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Title: A size-invariant bud-duration timer enables robustness in yeast cell size control

Abstract

Cell populations across nearly all forms of life generally maintain a characteristic cell type-dependent size, but how size control is achieved has been a long-standing question. The G1/S boundary of the cell cycle serves as a major point of size control, and mechanisms operating here restrict passage of cells to Start if they are too small. In contrast, it is less clear how size is regulated post-Start, during S/G2/M. To gain further insight into post-Start size control, we prepared budding yeast that can be reversibly blocked from bud initiation. While blocked, cells continue to grow isotropically, increasing their volume by more than an order of magnitude over unperturbed cells. Upon release from their block, giant mothers reenter the cell cycle and their progeny rapidly return to the original unperturbed size. We found this behavior to be consistent with a size-invariant 'timer' specifying the duration of S/G2/M. These results indicate that yeast use at least two distinct mechanisms at different cell cycle phases to ensure size homeostasis.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4]; ORCiD logo [3];  [5]
  1. Marine Biological Lab., Woods Hole, MA (United States); Geisel School of Medicine at Dartmouth, Hanover, NH (United States)
  2. Marine Biological Lab., Woods Hole, MA (United States); Max Planck Inst. for the Physics of Complex Systems, Max Planck Inst. of Molecular Cell Biology and Genetics, Dresden (Germany). Center for Systems Biology Dresden
  3. Marine Biological Lab., Woods Hole, MA (United States); Univ. of California, San Francisco, CA (United States)
  4. Marine Biological Lab., Woods Hole, MA (United States); Princeton Univ., NJ (United States)
  5. Univ. of Lausanne, Lausanne (Switzerland); editor
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1561878
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 13; Journal Issue: 12; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Allard, Corey A. H., Decker, Franziska, Weiner, Orion D., Toettcher, Jared E., Graziano, Brian R., and Martin, Sophie G. A size-invariant bud-duration timer enables robustness in yeast cell size control. United States: N. p., 2018. Web. doi:10.1371/journal.pone.0209301.
Allard, Corey A. H., Decker, Franziska, Weiner, Orion D., Toettcher, Jared E., Graziano, Brian R., & Martin, Sophie G. A size-invariant bud-duration timer enables robustness in yeast cell size control. United States. doi:10.1371/journal.pone.0209301.
Allard, Corey A. H., Decker, Franziska, Weiner, Orion D., Toettcher, Jared E., Graziano, Brian R., and Martin, Sophie G. Fri . "A size-invariant bud-duration timer enables robustness in yeast cell size control". United States. doi:10.1371/journal.pone.0209301. https://www.osti.gov/servlets/purl/1561878.
@article{osti_1561878,
title = {A size-invariant bud-duration timer enables robustness in yeast cell size control},
author = {Allard, Corey A. H. and Decker, Franziska and Weiner, Orion D. and Toettcher, Jared E. and Graziano, Brian R. and Martin, Sophie G.},
abstractNote = {Cell populations across nearly all forms of life generally maintain a characteristic cell type-dependent size, but how size control is achieved has been a long-standing question. The G1/S boundary of the cell cycle serves as a major point of size control, and mechanisms operating here restrict passage of cells to Start if they are too small. In contrast, it is less clear how size is regulated post-Start, during S/G2/M. To gain further insight into post-Start size control, we prepared budding yeast that can be reversibly blocked from bud initiation. While blocked, cells continue to grow isotropically, increasing their volume by more than an order of magnitude over unperturbed cells. Upon release from their block, giant mothers reenter the cell cycle and their progeny rapidly return to the original unperturbed size. We found this behavior to be consistent with a size-invariant 'timer' specifying the duration of S/G2/M. These results indicate that yeast use at least two distinct mechanisms at different cell cycle phases to ensure size homeostasis.},
doi = {10.1371/journal.pone.0209301},
journal = {PLoS ONE},
issn = {1932-6203},
number = 12,
volume = 13,
place = {United States},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Fig 1 Fig 1: Control of yeast cell size using optogenetics. (A) Exogenous PhyB (phytochrome B; dark green) is fused to the C-terminus of S. cerevisiae Tom20, anchoring it to the mitochondria outer membrane (orange). PIF (phytochromeinteracting factor; light green) is fused to endogenous Bem1 (blue). Illumination with red light drives amore » conformational change in PhyB allowing it to bind PIF-Bem1. Conversely, illumination with infrared (IR) light drives the reverse reaction, releasing PIF-Bem1. (B) Production of ‘giant’ yeast using reversible optogenetic-based Bem1 disruption. (C) Cells were illuminated with red light for 8 h (indicated by red borders) and imaged every 10 min using bright-field microscopy. (D) Following red light illumination for 6–10 hours as in Fig 1C, large cells were illuminated with IR light (indicated by grey borders) and imaged every 5–10 min using bright-field microscopy.« less

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