Antagonism between Germ cell-less and Torso regulates transcriptional quiescence underlying germline/soma distinction
- Princeton University, United States
- Emory University, United States
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
Megan M Colonnetta
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.
Reviewing Editor
- Michael B Eisen, University of California, Berkeley, United States
Version history
- Received: December 11, 2019
- Accepted: January 15, 2021
- Accepted Manuscript published: January 18, 2021 (version 1)
- Version of Record published: January 28, 2021 (version 2)
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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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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