Rafael D ; Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain ; Epigenetics and Sex Development Group, Berlin Institute for Medical Systems Biology, Max-Delbrück Center for Molecular Medicine, Berlin, Germany
Naranjo, Silvia ; Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain
Łapiński, Maciej ; International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
Chong, Vanessa ; MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK
Mathavan, Sinnakaruppan; Vision Research Foundation, Sankara Nethralayas, Chennai, India
Peers, Bernard ; Université de Liège - ULiège > Département des sciences de la vie
Sauka-Spengler, Tatjana ; MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK
Vingron, Martin ; Max Planck Institute for Molecular Genetics, Department of Computational Molecular Biology, Berlin, Germany
Carninci, Piero ; Laboratory for Transcriptome Technology, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan ; Fondazione Human Technopole, Milano, Italy
Ohler, Uwe ; Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany ; Institute of Biology, Humboldt University, Berlin, Germany
Lacadie, Scott Allen; Max-Delbrück-Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany
Burgess, Shawn M ; Southern Marine Science and Engineering Guangdong Laboratory, Guangzhou, China
Winata, Cecilia ; International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
van Eeden, Freek ; Bateson Centre/Biomedical Science, University of Sheffield, Sheffield, UK
Vaquerizas, Juan M ; MRC London Institute of Medical Sciences, London, UK ; Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, London, UK ; Max Planck Institute for Molecular Biomedicine, Muenster, Germany
Gómez-Skarmeta, José Luis ; Centro Andaluz de Biología del Desarrollo (CABD), CSIC-Universidad Pablo de Olavide-Junta de Andalucía, Seville, Spain
Onichtchouk, Daria ; Department of Developmental Biology, Signalling Research Centers BIOSS and CIBSS, University of Freiburg, Freiburg, Germany
Brown, Ben James ; Environmental Genomics & Systems Biology, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Bogdanovic, Ozren ; Genomics and Epigenetics Division, Garvan Institute of Medical Research, Sydney, New South Wales, Australia ; School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, New South Wales, Australia
van Nimwegen, Erik ; Biozentrum, University of Basel and Swiss Institute of Bioinformatics, Basel, Switzerland
Westerfield, Monte ; Institute of Neuroscience, University of Oregon, Eugene, OR, USA
Wardle, Fiona C ; Randall Centre for Cell & Molecular Biophysics, Guy's Campus, King's College London, London, UK
Daub, Carsten O ; Department of Biosciences and Nutrition, Karolinska Institutet, NEO, Huddinge, Sweden. carsten.daub@ki.se ; Science for Life Laboratory, Solna, Sweden. carsten.daub@ki.se
Lenhard, Boris ; MRC London Institute of Medical Sciences, London, UK. b.lenhard@imperial.ac.uk ; Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, Hammersmith Hospital Campus, London, UK. b.lenhard@imperial.ac.uk
Müller, Ferenc ; Institute 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
BBSRC - Biotechnology and Biological Sciences Research Council [GB] EC - European Commission [BE] Wellcome Trust [GB] Rutherford Fund
Funding text :
We are indebted to the late Jose Luis Gomez Skarmeta for his devoted support of the DANIO-CODE programme. We thank M. Haussler at UCSC and D. Zerbino at EBI for facilitating access of DANIO-CODE track hubs in the UCSC and Ensembl genome browsers, respectively. We thank ZFIN for hosting the DANIO-CODE DCC and raw data. We thank J. Horsefield for creating the DANIO-CODE logo. We thank data producers (for the list of laboratories visit the DANIO-CODE DCC) who directly uploaded data and provided metadata directly. We thank DNANexus for providing computer time for the reprocessing of public datasets. We thank our main funders, the Horizon 2020 MSCA-ITN project ZENCODE-ITN by the European Commission to F.M., B.L., C.O.D., J.M.V. and B.P. (GA no: 643062), BBSRC support (DanioPeaks, P61715) to B.L., F.M. and F.C.W., Wellcome Trust (Joint-Investigator award 106955/Z/15/Z) to F.M. and B.L. and AQUA-FAANG (Horizon 2020, GA 817923) to B.L., D.B. and F.M. and BBSRC (BB/R015457/1) to F.vE and Key Special Project for Introduced Talents Team to Z.C. (GML2019ZD0401) and PrecisionTox project by the European Commission (GA no: 965406). We thank SNP&SEQ Technology Platform in Uppsala, Sweden (CAGE sequencing), MRC LMS Genomics Facility and Genomics Birmingham facilities UK. D.B. was awarded the Rutherford Fund Fellowship.We are indebted to the late Jose Luis Gomez Skarmeta for his devoted support of the DANIO-CODE programme. We thank M. Haussler at UCSC and D. Zerbino at EBI for facilitating access of DANIO-CODE track hubs in the UCSC and Ensembl genome browsers, respectively. We thank ZFIN for hosting the DANIO-CODE DCC and raw data. We thank J. Horsefield for creating the DANIO-CODE logo. We thank data producers (for the list of laboratories visit the DANIO-CODE DCC) who directly uploaded data and provided metadata directly. We thank DNANexus for providing computer time for the reprocessing of public datasets. We thank our main funders, the Horizon 2020 MSCA-ITN project ZENCODE-ITN by the European Commission to F.M., B.L., C.O.D., J.M.V. and B.P. (GA no: 643062), BBSRC support (DanioPeaks, P61715) to B.L., F.M. and F.C.W., Wellcome Trust (Joint-Investigator award 106955/Z/15/Z) to F.M. and B.L. and AQUA-FAANG (Horizon 2020, GA 817923) to B.L., D.B. and F.M. and BBSRC (BB/R015457/1) to F.vE and Key Special Project for Introduced Talents Team to Z.C. (GML2019ZD0401) and PrecisionTox project by the European Commission (GA no: 965406 ) . We thank SNP&SEQ Technology Platform in Uppsala, Sweden (CAGE sequencing), MRC LMS Genomics Facility and Genomics Birmingham facilities UK. D.B. was awarded the Rutherford Fund Fellowship.
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