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:
-
- Marine Biological Lab., Woods Hole, MA (United States); Geisel School of Medicine at Dartmouth, Hanover, NH (United States)
- 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
- Marine Biological Lab., Woods Hole, MA (United States); Univ. of California, San Francisco, CA (United States)
- Marine Biological Lab., Woods Hole, MA (United States); Princeton Univ., NJ (United States)
- Univ. of Lausanne, Lausanne (Switzerland); editor
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1561878
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- 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. https://doi.org/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. https://doi.org/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},
number = 12,
volume = 13,
place = {United States},
year = {Fri Dec 21 00:00:00 EST 2018},
month = {Fri Dec 21 00:00:00 EST 2018}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Swe1p Responds to Cytoskeletal Perturbation, Not Bud Size, in S. cerevisiae
journal, December 2005
- McNulty, John J.; Lew, Daniel J.
- Current Biology, Vol. 15, Issue 24
Swe1p Responds to Cytoskeletal Perturbation, Not Bud Size, in S. cerevisiae
journal, December 2005
- McNulty, John J.; Lew, Daniel J.
- Current Biology, Vol. 15, Issue 24
Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae.
journal, August 1990
- Reed, S. I.; Wittenberg, C.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 15
Size control in mammalian cells involves modulation of both growth rate and cell cycle duration
journal, August 2018
- Cadart, Clotilde; Monnier, Sylvain; Grilli, Jacopo
- Nature Communications, Vol. 9, Issue 1
Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma
journal, February 2001
- Gregory, T. Ryan
- Biological Reviews of the Cambridge Philosophical Society, Vol. 76, Issue 1
Cortical regulation of cell size by a sizer cdr2p
journal, March 2014
- Pan, Kally Z.; Saunders, Timothy E.; Flor-Parra, Ignacio
- eLife, Vol. 3
Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae.
journal, August 1990
- Reed, S. I.; Wittenberg, C.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 15
Cell-Size Control and Homeostasis in Bacteria
journal, May 2017
- Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T.
- Current Biology, Vol. 27, Issue 9
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
journal, May 1989
- Sikorski, R. S.; Hieter, P.
- Genetics, Vol. 122, Issue 1
Archaeal cells share common size control with bacteria despite noisier growth and division
journal, December 2017
- Eun, Ye-Jin; Ho, Po-Yi; Kim, Minjeong
- Nature Microbiology, Vol. 3, Issue 2
Cell Growth and Size Homeostasis in Proliferating Animal Cells
journal, July 2009
- Tzur, Amit; Kafri, Ran; LeBleu, Valerie S.
- Science, Vol. 325, Issue 5937
The effects of molecular noise and size control on variability in the budding yeast cell cycle
journal, August 2007
- Talia, Stefano Di; Skotheim, Jan M.; Bean, James M.
- Nature, Vol. 448, Issue 7156
Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size
journal, September 2015
- Schmoller, Kurt M.; Turner, J. J.; Kõivomägi, M.
- Nature, Vol. 526, Issue 7572
The phenomenology of cell size control
journal, December 2017
- Schmoller, Kurt M.
- Current Opinion in Cell Biology, Vol. 49
Cell-Size Homeostasis and the Incremental Rule in a Bacterial Pathogen
journal, August 2015
- Deforet, Maxime; van Ditmarsch, Dave; Xavier, João B.
- Biophysical Journal, Vol. 109, Issue 3
Single-cell analysis of growth in budding yeast and bacteria reveals a common size regulation strategy
text, January 2014
- Soifer, Ilya; Robert, Lydia; Amir, Ariel
- arXiv
Single-Cell Analysis of Growth in Budding Yeast and Bacteria Reveals a Common Size Regulation Strategy
journal, February 2016
- Soifer, Ilya; Robert, Lydia; Amir, Ariel
- Current Biology, Vol. 26, Issue 3
Cell-Size Control
journal, August 2015
- Amodeo, Amanda A.; Skotheim, Jan M.
- Cold Spring Harbor Perspectives in Biology, Vol. 8, Issue 4
Cell-Size Control and Homeostasis in Bacteria
journal, February 2015
- Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T.
- Current Biology, Vol. 25, Issue 3
Probing Mammalian Cell Size Homeostasis by Channel-Assisted Cell Reshaping
journal, July 2017
- Varsano, Giulia; Wang, Yuedi; Wu, Min
- Cell Reports, Vol. 20, Issue 2
Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009
- Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
- Nature Methods, Vol. 6, Issue 5, p. 343-345
Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling
journal, September 2004
- Wedlich-Soldner, Roland; Wai, Stephanie C.; Schmidt, Thomas
- Journal of Cell Biology, Vol. 166, Issue 6
On being the right (cell) size
journal, May 2015
- Ginzberg, M. B.; Kafri, R.; Kirschner, M.
- Science, Vol. 348, Issue 6236
Cell cycle control of septin ring dynamics in the budding yeast
journal, June 2001
- Cid, Vı́ctor J.; Adamiková, Lubica; Nombela, César
- Microbiology, Vol. 147, Issue 6
Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae
journal, March 1991
- Bender, A.; Pringle, J. R.
- Molecular and Cellular Biology, Vol. 11, Issue 3
Wee1-dependent mechanisms required for coordination of cell growth and cell division
journal, December 2003
- Kellogg, D. R.
- Journal of Cell Science, Vol. 116, Issue 24
Endoreplication Cell Cycles
journal, May 2001
- Edgar, Bruce A.; Orr-Weaver, Terry L.
- Cell, Vol. 105, Issue 3
Coordination of growth with cell division in the yeast
journal, March 1977
- Johnston, G.; Pringle, J.; Hartwell, L.
- Experimental Cell Research, Vol. 105, Issue 1
The rate of cell growth is governed by cell cycle stage
journal, June 2009
- Goranov, A. I.; Cook, M.; Ricicova, M.
- Genes & Development, Vol. 23, Issue 12
Cell growth, cell division and cell size homeostasis in Swiss 3T3 cells
journal, January 1985
- Brooks, Robert F.; Shields, Robert
- Experimental Cell Research, Vol. 156, Issue 1
Tropomyosin-containing Actin Cables Direct the Myo2p-dependent Polarized Delivery of Secretory Vesicles in Budding Yeast
journal, November 1998
- Pruyne, David W.; Schott, Daniel H.; Bretscher, Anthony
- Journal of Cell Biology, Vol. 143, Issue 7
Wee1-dependent mechanisms required for coordination of cell growth and cell division
journal, December 2003
- Kellogg, D. R.
- Journal of Cell Science, Vol. 116, Issue 24
Cell growth, cell division and cell size homeostasis in Swiss 3T3 cells
journal, January 1985
- Brooks, Robert F.; Shields, Robert
- Experimental Cell Research, Vol. 156, Issue 1
Rate of macromolecular synthesis through the cell cycle of the yeast Saccharomyces cerevisiae.
journal, September 1978
- Elliott, S. G.; McLaughlin, C. S.
- Proceedings of the National Academy of Sciences, Vol. 75, Issue 9
The Adder Phenomenon Emerges from Independent Control of Pre- and Post-Start Phases of the Budding Yeast Cell Cycle
journal, September 2017
- Chandler-Brown, Devon; Schmoller, Kurt M.; Winetraub, Yonatan
- Current Biology, Vol. 27, Issue 18
The Adder Phenomenon Emerges from Independent Control of Pre- and Post-Start Phases of the Budding Yeast Cell Cycle
journal, September 2017
- Chandler-Brown, Devon; Schmoller, Kurt M.; Winetraub, Yonatan
- Current Biology, Vol. 27, Issue 18
Forced periodic expression of G1 cyclins phase-locks the budding yeast cell cycle
journal, April 2009
- Charvin, G.; Cross, F. R.; Siggia, E. D.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 16
Rate of macromolecular synthesis through the cell cycle of the yeast Saccharomyces cerevisiae.
journal, September 1978
- Elliott, S. G.; McLaughlin, C. S.
- Proceedings of the National Academy of Sciences, Vol. 75, Issue 9
Probing Yeast Polarity with Acute, Reversible, Optogenetic Inhibition of Protein Function
journal, June 2015
- Jost, Anna Payne-Tobin; Weiner, Orion D.
- ACS Synthetic Biology, Vol. 4, Issue 10
Cell cycle control of septin ring dynamics in the budding yeast
journal, June 2001
- Cid, Vı́ctor J.; Adamiková, Lubica; Nombela, César
- Microbiology, Vol. 147, Issue 6
On being the right (cell) size
journal, May 2015
- Ginzberg, M. B.; Kafri, R.; Kirschner, M.
- Science, Vol. 348, Issue 6236
Organelle Growth Control through Limiting Pools of Cytoplasmic Components
journal, May 2012
- Goehring, Nathan W.; Hyman, Anthony A.
- Current Biology, Vol. 22, Issue 9
Machine learning discovery of missing links that mediate alternative branches to plant alkaloids
journal, March 2022
- Vavricka, Christopher J.; Takahashi, Shunsuke; Watanabe, Naoki
- Nature Communications, Vol. 13, Issue 1
Spatiotemporal control of cell signalling using a light-switchable protein interaction
journal, September 2009
- Levskaya, Anselm; Weiner, Orion D.; Lim, Wendell A.
- Nature, Vol. 461, Issue 7266
Using buoyant mass to measure the growth of single cells
journal, April 2010
- Godin, Michel; Delgado, Francisco Feijó; Son, Sungmin
- Nature Methods, Vol. 7, Issue 5
A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains
journal, March 1992
- Chenevert, Janet; Corrado, Kathleen; Bender, Alan
- Nature, Vol. 356, Issue 6364
Cell Size Regulation in Bacteria
journal, May 2014
- Amir, Ariel
- Physical Review Letters, Vol. 112, Issue 20
Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size
journal, September 2015
- Schmoller, Kurt M.; Turner, J. J.; Kõivomägi, M.
- Nature, Vol. 526, Issue 7572
Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division
journal, November 1977
- Hartwell, L. H.
- The Journal of Cell Biology, Vol. 75, Issue 2
The duration of mitosis and daughter cell size are modulated by nutrients in budding yeast
journal, September 2017
- Leitao, Ricardo M.; Kellogg, Douglas R.
- The Journal of Cell Biology, Vol. 216, Issue 11
Spatiotemporal control of cell signalling using a light-switchable protein interaction
journal, September 2009
- Levskaya, Anselm; Weiner, Orion D.; Lim, Wendell A.
- Nature, Vol. 461, Issue 7266
Cell Size Control in Yeast
journal, May 2012
- Turner, Jonathan J.; Ewald, Jennifer C.; Skotheim, Jan M.
- Current Biology, Vol. 22, Issue 9
The phenomenology of cell size control
journal, December 2017
- Schmoller, Kurt M.
- Current Opinion in Cell Biology, Vol. 49
Cell-Size Control and Homeostasis in Bacteria
journal, February 2015
- Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T.
- Current Biology, Vol. 25, Issue 3
Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division
journal, November 1977
- Hartwell, L. H.
- The Journal of Cell Biology, Vol. 75, Issue 2
Cell Size Control in Yeast
journal, May 2012
- Turner, Jonathan J.; Ewald, Jennifer C.; Skotheim, Jan M.
- Current Biology, Vol. 22, Issue 9
Forced periodic expression of G1 cyclins phase-locks the budding yeast cell cycle
journal, April 2009
- Charvin, G.; Cross, F. R.; Siggia, E. D.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 16
Conservation of Mechanisms Controlling Entry into Mitosis
journal, February 2003
- Harvey, Stacy L.; Kellogg, Douglas R.
- Current Biology, Vol. 13, Issue 4
Cell-Size Control
journal, August 2015
- Amodeo, Amanda A.; Skotheim, Jan M.
- Cold Spring Harbor Perspectives in Biology, Vol. 8, Issue 4
A Constant Size Extension Drives Bacterial Cell Size Homeostasis
journal, December 2014
- Campos, Manuel; Surovtsev, Ivan V.; Kato, Setsu
- Cell, Vol. 159, Issue 6
Probing Mammalian Cell Size Homeostasis by Channel-Assisted Cell Reshaping
journal, July 2017
- Varsano, Giulia; Wang, Yuedi; Wu, Min
- Cell Reports, Vol. 20, Issue 2
Archaeal cells share common size control with bacteria despite noisier growth and division
journal, December 2017
- Eun, Ye-Jin; Ho, Po-Yi; Kim, Minjeong
- Nature Microbiology, Vol. 3, Issue 2
The effects of molecular noise and size control on variability in the budding yeast cell cycle
journal, August 2007
- Talia, Stefano Di; Skotheim, Jan M.; Bean, James M.
- Nature, Vol. 448, Issue 7156
Using buoyant mass to measure the growth of single cells
journal, April 2010
- Godin, Michel; Delgado, Francisco Feijó; Son, Sungmin
- Nature Methods, Vol. 7, Issue 5
Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae.
journal, March 1991
- Bender, A.; Pringle, J. R.
- Molecular and Cellular Biology, Vol. 11, Issue 3
Organelle Growth Control through Limiting Pools of Cytoplasmic Components
journal, May 2012
- Goehring, Nathan W.; Hyman, Anthony A.
- Current Biology, Vol. 22, Issue 9
Probing Yeast Polarity with Acute, Reversible, Optogenetic Inhibition of Protein Function
journal, June 2015
- Jost, Anna Payne-Tobin; Weiner, Orion D.
- ACS Synthetic Biology, Vol. 4, Issue 10
Control of cell size and cycle time in Schizosaccharomyces pombe
journal, April 1977
- Fantes, P. A.
- Journal of Cell Science, Vol. 24, Issue 1
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
journal, May 1989
- Sikorski, R. S.; Hieter, P.
- Genetics, Vol. 122, Issue 1
Figures / Tables found in this record: