Differentiating Drosophila female germ cells initiate Polycomb silencing by regulating PRC2-interacting proteins

  1. Steven Z Deluca
  2. Megha Ghildiyal
  3. Liang-Yu Pang
  4. Allan C Spradling  Is a corresponding author
  1. Carnegie Institution for Science, United States

Abstract

Polycomb silencing represses gene expression and provides a molecular memory of chromatin state that is essential for animal development. We show that Drosophila female germline stem cells (GSCs) provide a powerful system for studying Polycomb silencing. GSCs have a non-canonical distribution of PRC2 activity and lack silenced chromatin, like embryonic progenitors. As GSC daughters differentiate into nurse cells and oocytes, nurse cells silence genes in traditional Polycomb domains and in generally inactive chromatin like embryonic somatic cells. Developmentally controlled expression of two Polycomb repressive complex 2 (PRC2)-interacting proteins, Pcl and Scm, initiate silencing during differentiation. In GSCs, abundant Pcl inhibits PRC2-dependent silencing globally, while in nurse cells Pcl declines and newly-induced Scm concentrates PRC2 activity on traditional Polycomb domains. Our results suggest that PRC2-dependent silencing is developmentally regulated by accessory proteins that either increase the concentration of PRC2 at target sites or inhibit the rate that PRC2 samples chromatin.

Data availability

High throughput sequencing data can be found under accession GSE145282 and code is available at github.com/ciwemb/polycomb-development. Source data of image quantification is included as supporting files.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Steven Z Deluca

    Embryology, Carnegie Institution for Science, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0683-8413
  2. Megha Ghildiyal

    Embryology, Carnegie Institution for Science, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Liang-Yu Pang

    Department of Embryology, Carnegie Institution for Science, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8373-5656
  4. Allan C Spradling

    Department of Embryology, Carnegie Institution for Science, Baltimore, United States
    For correspondence
    spradling@carnegiescience.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5251-1801

Funding

Howard Hughes Medical Institute (ACS received the funding)

  • Allan C Spradling

Helen Hay Whitney Foundation (Postdoc Fellowhip to Steven DeLuca)

  • Steven Z Deluca

Jane Coffin Childs Memorial Fund for Medical Research (Postdoc Fellowship to Megha Ghildiyal)

  • Megha Ghildiyal

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mia T Levine, University of Pennsylvania, United States

Publication history

  1. Received: March 13, 2020
  2. Accepted: August 6, 2020
  3. Accepted Manuscript published: August 10, 2020 (version 1)
  4. Version of Record published: August 19, 2020 (version 2)

Copyright

© 2020, Deluca et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Steven Z Deluca
  2. Megha Ghildiyal
  3. Liang-Yu Pang
  4. Allan C Spradling
(2020)
Differentiating Drosophila female germ cells initiate Polycomb silencing by regulating PRC2-interacting proteins
eLife 9:e56922.
https://doi.org/10.7554/eLife.56922
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