β-heavy-spectrin stabilizes the constricting contractile ring during cytokinesis

Silva et al. show that plastin/PLST-1 and the beta-heavy-spectrin/SMA-1 make distinct contributions to constriction of the cytokinetic contractile ring: PLST-1 promotes F-actin connectivity at the cell cortex and cortical tension that counteracts ring constriction, while beta-heavy-spectrin protects fragile rings from ruptures and facilitates ring repair. Cytokinesis requires the constriction of an actomyosin-based contractile ring and involves multiple F-actin crosslinkers. We show that partial depletion of the C. elegans cytokinetic formin generates contractile rings with low F-actin levels that constrict but are structurally fragile, and we use this background to investigate the roles of the crosslinkers plastin/PLST-1 and beta-heavy-spectrin/SMA-1 during ring constriction. We show that the removal of PLST-1 or SMA-1 has opposite effects on the structural integrity of fragile rings. PLST-1 loss reduces cortical tension that resists ring constriction and makes fragile rings less prone to ruptures and regressions, whereas SMA-1 loss exacerbates structural defects, leading to frequent ruptures and cytokinesis failure. Fragile rings without SMA-1 or containing a shorter SMA-1, repeatedly rupture at the same site, and SMA-1::GFP accumulates at repair sites in fragile rings and in rings cut by laser microsurgery. These results establish that beta-heavy-spectrin stabilizes the constricting ring and reveals the importance of beta-heavy-spectrin size for network connectivity at low F-actin density.

Automated summary

Silva et al. demonstrate the distinct contributions of plastin/PLST-1 and beta-heavy-spectrin/SMA-1 to cytokinetic contractile ring constriction. PLST-1 promotes F-actin connectivity and cortical tension, counteracting ring constriction, while beta-heavy-spectrin protects fragile rings and facilitates ring repair. The loss of PLST-1 reduces cortical tension and makes fragile rings less prone to ruptures and regressions, while the loss of SMA-1 exacerbates structural defects, leading to frequent ruptures and cytokinesis failure. Beta-heavy-spectrin stabilizes the constricting ring and plays a crucial role in network connectivity at low F-actin density.