Abstract
Cells can position multiple copies of components like carboxysomes, nucleoids, and nuclei at regular intervals. By controlling positions, cells, for example, ensure equal partitioning of organelles over daughter cells and, in the case of nuclei, control cell sizes during cellularization. Mechanisms that generate regular patterns are as yet poorly understood. We used fission yeast cell cycle mutants to investigate the dispersion of multiple nuclei by microtubule-generated forces in single cells. After removing internuclear attractive forces by microtubule-based molecular motors, we observed the establishment of regular patterns of nuclei. Based on live-cell imaging, we hypothesized that microtubule growth within internuclear spaces pushes neighbouring nuclei apart. In the proposed mechanism, which was validated by stochastic simulations, the repulsive force weakens with increasing separation because stochastic shortening events limit the extent over which microtubules generate forces. Our results, therefore, demonstrate how cells can exploit the dynamics of microtubule growth for the equidistant positioning of organelles.
Highlights
Generation of internuclear attractive forces by minus-end-directed motors was, demonstrated during cell division when duplicated nuclei momentarily share a single cell before cytokinesis divides the cell in two
Removal of internuclear attractive forces exposed a hidden positioning mechanism that was adaptive to cell length
Our simulations demonstrate that barrier-induced catastrophes are sufficient for achieving equidistant positioning of nuclei, but unconstrained catastrophes, especially at the rate observed in yeast, are required to reduce fluctuations in internuclear distances and to speed up nuclear repositioning to the levels observed in tetranucleated cells (Fig. S1B and Fig. 3c)
Summary
Wild-type fission yeast cells have a single nucleus during interphase From this nucleus, plus ends of microtubules grow away and generate pushing forces in contact with cell ends. Generation of internuclear attractive forces by minus-end-directed motors was, demonstrated during cell division when duplicated nuclei momentarily share a single cell before cytokinesis divides the cell in two. Fission yeast cells with more than two nuclei can be experimentally obtained using mutations in cell cycle genes that cause cells to undergo multiple rounds of nuclear division without completing cytokinesis. We observed that these mutants can form equidistant nuclear patterns in the absence of motor-driven internuclear attractive forces. Stochastic switching between microtubule growth and shrinkage (dynamic instability) ensures that the net repulsion force between nuclei is distance-dependent, a prerequisite for the formation of equidistant patterns
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