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Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development

Sergio Martin Espinola, Markus Götz, Jean-Bernard Fiche, Maelle Bellec, Christophe Houbron, Andrés M. Cardozo Gizzi, Mounia Lagha, View ORCID ProfileMarcelo Nollmann
doi: https://doi.org/10.1101/2020.07.07.191015
Sergio Martin Espinola
1Centre de Biochimie Structurale, CNRS UMR 5048, INSERM U1054, Université de Montpellier, 60 rue de Navacelles, 34090, Montpellier, France
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Markus Götz
1Centre de Biochimie Structurale, CNRS UMR 5048, INSERM U1054, Université de Montpellier, 60 rue de Navacelles, 34090, Montpellier, France
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Jean-Bernard Fiche
1Centre de Biochimie Structurale, CNRS UMR 5048, INSERM U1054, Université de Montpellier, 60 rue de Navacelles, 34090, Montpellier, France
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Maelle Bellec
2Institut de Génétique Moléculaire de Montpellier, CNRS UMR, Université de Montpellier, 119 route de Mende, 34090, Montpellier, France
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Christophe Houbron
1Centre de Biochimie Structurale, CNRS UMR 5048, INSERM U1054, Université de Montpellier, 60 rue de Navacelles, 34090, Montpellier, France
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Andrés M. Cardozo Gizzi
3CIQUIBIC (CONICET), Departamento de Química Biológica Ranwel Caputto, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Haya de la Torre y Medina Allende, Ciudad Universitaria, 5000, Córdoba, Argentina
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Mounia Lagha
2Institut de Génétique Moléculaire de Montpellier, CNRS UMR, Université de Montpellier, 119 route de Mende, 34090, Montpellier, France
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  • For correspondence: marcelo.nollmann@cbs.cnrs.fr mounia.lagha@igmm.cnrs.fr
Marcelo Nollmann
1Centre de Biochimie Structurale, CNRS UMR 5048, INSERM U1054, Université de Montpellier, 60 rue de Navacelles, 34090, Montpellier, France
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  • ORCID record for Marcelo Nollmann
  • For correspondence: marcelo.nollmann@cbs.cnrs.fr mounia.lagha@igmm.cnrs.fr
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Abstract

During development, naïve cells gradually acquire distinct cell fates, through sophisticated mechanisms of precise spatio-temporal gene regulation. Acquisition of cell fate is thought to rely on the specific interaction of remote cis-regulatory modules (e.g. enhancers, silencers) (CRM) and target promoters. However, the precise interplay between chromatin structure and gene expression is still unclear, particularly in single cells within multicellular developing organisms. Here we employ Hi-M, a single-cell spatial genomics approach, to systematically detect CRM-promoter looping interactions within topological associating domains (TADs) during Drosophila development. By comparing cis-regulatory loops in alternate cell types, we show that physical proximity does not necessarily instruct transcriptional states. Moreover, multi-way analyses revealed the existence of local interactions between multiple remote CRMs to form hubs. We found that loops and CRM hubs are established early during development, prior to the emergence of TADs. Moreover, CRM hubs are formed via the action of the pioneer transcription factor Zelda and precede transcriptional activation. Our approach offers a new perspective on the role of CRM-promoter interactions in defining transcriptional activation and repression states, as well as distinct cell types.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted July 07, 2020.
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Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development
Sergio Martin Espinola, Markus Götz, Jean-Bernard Fiche, Maelle Bellec, Christophe Houbron, Andrés M. Cardozo Gizzi, Mounia Lagha, Marcelo Nollmann
bioRxiv 2020.07.07.191015; doi: https://doi.org/10.1101/2020.07.07.191015
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Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development
Sergio Martin Espinola, Markus Götz, Jean-Bernard Fiche, Maelle Bellec, Christophe Houbron, Andrés M. Cardozo Gizzi, Mounia Lagha, Marcelo Nollmann
bioRxiv 2020.07.07.191015; doi: https://doi.org/10.1101/2020.07.07.191015

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