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

• Published in: eLife Vol. 10
• Main Authors: Colonnetta, Megan M, Lym, Lauren R, Wilkins, Lillian, Kappes, Gretchen, Castro, Elias A, Ryder, Pearl V, Schedl, Paul, Lerit, Dorothy A, Deshpande, Girish
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 18.01.2021; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Animals; Cell cycle; cell fate; Controlled release; Developmental Biology; Drosophila; Drosophila melanogaster - embryology; Drosophila melanogaster - genetics; Drosophila melanogaster - metabolism; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Ectopic expression; Embryo, Nonmammalian - embryology; Embryonic development; Embryos; Female; Gene silencing; Genes; Genetic aspects; Genetic research; Genetic transcription; germ cell-less; Germ cells; germline; Germplasm; Insects; Intercellular Signaling Peptides and Proteins - genetics; Intercellular Signaling Peptides and Proteins - metabolism; Kinases; Male; Mutation; Phosphorylation; Proteins; Proteolysis; Receptor Protein-Tyrosine Kinases - genetics; Receptor Protein-Tyrosine Kinases - metabolism; RNA polymerase; RNA-Binding Proteins - genetics; RNA-Binding Proteins - metabolism; Sex Determination Processes; Signal transduction; torso receptor; Transcription, Genetic; transcriptional quiescence; transcriptional quiescence; germ cell-less; germline; torso receptor; cell fate; developmental biology; D. melanogaster; germ cells
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.54346

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 ( torso Deg ) 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 torso Deg 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.