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In both animal cells and fungi, cytokinesis proceeds via a contractile actomyosin ring (CAR). Many CAR components and regulators are evolutionarily conserved. In Schizosaccharomyces pombe, the spatial cue for cytokinesis is provided by Mid1p/Anillin, whereas temporal coordination is ensured by the septation initiation network (SIN). However, neither Mid1p nor the SIN is considered to be essential for CAR assembly per se. Here, using 4D imaging, we reveal an unanticipated, novel role for the SIN in CAR assembly. We demonstrate that CAR assembly involves three, genetically separable steps: establishment of a cortical network of CAR proteins, its lateral condensation, and finally, the formation of a homogeneous CAR. We show that SIN mutants fail to form a homogeneous CAR; we identify hypophosphorylation and recruitment of the conserved PCH-family protein Cdc15p to the CAR as critical steps requiring …