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ABSTRACT The fission yeastSchizosaccharomyces pombedivides via closed mitosis, meaning that spindle elongation and chromosome segregation transpire entirely within the closed nuclear envelope. Both the spindle and nuclear envelope must undergo shape changes and exert varying forces on each other during this process. Previous work has demonstrated that nuclear envelope expansion (Yam, He, Zhang, Chiam, & Oliferenko, 2011; Mori & Oliferenko, 2020) and spindle pole body (SPB) embedding in the nuclear envelope are required for normalS. pombemitosis, and mechanical modeling has described potential contributions of the spindle to nuclear morphology (Fang et al., 2020; Zhu et al., 2016). However, it is not yet fully clear how and to what extent the nuclear envelope and mitotic spindle each directly shape each other during closed mitosis. Here, we investigate this relationship by observing the behaviors of spindles and nuclei in live mitotic fission yeast following laser ablation. First, we characterize these dynamics in mitoticS. pombenuclei with increased envelope tension, finding that nuclear envelope tension can both bend the spindle and slow elongation. Next, we directly probe the mechanical connection between spindles and nuclear envelopes by ablating each structure. We demonstrate that envelope tension can be relieved by severing spindles and that spindle compression can be relieved by rupturing the envelope. We interpret our experimental data via two quantitative models that demonstrate that fission yeast spindles and nuclear envelopes are a mechanical pair that can each shape the other's morphology.
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Mechanical Mechanisms of Chromosome Segregation
Chromosome segregation—the partitioning of genetic material into two daughter cells—is one of the most crucial processes in cell division. In all Eukaryotes, chromosome segregation is driven by the spindle, a microtubule-based, self-organizing subcellular structure. Extensive research performed over the past 150 years has identified numerous commonalities and contrasts between spindles in different systems. In this review, we use simple coarse-grained models to organize and integrate previous studies of chromosome segregation. We discuss sites of force generation in spindles and fundamental mechanical principles that any understanding of chromosome segregation must be based upon. We argue that conserved sites of force generation may interact differently in different spindles, leading to distinct mechanical mechanisms of chromosome segregation. We suggest experiments to determine which mechanical mechanism is operative in a particular spindle under study. Finally, we propose that combining biophysical experiments, coarse-grained theories, and evolutionary genetics will be a productive approach to enhance our understanding of chromosome segregation in the future.
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- Award ID(s):
- 1764269
- PAR ID:
- 10328912
- Date Published:
- Journal Name:
- Cells
- Volume:
- 10
- Issue:
- 2
- ISSN:
- 2073-4409
- Page Range / eLocation ID:
- 465
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/cells10020465
