The Role of the Contractile Ring during Cytokinesis

Abstract

Cytokinesis in animals and fungi involves constriction of an actomyosin contractile ring, but the constriction mechanisms and the role of the ring are not established. The constriction rate could be determined only by the properties and internal dynamics of the ring itself (a “dynamically autonomous” mechanism) as suggested by recent experiments on C. elegans embryos. Alternatively, the ring constriction rate could be set by coupled processes that occur simultaneously with constriction (a “dynamically coupled” mechanism). In fission yeast constriction occurs simultaneously with septation, the poorly understood process of cell wall growth in the wake of the constricting ring. To isolate the ring constriction mechanism, we combined mathematical modeling with experiments on fission yeast protoplasts which lack cell wall and adopt a rounded shape. Protoplasts assembled functional contractile rings that constricted without septation by sliding along the plasma membrane without dividing the cell. Because we could manipulate the shapes of protoplast cells, we could test the influence of cell shape on ring constriction dynamics and distinguish between dynamically autonomous and dynamically coupled constriction dynamics. In compressed protoplasts that had a partially flattened shape, contractile rings adopted characteristic bent shapes during constriction that were in remarkably close quantitative and parameter-free agreement with a mathematical model that assumed the ring produces tension but its constriction rate is set by the sliding of ring anchors in the membrane. Thus, ring constriction in fission yeast protoplasts is dynamically coupled: the ring does not set its own constriction rate. Dynamically autonomous models could not reproduce our experimental observations. Our results suggest that in normal yeast cells the constriction rate is determined by the septum growth rate or other coupled process and the role of the ring could be to exert tension on the septum to regulate its growth.