A transitory signaling center controls timing of primordial germ cell differentiation

Dev Cell. 2021 Jun 21;56(12):1742-1755.e4. doi: 10.1016/j.devcel.2021.05.008. Epub 2021 Jun 2.

Abstract

Organogenesis requires exquisite spatiotemporal coordination of cell morphogenesis, migration, proliferation, and differentiation of multiple cell types. For gonads, this involves complex interactions between somatic and germline tissues. During Drosophila ovary morphogenesis, primordial germ cells (PGCs) either are sequestered in stem cell niches and are maintained in an undifferentiated germline stem cell state or transition directly toward differentiation. Here, we identify a mechanism that links hormonal triggers of somatic tissue morphogenesis with PGC differentiation. An early ecdysone pulse initiates somatic swarm cell (SwC) migration, positioning these cells close to PGCs. A second hormone peak activates Torso-like signal in SwCs, which stimulates the Torso receptor tyrosine kinase (RTK) signaling pathway in PGCs promoting their differentiation by de-repression of the differentiation gene, bag of marbles. Thus, systemic temporal cues generate a transitory signaling center that coordinates ovarian morphogenesis with stem cell self-renewal and differentiation programs, highlighting a more general role for such centers in reproductive and developmental biology.

Keywords: Drosophila; Torso; ecdysone; germline; gonad morphogensis; primordial germ cells; stem cells; steroid hormone; swarm cell; transitory signaling center.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation / genetics*
  • Cell Movement / genetics
  • Cell Proliferation / genetics
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Ecdysone / genetics
  • Female
  • Gene Expression Regulation, Developmental / genetics
  • Germ Cells / growth & development*
  • Larva / genetics
  • Larva / growth & development
  • Morphogenesis / genetics*
  • Ovary / growth & development*
  • Ovary / metabolism
  • Receptor Protein-Tyrosine Kinases / genetics*

Substances

  • Drosophila Proteins
  • bam protein, Drosophila
  • Ecdysone
  • Receptor Protein-Tyrosine Kinases
  • tor protein, Drosophila