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Single-cell absolute contact probability detection reveals that chromosomes are organized by modulated stochasticity

Diego I. Cattoni, Andrés M. Cardozo Gizzi, Mariya Georgieva, Marco Di Stefano, Alessandro Valeri, Delphine Chamousset, Christophe Houbron, Stephanie Déjardin, Jean-Bernard Fiche, Marc A. Marti-Renom, Frédéric Bantignies, Giacomo Cavalli, Marcelo Nollmann
doi: https://doi.org/10.1101/159814
Diego I. Cattoni
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Andrés M. Cardozo Gizzi
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Mariya Georgieva
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Marco Di Stefano
2CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain; Gene Regulation, Stem Cells and Cancer Program, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Barcelona, Spain; ICREA, Pg. Lluís Companys 23, 08010 Barcelona, Spain.
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Alessandro Valeri
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Delphine Chamousset
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Christophe Houbron
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Stephanie Déjardin
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
3Institut de Génétique Humaine, CNRS UMR 9002, Université de Montpellier, 141 rue de la Cardonille, 34396 Montpellier, France
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Jean-Bernard Fiche
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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Marc A. Marti-Renom
3Institut de Génétique Humaine, CNRS UMR 9002, Université de Montpellier, 141 rue de la Cardonille, 34396 Montpellier, France
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Frédéric Bantignies
3Institut de Génétique Humaine, CNRS UMR 9002, Université de Montpellier, 141 rue de la Cardonille, 34396 Montpellier, France
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Giacomo Cavalli
3Institut de Génétique Humaine, CNRS UMR 9002, Université de Montpellier, 141 rue de la Cardonille, 34396 Montpellier, France
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Marcelo Nollmann
1Centre de Biochimie Structurale, CNRS UMR5048, INSERM U1054, Université de Montpellier, 29 rue de Navacelles, 34090 Montpellier, France
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  • For correspondence: marcelo.nollmann@cbs.cnrs.fr
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Abstract

The multi-scale organization of eukaryotic genomes defines and regulates cellular identity and tissue-specific functions1–3. At the kilo-megabase scales, genomes are partitioned into self-interacting modules or topologically associated domains (TADs) 4–6. TADs formation seems to require specific looping interactions between TAD borders 7,8, while association of TADs can lead to the formation of active/repressed compartments 9. These structural levels are often seen as highly stable over time, however, recent studies have reported different degrees of heterogeneity 10,11. Access to single-cell absolute probability contact measurements between loci and efficient detection of low-frequency, long-range interactions is thus essential to unveil the stochastic behaviour of chromatin at different scales. Here, we combined super-resolution microscopy with state-of-the-art DNA labeling methods to reveal the variability in the multiscale organization of chromosomes in different cell-types and developmental stages in Drosophila. Remarkably, we found that stochasticity is present at all levels of chromosome architecture, but is locally modulated by sequence and epigenetic state. Contacts between consecutive TAD borders were infrequent, independently of TAD size, epigenetic state, or cell type. Moreover, long-range contact probabilities between non-consecutive borders, the overall folding of chromosomes, and the clustering of epigenetic domains into active/repressed compartments displayed different degrees of stochasticity that globally depended on cell-type. Overall, our results show that stochasticity can be specifically modulated to give rise to different levels of genome organization. We anticipate that our results will guide new statistical models of genome architecture and will be a starting point for more sophisticated studies to understand how a highly variable, multi-scale organization can ensure the maintenance of stable transcriptional programs through cell division and during development.

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Single-cell absolute contact probability detection reveals that chromosomes are organized by modulated stochasticity
Diego I. Cattoni, Andrés M. Cardozo Gizzi, Mariya Georgieva, Marco Di Stefano, Alessandro Valeri, Delphine Chamousset, Christophe Houbron, Stephanie Déjardin, Jean-Bernard Fiche, Marc A. Marti-Renom, Frédéric Bantignies, Giacomo Cavalli, Marcelo Nollmann
bioRxiv 159814; doi: https://doi.org/10.1101/159814
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Single-cell absolute contact probability detection reveals that chromosomes are organized by modulated stochasticity
Diego I. Cattoni, Andrés M. Cardozo Gizzi, Mariya Georgieva, Marco Di Stefano, Alessandro Valeri, Delphine Chamousset, Christophe Houbron, Stephanie Déjardin, Jean-Bernard Fiche, Marc A. Marti-Renom, Frédéric Bantignies, Giacomo Cavalli, Marcelo Nollmann
bioRxiv 159814; doi: https://doi.org/10.1101/159814

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