Antagonism between Germ cell-less and Torso regulates transcriptional quiescence underlying germline/soma distinction

Abstract

Transcriptional quiescence, an evolutionarily conserved trait, distinguishes the embryonic primordial germ cells
(PGCs) from their somatic neighbors. In Drosophila melanogaster, PGCs from embryos maternally compromised for germ cell-less (gcl) misexpress somatic genes, possibly resulting in PGC loss. Recent studies documented a requirement for Gcl during proteolytic degradation of the terminal patterning determinant, Torso receptor. Here we demonstrate that the somatic determinant of female fate, Sex-lethal (Sxl), is a biologically relevant transcriptional target of Gcl. Underscoring the significance of transcriptional silencing mediated by Gcl, ectopic expression of a degradation-resistant form of Torso (torsoDeg) can activate Sxl transcription in PGCs, whereas simultaneous loss of torso-like (tsl) reinstates the quiescent status of gcl PGCs. Intriguingly, like gcl mutants, embryos derived from mothers expressing torsoDeg in the germline display aberrant spreading of pole plasm RNAs, suggesting that mutual antagonism between Gcl and Torso ensures the controlled release of germ-plasm underlying the germline/soma distinction.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3,5,6, and 8.

Article and author information

Author details

  1. Megan M Colonnetta

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5685-1670
  2. Lauren R Lym

    Department of Cell Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5039-2303
  3. Lillian Wilkins

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Gretchen Kappes

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Elias A Castro

    Department of Cell Biology, Emory University, Lilburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1439-5918
  6. Pearl Ryder

    Department of Cell Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Paul Schedl

    Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Dorothy A Lerit

    Department of Cell Biology, Emory University, Atlanta, United States
    For correspondence
    dlerit@emory.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3362-8078
  9. Girish Deshpande

    Department of Molecular Biology, Princeton University, Princeton, United States
    For correspondence
    gdeshpan@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5200-7090

Funding

National Institute of General Medical Sciences (126975)

  • Paul Schedl

Eunice Kennedy Shriver National Institute of Child Health and Human Development (093913)

  • Paul Schedl
  • Girish Deshpande

National Heart, Lung, and Blood Institute (K22HL126922)

  • Dorothy A Lerit

National Institute of General Medical Sciences (138544)

  • Dorothy A Lerit

National Science Foundation (DGE-1656466)

  • Megan M Colonnetta

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

Copyright

© 2021, Colonnetta 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. Megan M Colonnetta
  2. Lauren R Lym
  3. Lillian Wilkins
  4. Gretchen Kappes
  5. Elias A Castro
  6. Pearl Ryder
  7. Paul Schedl
  8. Dorothy A Lerit
  9. Girish Deshpande
(2021)
Antagonism between Germ cell-less and Torso regulates transcriptional quiescence underlying germline/soma distinction
eLife 10:e54346.
https://doi.org/10.7554/eLife.54346

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https://doi.org/10.7554/eLife.54346