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

Allard, Corey A.  H.; Decker, Franziska; Weiner, Orion D.; Toettcher, Jared E.; Graziano, Brian R.; Martin, Sophie G.

doi:10.1371/journal.pone.0209301

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

Journal Article · Fri Dec 21 00:00:00 EST 2018 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0209301· OSTI ID:1561878

^[1];

^[2];

^[3]; Toettcher, Jared E. ^[4];

^[3]; Martin, Sophie G. ^[5]

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

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1561878

Journal Information:: PLoS ONE, Vol. 13, Issue 12; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 6 works

Citation information provided by
Web of Science

References (48)

Swe1p Responds to Cytoskeletal Perturbation, Not Bud Size, in S. cerevisiae McNulty, John J.; Lew, Daniel J. Current Biology, Vol. 15, Issue 24 https://doi.org/10.1016/j.cub.2005.11.039	journal	December 2005
Mitotic role for the Cdc28 protein kinase of Saccharomyces cerevisiae. Reed, S. I.; Wittenberg, C. Proceedings of the National Academy of Sciences, Vol. 87, Issue 15 https://doi.org/10.1073/pnas.87.15.5697	journal	August 1990
Size control in mammalian cells involves modulation of both growth rate and cell cycle duration Cadart, Clotilde; Monnier, Sylvain; Grilli, Jacopo Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05393-0	journal	August 2018
Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma Gregory, T. Ryan Biological Reviews of the Cambridge Philosophical Society, Vol. 76, Issue 1 https://doi.org/10.1017/s1464793100005595	journal	February 2001
Cortical regulation of cell size by a sizer cdr2p Pan, Kally Z.; Saunders, Timothy E.; Flor-Parra, Ignacio eLife, Vol. 3 https://doi.org/10.7554/elife.02040	journal	March 2014
Cell-Size Control and Homeostasis in Bacteria Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T. Current Biology, Vol. 27, Issue 9 https://doi.org/10.1016/j.cub.2017.04.028	journal	May 2017
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Sikorski, R. S.; Hieter, P. Genetics, Vol. 122, Issue 1 https://doi.org/10.1093/genetics/122.1.19	journal	May 1989
The Regulation of Cell Size Lloyd, Alison C. Cell, Vol. 154, Issue 6 https://doi.org/10.1016/j.cell.2013.08.053	journal	September 2013
Archaeal cells share common size control with bacteria despite noisier growth and division Eun, Ye-Jin; Ho, Po-Yi; Kim, Minjeong Nature Microbiology, Vol. 3, Issue 2 https://doi.org/10.1038/s41564-017-0082-6	journal	December 2017
Cell Growth and Size Homeostasis in Proliferating Animal Cells Tzur, Amit; Kafri, Ran; LeBleu, Valerie S. Science, Vol. 325, Issue 5937 https://doi.org/10.1126/science.1174294	journal	July 2009
The effects of molecular noise and size control on variability in the budding yeast cell cycle Talia, Stefano Di; Skotheim, Jan M.; Bean, James M. Nature, Vol. 448, Issue 7156 https://doi.org/10.1038/nature06072	journal	August 2007
Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size Schmoller, Kurt M.; Turner, J. J.; Kõivomägi, M. Nature, Vol. 526, Issue 7572 https://doi.org/10.1038/nature14908	journal	September 2015
The phenomenology of cell size control Schmoller, Kurt M. Current Opinion in Cell Biology, Vol. 49 https://doi.org/10.1016/j.ceb.2017.11.011	journal	December 2017
Cell-Size Homeostasis and the Incremental Rule in a Bacterial Pathogen Deforet, Maxime; van Ditmarsch, Dave; Xavier, João B. Biophysical Journal, Vol. 109, Issue 3 https://doi.org/10.1016/j.bpj.2015.07.002	journal	August 2015
Single-cell analysis of growth in budding yeast and bacteria reveals a common size regulation strategy Soifer, Ilya; Robert, Lydia; Amir, Ariel arXiv https://doi.org/10.48550/arxiv.1410.4771	text	January 2014
Single-Cell Analysis of Growth in Budding Yeast and Bacteria Reveals a Common Size Regulation Strategy Soifer, Ilya; Robert, Lydia; Amir, Ariel Current Biology, Vol. 26, Issue 3 https://doi.org/10.1016/j.cub.2015.11.067	journal	February 2016
Cell-Size Control Amodeo, Amanda A.; Skotheim, Jan M. Cold Spring Harbor Perspectives in Biology, Vol. 8, Issue 4 https://doi.org/10.1101/cshperspect.a019083	journal	August 2015
Origins of cellular geometry Marshall, Wallace F. BMC Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1741-7007-9-57	journal	August 2011
Cell-Size Control and Homeostasis in Bacteria Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T. Current Biology, Vol. 25, Issue 3 https://doi.org/10.1016/j.cub.2014.12.009	journal	February 2015
Probing Mammalian Cell Size Homeostasis by Channel-Assisted Cell Reshaping Varsano, Giulia; Wang, Yuedi; Wu, Min Cell Reports, Vol. 20, Issue 2 https://doi.org/10.1016/j.celrep.2017.06.057	journal	July 2017
Enzymatic assembly of DNA molecules up to several hundred kilobases Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan Nature Methods, Vol. 6, Issue 5, p. 343-345 https://doi.org/10.1038/nmeth.1318	journal	April 2009
Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling Wedlich-Soldner, Roland; Wai, Stephanie C.; Schmidt, Thomas Journal of Cell Biology, Vol. 166, Issue 6 https://doi.org/10.1083/jcb.200405061	journal	September 2004
On being the right (cell) size Ginzberg, M. B.; Kafri, R.; Kirschner, M. Science, Vol. 348, Issue 6236 https://doi.org/10.1126/science.1245075	journal	May 2015
Cell cycle control of septin ring dynamics in the budding yeast Cid, Vı́ctor J.; Adamiková, Lubica; Nombela, César Microbiology, Vol. 147, Issue 6 https://doi.org/10.1099/00221287-147-6-1437	journal	June 2001
Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae Bender, A.; Pringle, J. R. Molecular and Cellular Biology, Vol. 11, Issue 3 https://doi.org/10.1128/mcb.11.3.1295-1305.1991	journal	March 1991
Wee1-dependent mechanisms required for coordination of cell growth and cell division Kellogg, D. R. Journal of Cell Science, Vol. 116, Issue 24 https://doi.org/10.1242/jcs.00908	journal	December 2003
Endoreplication Cell Cycles Edgar, Bruce A.; Orr-Weaver, Terry L. Cell, Vol. 105, Issue 3 https://doi.org/10.1016/S0092-8674(01)00334-8	journal	May 2001
Coordination of growth with cell division in the yeast Johnston, G.; Pringle, J.; Hartwell, L. Experimental Cell Research, Vol. 105, Issue 1 https://doi.org/10.1016/0014-4827(77)90154-9	journal	March 1977
The rate of cell growth is governed by cell cycle stage Goranov, A. I.; Cook, M.; Ricicova, M. Genes & Development, Vol. 23, Issue 12 https://doi.org/10.1101/gad.1777309	journal	June 2009
Cell growth, cell division and cell size homeostasis in Swiss 3T3 cells Brooks, Robert F.; Shields, Robert Experimental Cell Research, Vol. 156, Issue 1 https://doi.org/10.1016/0014-4827(85)90255-1	journal	January 1985
Tropomyosin-containing Actin Cables Direct the Myo2p-dependent Polarized Delivery of Secretory Vesicles in Budding Yeast Pruyne, David W.; Schott, Daniel H.; Bretscher, Anthony Journal of Cell Biology, Vol. 143, Issue 7 https://doi.org/10.1083/jcb.143.7.1931	journal	November 1998
Rate of macromolecular synthesis through the cell cycle of the yeast Saccharomyces cerevisiae. Elliott, S. G.; McLaughlin, C. S. Proceedings of the National Academy of Sciences, Vol. 75, Issue 9 https://doi.org/10.1073/pnas.75.9.4384	journal	September 1978
The Adder Phenomenon Emerges from Independent Control of Pre- and Post-Start Phases of the Budding Yeast Cell Cycle Chandler-Brown, Devon; Schmoller, Kurt M.; Winetraub, Yonatan Current Biology, Vol. 27, Issue 18 https://doi.org/10.1016/j.cub.2017.08.015	journal	September 2017
Forced periodic expression of G1 cyclins phase-locks the budding yeast cell cycle Charvin, G.; Cross, F. R.; Siggia, E. D. Proceedings of the National Academy of Sciences, Vol. 106, Issue 16 https://doi.org/10.1073/pnas.0809227106	journal	April 2009
Probing Yeast Polarity with Acute, Reversible, Optogenetic Inhibition of Protein Function Jost, Anna Payne-Tobin; Weiner, Orion D. ACS Synthetic Biology, Vol. 4, Issue 10 https://doi.org/10.1021/acssynbio.5b00053	journal	June 2015
Organelle Growth Control through Limiting Pools of Cytoplasmic Components Goehring, Nathan W.; Hyman, Anthony A. Current Biology, Vol. 22, Issue 9 https://doi.org/10.1016/j.cub.2012.03.046	journal	May 2012
Machine learning discovery of missing links that mediate alternative branches to plant alkaloids Vavricka, Christopher J.; Takahashi, Shunsuke; Watanabe, Naoki Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28883-8	journal	March 2022
Spatiotemporal control of cell signalling using a light-switchable protein interaction Levskaya, Anselm; Weiner, Orion D.; Lim, Wendell A. Nature, Vol. 461, Issue 7266 https://doi.org/10.1038/nature08446	journal	September 2009
Using buoyant mass to measure the growth of single cells Godin, Michel; Delgado, Francisco Feijó; Son, Sungmin Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.1452	journal	April 2010
A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains Chenevert, Janet; Corrado, Kathleen; Bender, Alan Nature, Vol. 356, Issue 6364 https://doi.org/10.1038/356077a0	journal	March 1992
Cell Size Regulation in Bacteria Amir, Ariel Physical Review Letters, Vol. 112, Issue 20 https://doi.org/10.1103/PhysRevLett.112.208102	journal	May 2014
Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division Hartwell, L. H. The Journal of Cell Biology, Vol. 75, Issue 2 https://doi.org/10.1083/jcb.75.2.422	journal	November 1977
The duration of mitosis and daughter cell size are modulated by nutrients in budding yeast Leitao, Ricardo M.; Kellogg, Douglas R. The Journal of Cell Biology, Vol. 216, Issue 11 https://doi.org/10.1083/jcb.201609114	journal	September 2017
Cell Size Control in Yeast Turner, Jonathan J.; Ewald, Jennifer C.; Skotheim, Jan M. Current Biology, Vol. 22, Issue 9 https://doi.org/10.1016/j.cub.2012.02.041	journal	May 2012
Conservation of Mechanisms Controlling Entry into Mitosis Harvey, Stacy L.; Kellogg, Douglas R. Current Biology, Vol. 13, Issue 4 https://doi.org/10.1016/S0960-9822(03)00049-6	journal	February 2003
A Constant Size Extension Drives Bacterial Cell Size Homeostasis Campos, Manuel; Surovtsev, Ivan V.; Kato, Setsu Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.11.022	journal	December 2014
Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Bender, A.; Pringle, J. R. Molecular and Cellular Biology, Vol. 11, Issue 3 https://doi.org/10.1128/mcb.11.3.1295	journal	March 1991
Control of cell size and cycle time in Schizosaccharomyces pombe Fantes, P. A. Journal of Cell Science, Vol. 24, Issue 1 https://doi.org/10.1242/jcs.24.1.51	journal	April 1977