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Cell-type-specific chromatin occupancy by the pioneer factor Zelda drives key developmental transitions in Drosophila

Author

Listed:
  • Elizabeth D. Larson

    (University of Wisconsin School of Medicine and Public Health)

  • Hideyuki Komori

    (University of Michigan)

  • Tyler J. Gibson

    (University of Wisconsin School of Medicine and Public Health)

  • Cyrina M. Ostgaard

    (University of Michigan Medical School)

  • Danielle C. Hamm

    (University of Wisconsin School of Medicine and Public Health
    Human Biology Division, Fred Hutchinson Cancer Research Center)

  • Jack M. Schnell

    (University of Wisconsin School of Medicine and Public Health
    Keck School of Medicine of the University of Southern California)

  • Cheng-Yu Lee

    (University of Michigan Medical School)

  • Melissa M. Harrison

    (University of Wisconsin School of Medicine and Public Health)

Abstract

During Drosophila embryogenesis, the essential pioneer factor Zelda defines hundreds of cis-regulatory regions and in doing so reprograms the zygotic transcriptome. While Zelda is essential later in development, it is unclear how the ability of Zelda to define cis-regulatory regions is shaped by cell-type-specific chromatin architecture. Asymmetric division of neural stem cells (neuroblasts) in the fly brain provide an excellent paradigm for investigating the cell-type-specific functions of this pioneer factor. We show that Zelda synergistically functions with Notch to maintain neuroblasts in an undifferentiated state. Zelda misexpression reprograms progenitor cells to neuroblasts, but this capacity is limited by transcriptional repressors critical for progenitor commitment. Zelda genomic occupancy in neuroblasts is reorganized as compared to the embryo, and this reorganization is correlated with differences in chromatin accessibility and cofactor availability. We propose that Zelda regulates essential transitions in the neuroblasts and embryo through a shared gene-regulatory network driven by cell-type-specific enhancers.

Suggested Citation

  • Elizabeth D. Larson & Hideyuki Komori & Tyler J. Gibson & Cyrina M. Ostgaard & Danielle C. Hamm & Jack M. Schnell & Cheng-Yu Lee & Melissa M. Harrison, 2021. "Cell-type-specific chromatin occupancy by the pioneer factor Zelda drives key developmental transitions in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27506-y
    DOI: 10.1038/s41467-021-27506-y
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    References listed on IDEAS

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    1. Muhammad A. Zabidi & Cosmas D. Arnold & Katharina Schernhuber & Michaela Pagani & Martina Rath & Olga Frank & Alexander Stark, 2015. "Enhancer–core-promoter specificity separates developmental and housekeeping gene regulation," Nature, Nature, vol. 518(7540), pages 556-559, February.
    2. Hsiao-Lan Liang & Chung-Yi Nien & Hsiao-Yun Liu & Mark M. Metzstein & Nikolai Kirov & Christine Rushlow, 2008. "The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila," Nature, Nature, vol. 456(7220), pages 400-403, November.
    3. Cheng-Yu Lee & Kristin J. Robinson & Chris Q. Doe, 2006. "Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation," Nature, Nature, vol. 439(7076), pages 594-598, February.
    4. Alexander M. Tsankov & Hongcang Gu & Veronika Akopian & Michael J. Ziller & Julie Donaghey & Ido Amit & Andreas Gnirke & Alexander Meissner, 2015. "Transcription factor binding dynamics during human ES cell differentiation," Nature, Nature, vol. 518(7539), pages 344-349, February.
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