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Temporal control of gene expression by the pioneer factor Zelda through transient interactions in hubs

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  • Jeremy Dufourt

    (University of Montpellier, CNRS-UMR 5535)

  • Antonio Trullo

    (University of Montpellier, CNRS-UMR 5535)

  • Jennifer Hunter

    (University of Montpellier, CNRS-UMR 5535)

  • Carola Fernandez

    (University of Montpellier, CNRS-UMR 5535)

  • Jorge Lazaro

    (University of Montpellier, CNRS-UMR 5535)

  • Matthieu Dejean

    (University of Montpellier, CNRS-UMR 5535)

  • Lucas Morales

    (University of Montpellier, CNRS-UMR 5535)

  • Saida Nait-Amer

    (University of Montpellier, CNRS-UMR 5535)

  • Katharine N. Schulz

    (University of Wisconsin School of Medicine and Public Health Madison)

  • Melissa M. Harrison

    (University of Wisconsin School of Medicine and Public Health Madison)

  • Cyril Favard

    (CNRS, University of Montpellier UMR 9004)

  • Ovidiu Radulescu

    (DIMNP, UMR CNRS 5235, University of Montpellier, Place E. Bataillon – Bât. 24 cc 107)

  • Mounia Lagha

    (University of Montpellier, CNRS-UMR 5535)

Abstract

Pioneer transcription factors can engage nucleosomal DNA, which leads to local chromatin remodeling and to the establishment of transcriptional competence. However, the impact of enhancer priming by pioneer factors on the temporal control of gene expression and on mitotic memory remains unclear. Here we employ quantitative live imaging methods and mathematical modeling to test the effect of the pioneer factor Zelda on transcriptional dynamics and memory in Drosophila embryos. We demonstrate that increasing the number of Zelda binding sites accelerates the kinetics of nuclei transcriptional activation regardless of their transcriptional past. Despite its known pioneering activities, we show that Zelda does not remain detectably associated with mitotic chromosomes and is neither necessary nor sufficient to foster memory. We further reveal that Zelda forms sub-nuclear dynamic hubs where Zelda binding events are transient. We propose that Zelda facilitates transcriptional activation by accumulating in microenvironments where it could accelerate the duration of multiple pre-initiation steps.

Suggested Citation

  • Jeremy Dufourt & Antonio Trullo & Jennifer Hunter & Carola Fernandez & Jorge Lazaro & Matthieu Dejean & Lucas Morales & Saida Nait-Amer & Katharine N. Schulz & Melissa M. Harrison & Cyril Favard & Ovi, 2018. "Temporal control of gene expression by the pioneer factor Zelda through transient interactions in hubs," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-07613-z
    DOI: 10.1038/s41467-018-07613-z
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    Cited by:

    1. Chun-Yi Cho & Patrick H. O’Farrell, 2023. "Stepwise modifications of transcriptional hubs link pioneer factor activity to a burst of transcription," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Jonathan Liu & Donald Hansen & Elizabeth Eck & Yang Joon Kim & Meghan Turner & Simon Alamos & Hernan Garcia, 2021. "Real-time single-cell characterization of the eukaryotic transcription cycle reveals correlations between RNA initiation, elongation, and cleavage," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-26, May.
    3. Niklas Korsbo & Henrik Jönsson, 2020. "It’s about time: Analysing simplifying assumptions for modelling multi-step pathways in systems biology," PLOS Computational Biology, Public Library of Science, vol. 16(6), pages 1-29, June.
    4. Jiegen Wu & Baoqiang Chen & Yadi Liu & Liang Ma & Wen Huang & Yihan Lin, 2022. "Modulating gene regulation function by chemically controlled transcription factor clustering," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. 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.
    6. Maëlle Bellec & Jérémy Dufourt & George Hunt & Hélène Lenden-Hasse & Antonio Trullo & Amal Zine El Aabidine & Marie Lamarque & Marissa M. Gaskill & Heloïse Faure-Gautron & Mattias Mannervik & Melissa , 2022. "The control of transcriptional memory by stable mitotic bookmarking," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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