Interdependence of Ring Constriction and Septation in Fission Yeast Cytokinesis

Abstract

Cytokinesis concludes the cell cycle and entails physical division of the cytoplasm into two parts. In animals and fungi, cytokinesis involves constriction of an actomyosin contractile ring coupled to other simultaneous processes but how these processes coordinate with the ring is not established. In fission yeast, constriction is tightly coupled to septation, the growth of new cell wall in the wake of the constricting ring. It is unknown whether ring closure is driven by septation or the ring itself. Here we developed a model of cytokinesis in fission yeast that describes the coupling of the tensile contractile ring to the growth of primary septum by Bgs1p and other proteins that synthesize septum material. The model hypothesizes that ring tension influences the local rate of septum growth through the effect of radial ring-generated forces on Bgs1p or other motors. We used our model to calculate the rate of inward growth of the septum and the evolution of the shape of the inner septum boundary during ring closure. Our model results are consistent with experimental observations in wild type and mutant yeast cells and suggest that while the ring-septum closure rate is independently set by the septation process, the ring tension serves a vital role by regulating septum growth and thereby suppressing roughness of the septum boundary and maintaining its circular shape. From the model we calculated the minimum ring tension required for a given degree of smoothness in the growing septum, consistent with model computations of wild type fission yeast ring tension. Thus, our model suggests that the primary role of the contractile ring in fission yeast cytokinesis is as a tension-producing machine that regulates septum circularity to ensure ordered closure and separation of the daughter cells.