A transitory signaling center controls timing of primordial germ cell differentiation

Abstract

Organogenesis requires exquisite spatio-temporal 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) are either sequestered in stem cell niches and maintained in an undifferentiated, germline stem cell state, or transition directly towards 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 them close to PGCs. A second hormone peak activates Torso-like signal in SwCs, which stimulates the Torso 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 coordinate ovarian morphogenesis with stem cell self-renewal and differentiation programs, a concept applicable broadly to the integration of stem cells and their niches. HIGHLIGHTSO_LISteroid pulses coordinate gonadogenesis, stem cell self-renewal and differentiation C_LIO_LIAn early steroid pulse initiates migration of Swarm Cells, a transitory support cell type C_LIO_LIA late steroid pulse induces Torso-like expression, a Torso receptor tyrosine kinase (RTK) activator, in Swarm Cells C_LIO_LITorso RTK signaling in primordial germ cells activates the key differentiation gene bam by relieving Kruppel-mediated repression C_LI