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Global regulatory transitions at core promoters demarcate the mammalian germline cycle

View ORCID ProfileNevena Cvetesic, View ORCID ProfileMalgorzata Borkowska, View ORCID ProfileYuki Hatanaka, View ORCID ProfileHarry G. Leitch, View ORCID ProfileFerenc Müller, View ORCID ProfileChangwei Yu, View ORCID ProfileStéphane D. Vincent, View ORCID ProfileLászló Tora, View ORCID ProfilePetra Hajkova, View ORCID ProfileBoris Lenhard
doi: https://doi.org/10.1101/2020.10.30.361865
Nevena Cvetesic
1Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, UK
2MRC London Institute of Medical Sciences, London W12 0NN, UK
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  • ORCID record for Nevena Cvetesic
  • For correspondence: ncvetesi@ic.ac.uk petra.hajkova@lms.mrc.ac.uk b.lenhard@imperial.ac.uk
Malgorzata Borkowska
1Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, UK
2MRC London Institute of Medical Sciences, London W12 0NN, UK
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  • ORCID record for Malgorzata Borkowska
Yuki Hatanaka
1Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, UK
2MRC London Institute of Medical Sciences, London W12 0NN, UK
3Bioresource Engineering Division, RIKEN BioResource Research Center, 305-0074 Ibaraki, Japan
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Harry G. Leitch
1Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, UK
2MRC London Institute of Medical Sciences, London W12 0NN, UK
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Ferenc Müller
4Institute of Cancer and Genomic Sciences, College of Medical and Dental Sciences, University of Birmingham, Edgbaston B15 2TT, UK
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Changwei Yu
5Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
6Centre National de la Recherche Scientifique (CNRS), UMR7104, Illkirch, France
7Institut National de la Santé et de la Recherche Médicale (INSERM), U1258, Illkirch, France
8Université de Strasbourg, Illkirch, France
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Stéphane D. Vincent
5Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
6Centre National de la Recherche Scientifique (CNRS), UMR7104, Illkirch, France
7Institut National de la Santé et de la Recherche Médicale (INSERM), U1258, Illkirch, France
8Université de Strasbourg, Illkirch, France
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László Tora
5Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
6Centre National de la Recherche Scientifique (CNRS), UMR7104, Illkirch, France
7Institut National de la Santé et de la Recherche Médicale (INSERM), U1258, Illkirch, France
8Université de Strasbourg, Illkirch, France
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Petra Hajkova
1Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, UK
2MRC London Institute of Medical Sciences, London W12 0NN, UK
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  • For correspondence: ncvetesi@ic.ac.uk petra.hajkova@lms.mrc.ac.uk b.lenhard@imperial.ac.uk
Boris Lenhard
1Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, UK
2MRC London Institute of Medical Sciences, London W12 0NN, UK
9Sars International Centre for Marine Molecular Biology, University of Bergen, N-5008 Bergen, Norway
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  • For correspondence: ncvetesi@ic.ac.uk petra.hajkova@lms.mrc.ac.uk b.lenhard@imperial.ac.uk
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Abstract

Core promoters integrate regulatory inputs of genes1–3. Global dynamics of promoter usage can reveal systemic changes in how genomic sequence is interpreted by the cell. We previously discovered that early development in fish is associated with a genome-wide shift in how promoters are read: the switch from the oocyte-specific to the somatic-specific promoter usage observed during Zygotic Genome Activation (ZGA) represents one of the most dramatic instances of transcriptional regulatory rewiring known in the animal life cycle4 However, the key question of how and when the oocyte-specific pattern is established in the germ line has been hitherto impossible to answer, as well as whether this switch is universal across vertebrate development. Here we report the first analysis of promoter dynamics and code switching in the mammalian germ line. Using the Super Low Input Carrier-CAGE5, 6 (SLIC-CAGE) we show that mouse germline development starts with the somatic promoter code with a prominent switch to the maternal code occurring during follicular oogenesis. The sequence features underlying the shift from somatic to maternal code are conserved across vertebrates, despite large differences in promoter nucleotide compositions. Surprisingly, we also find that the promoters of gonadal germ cells diverge from the canonical somatic transcription initiation. This divergence is distinct from the promoter code used later by developing oocytes and reveals genome-wide promoter remodelling driven by alternative nucleosome positioning during early female and male germline development. Collectively, our findings establish promoter-level regulatory transitions as a central, conserved feature of the vertebrate life cycle.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 30, 2020.
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Global regulatory transitions at core promoters demarcate the mammalian germline cycle
Nevena Cvetesic, Malgorzata Borkowska, Yuki Hatanaka, Harry G. Leitch, Ferenc Müller, Changwei Yu, Stéphane D. Vincent, László Tora, Petra Hajkova, Boris Lenhard
bioRxiv 2020.10.30.361865; doi: https://doi.org/10.1101/2020.10.30.361865
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Global regulatory transitions at core promoters demarcate the mammalian germline cycle
Nevena Cvetesic, Malgorzata Borkowska, Yuki Hatanaka, Harry G. Leitch, Ferenc Müller, Changwei Yu, Stéphane D. Vincent, László Tora, Petra Hajkova, Boris Lenhard
bioRxiv 2020.10.30.361865; doi: https://doi.org/10.1101/2020.10.30.361865

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