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

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, Ovidiu Radulescu and Mounia Lagha ()
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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

Nature Communications, 2018, vol. 9, issue 1, 1-13

Abstract: 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.

Date: 2018
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DOI: 10.1038/s41467-018-07613-z

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