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Specialized microenvironments called niches regulate tissue homeostasis by controlling the balance between stem cell self-renewal and the differentiation of stem cell daughters. However the mechanisms that govern the formation, size and signaling of  in vivo  niches remain poorly understood. Loss of the highly conserved histone demethylase  Lsd1  in  Drosophila  escort cells results in increased BMP signaling outside the cap cell niche and an expanded germline stem cell (GSC) phenotype. Here we present evidence that loss of  Lsd1  also results in gradual changes in escort cell morphology and their eventual death. To better characterize the function of Lsd1 in different cell populations within the ovary, we performed Chromatin immunoprecipitation coupled with massive parallel sequencing (ChIP-seq). This analysis shows that Lsd1 associates with a surprisingly limited number of sites in escort cells and fewer, and often, different sites in cap cells. These findings indicate that Lsd1 exhibits highly selective binding that depends greatly on specific cellular contexts. Lsd1 does not directly target the  dpp  locus in escort cells. Instead, Lsd1 regulates  engrailed  expression and disruption of  engrailed  and its putative downstream target  hedgehog  suppress the  Lsd1  mutant phenotype. Interestingly, over-expression of  engrailed , but not  hedgehog , results in an expansion of GSC cells, marked by the expansion of BMP signaling. Knockdown of other potential direct Lsd1 target genes, not obviously linked to BMP signaling, also partially suppresses the  Lsd1  mutant phenotype. These results suggest that Lsd1 restricts the number of GSC-like cells by regulating a diverse group of genes and provide further evidence that escort cell function must be carefully controlled during development and adulthood to ensure proper germline differentiation.

Lsd1 Restricts the Number of Germline Stem Cells by Regulating Multiple Targets in Escort Cells