Fission Yeast Contractile Ring Tension Increases ∼2-Fold Throughout Constriction and Regulates Septum Closure but does not Set the Constriction Rate

Abstract

What is the role of the cytokinetic contractile ring? The tensile actomyosin ring is central to cytokinesis, and widely thought to drive cell cleavage as it constricts. Here we directly addressed this question by measurements of cytokinetic ring tension and mathematical modeling. In the model organism fission yeast, as in other fungi, ring constriction is accompanied by septation, the inward growth of cell wall in the wake of the constricting ring that seals daughter cells in new cell wall.We measured ring tensions in live fission yeast protoplasts using a novel method based on measuring membrane tension and the furrow geometry. As constricted progressed, ring tension increased from ∼ 400 pN to ∼ 800 pN. To our knowledge these are the first measurements of the evolving ring tension throughout constriction.We used these tension values in a mathematical model of septum growth, mediated by beta-glucan synthases (Bgs) at the septum edge, hypothesized mechanosensitive (Thiyagarajan et al., 2015). The stochastic septum growth produced faceting, defects and edge roughness. In simulations, ring tension modulated Bgs growth rates in a curvature-dependent fashion, suppressing defects and roughness so septum edges were nearly circular. Simulated edges had low roughnesses (∼5%) and a roughness exponent ∼0.5, consistent with septum edges we measured in live cells. Our model revealed a mechanosensitivity ∼15% per pN per Bgs complex.Thus, ring tension regulates septum growth to ensure the septum closes as a shrinking circle (not a slit) and daughter cells are properly sealed by new cell wall. However, the model showed constriction rates are set by the septum growth machinery, while ring tension had little effect on the mean rate, explaining why experimentally the rate is constant in time.