Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast
- UCSF, United States
- Massachusetts Institute of Technology, United States
- Korea Institute of Science and Technology, Republic of Korea
- University of Amsterdam, Netherlands
- Stanford University, United States
Abstract
Intracellular density impacts the physical nature of the cytoplasm and can globally affect cellular processes, yet density regulation remains poorly understood. Here, using a new quantitative phase imaging method, we determined that dry-mass density in fission yeast is maintained in a narrow distribution and exhibits homeostatic behavior. However, density varied during the cell cycle, decreasing during G2, increasing in mitosis and cytokinesis, and dropping rapidly at cell birth. These density variations were explained by a constant rate of biomass synthesis, coupled to slowdown of volume growth during cell division and rapid expansion post-cytokinesis. Arrest at specific cell-cycle stages exacerbated density changes. Spatially heterogeneous patterns of density suggested links between density regulation, tip growth, and intracellular osmotic pressure. Our results demonstrate that systematic density variations during the cell cycle are predominantly due to modulation of volume expansion, and reveal functional consequences of density gradients and cell-cycle arrests.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Custom Matlab code used for image analysis has been posted online at the Github repository https://bitbucket.org/kchuanglab/quantitative-phase-imaging/src/master/.
Article and author information
Author details
Kerwyn Casey Huang
Funding
Swiss National Foundation (P2ELP3_172318)
- Pascal D Odermatt
Swiss National Foundation (P400PB_180872)
- Pascal D Odermatt
National Institute of General Medical Sciences (NIH GM056836)
- Fred Chang
Wellcome Trust (110275/Z/15/Z)
- Teemu P Miettinen
Chan Zuckerberg Initiative
- Kerwyn Casey Huang
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Mohan K Balasubramanian, University of Warwick, United Kingdom
Version history
- Received: November 14, 2020
- Accepted: June 7, 2021
- Accepted Manuscript published: June 8, 2021 (version 1)
- Version of Record published: June 23, 2021 (version 2)
Copyright
© 2021, Odermatt et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast
eLife 10:e64901.
https://doi.org/10.7554/eLife.64901
Further reading
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- Cell Biology
The spindle assembly checkpoint (SAC) temporally regulates mitosis by preventing progression from metaphase to anaphase until all chromosomes are correctly attached to the mitotic spindle. Centrosomes refine the spatial organization of the mitotic spindle at the spindle poles. However, centrosome loss leads to elongated mitosis, suggesting that centrosomes also inform the temporal organization of mitosis in mammalian cells. Here, we find that the mitotic delay in acentrosomal cells is enforced by the SAC in a MPS1-dependent manner, and that a SAC-dependent mitotic delay is required for bipolar cell division to occur in acentrosomal cells. Although acentrosomal cells become polyploid, polyploidy is not sufficient to cause dependency on a SAC-mediated delay to complete cell division. Rather, the division failure in absence of MPS1 activity results from mitotic exit occurring before acentrosomal spindles can become bipolar. Furthermore, prevention of centrosome separation suffices to make cell division reliant on a SAC-dependent mitotic delay. Thus, centrosomes and their definition of two spindle poles early in mitosis provide a ‘timely two-ness’ that allows cell division to occur in absence of a SAC-dependent mitotic delay.
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- Cell Biology
Fertilization occurs before the completion of oocyte meiosis in the majority of animal species and sperm contents move long distances within the zygotes of mouse and C. elegans. If incorporated into the meiotic spindle, paternal chromosomes could be expelled into a polar body resulting in lethal monosomy. Through live imaging of fertilization in C. elegans, we found that the microtubule disassembling enzymes, katanin and kinesin-13 limit long-range movement of sperm contents and that maternal ataxin-2 maintains paternal DNA and paternal mitochondria as a cohesive unit that moves together. Depletion of katanin or double depletion of kinesin-13 and ataxin-2 resulted in the capture of the sperm contents by the meiotic spindle. Thus limiting movement of sperm contents and maintaining cohesion of sperm contents within the zygote both contribute to preventing premature interaction between maternal and paternal genomes.
