Abstract
ABSTRACTA limited BMP signaling range in the stem cell niche of the ovary protects against germ cell tumors and promotes germ cell homeostasis. The canonical repressor of BMP signaling in both the Drosophila embryo and wing disc is the transcription factor Brinker (Brk), yet the expression and potential role of Brk in the germarium has not previously been described. Here, we find that brk expression requires a promoter-proximal element (PPE) to support long-distance enhancer action as well as to drive expression in the germarium. Furthermore, PPE subdomains have different activities; in particular, the proximal portion acts as a damper to regulate brk levels precisely. Using PPE mutants as well as tissue-specific RNA interference and overexpression, we show that altering brk expression within either the soma or the germline affects germ cell homeostasis. Remarkably, we find that Decapentaplegic (Dpp), the main BMP ligand and canonical antagonist of Brk, is upregulated by Brk in the escort cells of the germarium, demonstrating that Brk can positively regulate this pathway.
Highlights
Maintenance of germline stem cell (GSC) homeostasis is regulated by numerous pathways that signal between the germline and somatic cells that comprise the stem cell niche, as well as by other external and long-range signals (Nelson et al, 2019; Zhang and Cai, 2020)
GSCs produce cystoblasts via asymmetric division aligned along the anteriorposterior axis of the germarium such that daughter cells that move out of the niche escape the self-renewal signal and begin to differentiate, whereas those that remain in contact with the cap cells (CCs) are maintained as GSCs
The brk promoter-proximal element (PPE) regulates expression in multiple ovarian tissues and is required for distal enhancer action To examine the role of the PPE in supporting ovary brk expression, we first used a set of large reporters in which the brk coding sequence is replaced with gfp in the context of ∼30 kb of flanking sequence
Summary
Maintenance of germline stem cell (GSC) homeostasis is regulated by numerous pathways that signal between the germline and somatic cells that comprise the stem cell niche, as well as by other external and long-range signals (Nelson et al, 2019; Zhang and Cai, 2020). This increase in pMad+ cell number occurred in all PPE mutants (i.e. ΔPPE2kb, ΔPPEdist and ΔPPEprox), despite the fact that these deletions had varying effects on brk reporter expression levels (Fig. 2G,H).
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