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Single-cell absolute contact probability detection reveals chromosomes are organized by multiple low-frequency yet specific interactions

Author

Listed:
  • Diego I. Cattoni

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Andrés M. Cardozo Gizzi

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Mariya Georgieva

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Marco Stefano

    (Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
    Stem Cells and Cancer Program, Centre for Genomic Regulation (CRG)
    Universitat Pompeu Fabra (UPF)
    ICREA)

  • Alessandro Valeri

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Delphine Chamousset

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Christophe Houbron

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Stephanie Déjardin

    (CNRS UMR5048, INSERM U1054, Université de Montpellier
    CNRS UMR 9002, Université de Montpellier)

  • Jean-Bernard Fiche

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

  • Inma González

    (CNRS UMR 9002, Université de Montpellier
    Department of Stem Cell and Developmental Biology, Institut Pasteur, CNRS UMR3738)

  • Jia-Ming Chang

    (CNRS UMR 9002, Université de Montpellier
    National Chengchi University)

  • Thomas Sexton

    (CNRS UMR 9002, Université de Montpellier
    Institut de génétique et de biologie moléculaire et cellulaire)

  • Marc A. Marti-Renom

    (Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
    Stem Cells and Cancer Program, Centre for Genomic Regulation (CRG)
    Universitat Pompeu Fabra (UPF)
    ICREA)

  • Frédéric Bantignies

    (CNRS UMR 9002, Université de Montpellier)

  • Giacomo Cavalli

    (CNRS UMR 9002, Université de Montpellier)

  • Marcelo Nollmann

    (CNRS UMR5048, INSERM U1054, Université de Montpellier)

Abstract

At the kilo- to megabase pair scales, eukaryotic genomes are partitioned into self-interacting modules or topologically associated domains (TADs) that associate to form nuclear compartments. Here, we combine high-content super-resolution microscopies with state-of-the-art DNA-labeling methods to reveal the variability in the multiscale organization of the Drosophila genome. We find that association frequencies within TADs and between TAD borders are below ~10%, independently of TAD size, epigenetic state, or cell type. Critically, despite this large heterogeneity, we are able to visualize nanometer-sized epigenetic domains at the single-cell level. In addition, absolute contact frequencies within and between TADs are to a large extent defined by genomic distance, higher-order chromosome architecture, and epigenetic identity. We propose that TADs and compartments are organized by multiple, small-frequency, yet specific interactions that are regulated by epigenetics and transcriptional state.

Suggested Citation

  • Diego I. Cattoni & Andrés M. Cardozo Gizzi & Mariya Georgieva & Marco Stefano & Alessandro Valeri & Delphine Chamousset & Christophe Houbron & Stephanie Déjardin & Jean-Bernard Fiche & Inma González &, 2017. "Single-cell absolute contact probability detection reveals chromosomes are organized by multiple low-frequency yet specific interactions," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01962-x
    DOI: 10.1038/s41467-017-01962-x
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    Cited by:

    1. Guang Shi & D. Thirumalai, 2023. "A maximum-entropy model to predict 3D structural ensembles of chromatin from pairwise distances with applications to interphase chromosomes and structural variants," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Markus Götz & Olivier Messina & Sergio Espinola & Jean-Bernard Fiche & Marcelo Nollmann, 2022. "Multiple parameters shape the 3D chromatin structure of single nuclei at the doc locus in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Olivier Messina & Flavien Raynal & Julian Gurgo & Jean-Bernard Fiche & Vera Pancaldi & Marcelo Nollmann, 2023. "3D chromatin interactions involving Drosophila insulators are infrequent but preferential and arise before TADs and transcription," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Mattia Conte & Ehsan Irani & Andrea M. Chiariello & Alex Abraham & Simona Bianco & Andrea Esposito & Mario Nicodemi, 2022. "Loop-extrusion and polymer phase-separation can co-exist at the single-molecule level to shape chromatin folding," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Matthew Antel & Romir Raj & Madona Y. G. Masoud & Ziwei Pan & Sheng Li & Barbara G. Mellone & Mayu Inaba, 2022. "Interchromosomal interaction of homologous Stat92E alleles regulates transcriptional switch during stem-cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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