Niche cell positioning drives functional heterogeneity in the Drosophila testis stem cell niche

Adult stem cells are critical for tissue homeostasis. They reside in dynamic, supportive microenvironments termed niches, which are generated by specialized niche cells. The adult Drosophila melanogaster testis contains a single niche generated by a small cluster of quiescent somatic niche cells called hub cells. Although much is known about the hub-produced signals that maintain the two stem cell populations of the testis, the composition of the hub itself is less well-characterized, particularly whether the hub is composed of a homogeneous or heterogeneous population of cells. Here, we investigate the position, origin, and function of hub cells in different lab strains of D. melanogaster. We find that hub architecture varies significantly within and between different genetic backgrounds and with age; that most but not all hub cells play a role in anchoring the niche to the testis apex through integrin-based adhesion; and that the positions occupied by hub cells within the niche relative to the testis wall (TW) and surrounding cells are not pre-determined by their origin. Furthermore, hub cell position, but not origin, is associated with Upd1 expression and ability to exit quiescence in response to tissue damage; stem cell-contacting hub cells produce more Upd1, while cycling hub cells are more likely to contact the TW. Recovery phenotypes following genetic ablation of the CySC lineage are not mediated by c-Jun N-terminal kinase (JNK) signaling nor integrin. This work is the first demonstration of functional heterogeneity among these niche cells and highlights the complexity of this simple niche.