Nuclear Repulsion Enables Division Autonomy in a Single Cytoplasm

• Published in: Current biology 2013-10, Vol.23 (20), p.1999-2010
• Main Authors: Anderson, Cori A., Eser, Umut, Korndorf, Therese, Borsuk, Mark E., Skotheim, Jan M., Gladfelter, Amy S.
• Format: Article
• Language: English
• Subjects: Ashbya gossypii; Cell Nucleus Division - physiology; Cytoplasm - physiology; cytosol; Eremothecium - cytology; Eremothecium - physiology; Eremothecium gossypii; fungi; giant cells; Giant Cells - cytology; Giant Cells - physiology; Green Fluorescent Proteins - metabolism; memory; Microscopy; microtubules; mitosis; Time-Lapse Imaging
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2013.07.076

Current models of cell-cycle control, based on classic studies of fused cells, predict that nuclei in a shared cytoplasm respond to the same CDK activities to undergo synchronous cycling. However, synchrony is rarely observed in naturally occurring syncytia, such as the multinucleate fungus Ashbya gossypii. In this system, nuclei divide asynchronously, raising the question of how nuclear timing differences are maintained despite sharing a common milieu. We observe that neighboring nuclei are highly variable in division-cycle duration and that neighbors repel one another to space apart and demarcate their own cytoplasmic territories. The size of these territories increases as a nucleus approaches mitosis and can influence cycling rates. This nonrandom nuclear spacing is regulated by microtubules and is required for nuclear asynchrony, as nuclei that transiently come in very close proximity will partially synchronize. Sister nuclei born of the same mitosis are generally not persistent neighbors over their lifetimes yet remarkably retain similar division cycle times. This indicates that nuclei carry a memory of their birth state that influences their division timing and supports that nuclei subdivide a common cytosol into functionally distinct yet mobile compartments. These findings support that nuclei use cytoplasmic microtubules to establish “cells within cells.” Individual compartments appear to push against one another to compete for cytoplasmic territory and insulate the division cycle. This provides a mechanism by which syncytial nuclei can spatially organize cell-cycle signaling and suggests size control can act in a system without physical boundaries. [Display omitted] •Nuclear division time is inherited despite lineages mixing in one cytoplasm•Nuclei repel neighbors to demarcate independent cytoplasmic territories•Nuclear territory size is sensed and controlled through the cell cycle•Nuclear spacing is controlled by microtubules and required for nuclear asynchrony