Evolutionarily conserved midbody remodeling precedes ring canal formation during gametogenesis

How canonical cytokinesis is altered during germ cell division to produce stable intercellular bridges, called “ring canals,” is poorly understood. Here, using time-lapse imaging in Drosophila, we observe that ring canal formation occurs through extensive remodeling of the germ cell midbody, a structure classically associated with its function in recruiting abscission-regulating proteins in complete cytokinesis. Germ cell midbody cores reorganize and join the midbody ring rather than being discarded, and this transition is accompanied by changes in centralspindlin dynamics. The midbody-to-ring canal transformation is conserved in the Drosophila male and female germlines and during mouse and Hydra spermatogenesis. In Drosophila, ring canal formation depends on Citron kinase function to stabilize the midbody, similar to its role during somatic cell cytokinesis. Our results provide important insights into the broader functions of incomplete cytokinesis events across biological systems, such as those observed during development and disease states. [Display omitted] •Midbody core remodeling precedes formation of transient and stable germline ring canals•Ring canals originate from stabilized midbody rings•Aberrant midbody remodeling impacts ring canal formation and protein movement•Abscission inhibition stabilizes germ cell ring canals after they form Ring canals connect germ cells in syncytial groups and are necessary for gamete development. Price et al. show that ring canals form through the remodeling of germ cell midbodies in Drosophila, Hydra, and mouse. Perturbation of midbody formation and subsequent reorganization into ring canals affect communication between germ cells.