Somatic cells non-autonomously control germline incomplete cytokinesis through FGF signaling

Abstract

Across species, germ cells divide and differentiate as interconnected units, termed cysts. These cysts are generated through reiterative rounds of mitosis followed by incomplete cytokinesis to generate stable ring canals (RCs). Despite the ubiquity of germ cell incomplete cytokinesis, it is still unclear how this program is mechanistically regulated across multiple cell cycles to retain integrity of the cyst. Here, by leveraging longitudinal live imaging of the Drosophila testis we have identified a critical, non-autonomous role for somatic support cells in maintenance of germline RC stability. We find that F-actin at RCs is stable throughout interphase but is dynamically disassembled and reassembled at each reiterative mitotic entrance and exit. Importantly, we find that somatic cells regulate the stability of interphase RC F-actin through the secreted growth factor, FGF. Genetic or pharmacological inhibition of FGF signaling induces disassembly of RC F-actin during interphase. Persistent clearance of F-actin from the RC leads to failure of incomplete cytokinesis and cyst abscission, suggesting that stable F-actin at RCs is required for the robust maintenance of incomplete cytokinesis through multiple rounds of germ cell divisions. Finally, we mechanistically link FGF signaling to germline activity of the non-receptor tyrosine kinase, Src64, which is known to regulate RC F-actin through Arp2/3. Taken together, we find a previously unappreciated role for somatic support cells in controlling an essential aspect of germ cell biology in the mitotically dividing spermatogonial pool. Summary StatementSomatic cells of the gonad secrete FGF ligand, Pyramus, which is required for maintenance of F-actin at germline ring canals and integrity of germline incomplete cytokinesis.