Not so Pristine After All: Non-Autonomous BMP Signaling Shapes Early PGC Identity in Drosophila

Abstract

In Drosophila melanogaster, the progenitors of the adult germline, the primordial germ cells (PGCs), are formed at the posterior pole of the pre-cellular blastoderm embryo. The process of PGC specification and development differs substantially from that of the surrounding soma. The important traits that distinguish the PGCs are precocious cellularization, restricted cell cycle progression, transcriptional quiescence, and special chromatin architecture. Also, unlike the soma, the specification and subsequent elaboration of PGC identity is thought to depend exclusively on cell autonomous factors that are assembled into a specialized cytoplasm, the pole plasm, at the posterior of the oocyte during oogenesis. In addition to orchestrating PGC development, these maternal factors (for e.g. polar granule component and nanos) are thought to insulate newly formed PGCs from the adverse effects of the cell-cell signaling pathways that are deployed to pattern the neighboring soma. However, our data on the BMP signaling pathway challenge this long-held view of PGC specification. Data obtained using both the ‘loss’ and ‘gain’ of function strategies suggests that successful survival as well as proper specification of early germ cells is sensitive to the BMP ligand, decapentaplegic (dpp), and its cognate receptor, thickveins (tkv). We thus find that PGCs are not only capable of responding to BMP signals from the soma, but also that these signals impact the specification and development of the PGCs. We have thus re-examined the problem of PGC specification, focusing on the role of this non-autonomous signaling pathway in PGC development. Taken together, these observations have revealed some unanticipated similarities between germ cell specification in mammals and in flies.