Characterization of dependencies between growth and division in budding yeast

Mayhew, Michael B.; Iversen, Edwin S.; Hartemink, Alexander J.

doi:10.1098/rsif.2016.0993

Title: Characterization of dependencies between growth and division in budding yeast

Abstract

Cell growth and division are processes vital to the proliferation and development of life. Coordination between these two processes has been recognized for decades in a variety of organisms. In the budding yeast Saccharomyces cerevisiae, this coordination or ‘size control’ appears as an inverse correlation between cell size and the rate of cell-cycle progression, routinely observed in G1 prior to cell division commitment. Beyond this point, cells are presumed to complete S/G₂/M at similar rates and in a size-independent manner. As such, studies of dependence between growth and division have focused on G1. Moreover, in unicellular organisms, coordination between growth and division has commonly been analyzed within the cycle of a single cell without accounting for correlations in growth and division characteristics between cycles of related cells. In a comprehensive analysis of three published time-lapse microscopy datasets, we analyze both intra- and inter-cycle dependencies between growth and division, revisiting assumptions about the coordination between these two processes. Interestingly, we find evidence (1) that S/G₂/M durations are systematically longer in daughters than in mothers, (2) of dependencies between S/G2/M and size at budding that echo the classical G1 dependencies, and, (3) in contrast with recent bacterial studies, of negative dependencies betweenmore »« less

Authors:

^[1]; Iversen, Edwin S. ^[2]; Hartemink, Alexander J. ^[2]

Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Duke Univ., Durham, NC (United States)

Publication Date:: Wed Feb 01 00:00:00 EST 2017

Research Org.:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1349007

Report Number(s):: LLNL-JRNL-702334
Journal ID: ISSN 1742-5689

Grant/Contract Number:: AC52-07NA27344

Resource Type:: Accepted Manuscript

Journal Name:: Journal of the Royal Society Interface

Additional Journal Information:: Journal Volume: 14; Journal Issue: 127; Journal ID: ISSN 1742-5689

Publisher:: The Royal Society

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Mayhew, Michael B., Iversen, Edwin S., and Hartemink, Alexander J. Characterization of dependencies between growth and division in budding yeast.  United States: N. p., 2017. 
Web.  doi:10.1098/rsif.2016.0993.

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                    Mayhew, Michael B., Iversen, Edwin S., & Hartemink, Alexander J. Characterization of dependencies between growth and division in budding yeast.  United States.  https://doi.org/10.1098/rsif.2016.0993

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                    Mayhew, Michael B., Iversen, Edwin S., and Hartemink, Alexander J. Wed .  
"Characterization of dependencies between growth and division in budding yeast".  United States.  https://doi.org/10.1098/rsif.2016.0993.  https://www.osti.gov/servlets/purl/1349007.

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@article{osti_1349007,

  title        = {Characterization of dependencies between growth and division in budding yeast},

  author       = {Mayhew, Michael B. and Iversen, Edwin S. and Hartemink, Alexander J.},

  abstractNote = {Cell growth and division are processes vital to the proliferation and development of life. Coordination between these two processes has been recognized for decades in a variety of organisms. In the budding yeast Saccharomyces cerevisiae, this coordination or ‘size control’ appears as an inverse correlation between cell size and the rate of cell-cycle progression, routinely observed in G1 prior to cell division commitment. Beyond this point, cells are presumed to complete S/G2/M at similar rates and in a size-independent manner. As such, studies of dependence between growth and division have focused on G1. Moreover, in unicellular organisms, coordination between growth and division has commonly been analyzed within the cycle of a single cell without accounting for correlations in growth and division characteristics between cycles of related cells. In a comprehensive analysis of three published time-lapse microscopy datasets, we analyze both intra- and inter-cycle dependencies between growth and division, revisiting assumptions about the coordination between these two processes. Interestingly, we find evidence (1) that S/G2/M durations are systematically longer in daughters than in mothers, (2) of dependencies between S/G2/M and size at budding that echo the classical G1 dependencies, and, (3) in contrast with recent bacterial studies, of negative dependencies between size at birth and size accumulated during the cell cycle. In addition, we develop a novel hierarchical model to uncover inter-cycle dependencies, and we find evidence for such dependencies in cells growing in sugar-poor environments. Our analysis highlights the need for experimentalists and modelers to account for new sources of cell-to-cell variation in growth and division, and our model provides a formal statistical framework for the continued study of dependencies between biological processes.},

  doi          = {10.1098/rsif.2016.0993},

  journal      = {Journal of the Royal Society Interface},

  number       = 127,

  volume       = 14,

  place        = {United States},

  year         = {Wed Feb 01 00:00:00 EST 2017},

  month        = {Wed Feb 01 00:00:00 EST 2017}

}

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Works referenced in this record:

Bayes Factors
journal, June 1995

Kass, Robert E.; Raftery, Adrian E.
Journal of the American Statistical Association, Vol. 90, Issue 430
DOI: 10.1080/01621459.1995.10476572

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
DOI: 10.1016/j.cub.2005.11.039

Involvement of an Actomyosin Contractile Ring in Saccharomyces cerevisiae Cytokinesis
text, January 1998

N., McMillan, John; Elaine, Yeh,; R., Pringle, John
The University of North Carolina at Chapel Hill University Libraries
DOI: 10.17615/k363-nk57

Nutritional Control of Growth and Development in Yeast
journal, September 2012

Broach, James R.
Genetics, Vol. 192, Issue 1
DOI: 10.1534/genetics.111.135731

Aging and Death in an Organism That Reproduces by Morphologically Symmetric Division
journal, February 2005

Stewart, Eric J.; Madden, Richard; Paul, Gregory
PLoS Biology, Vol. 3, Issue 2
DOI: 10.1371/journal.pbio.0030045

G1 Compartmentalization and Cell Fate Coordination
journal, September 2013

Dalton, Stephen
Cell, Vol. 155, Issue 1
DOI: 10.1016/j.cell.2013.09.015

Checking cell size in yeast
journal, September 2002

Rupeš, Ivan
Trends in Genetics, Vol. 18, Issue 9
DOI: 10.1016/S0168-9525(02)02745-2

Cell-Size Control and Homeostasis in Bacteria
journal, May 2017

Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T.
Current Biology, Vol. 27, Issue 9
DOI: 10.1016/j.cub.2017.04.028

Bayesian Adaptive Sampling for Variable Selection and Model Averaging
journal, January 2011

Clyde, Merlise A.; Ghosh, Joyee; Littman, Michael L.
Journal of Computational and Graphical Statistics, Vol. 20, Issue 1
DOI: 10.1198/jcgs.2010.09049

A Stochastic Model Correctly Predicts Changes in Budding Yeast Cell Cycle Dynamics upon Periodic Expression of CLN2
journal, May 2014

Oguz, Cihan; Palmisano, Alida; Laomettachit, Teeraphan
PLoS ONE, Vol. 9, Issue 5
DOI: 10.1371/journal.pone.0096726

Extensions of the bifurcating autoregressive model for cell lineage studies
journal, December 1999

Huggins, R. M.; Basawa, I. V.
Journal of Applied Probability, Vol. 36, Issue 04
DOI: 10.1017/S002190020001799X

Involvement of an Actomyosin Contractile Ring in Saccharomyces cerevisiae Cytokinesis
journal, September 1998

Bi, Erfei; Maddox, Paul; Lew, Daniel J.
The Journal of Cell Biology, Vol. 142, Issue 5
DOI: 10.1083/jcb.142.5.1301

Applications and implications of the exponentially modified gamma distribution as a model for time variabilities related to cell proliferation and gene expression
journal, March 2016

Golubev, A.
Journal of Theoretical Biology, Vol. 393
DOI: 10.1016/j.jtbi.2015.12.027

The yeast Cln3 protein is an unstable activator of Cdc28.
journal, June 1993

Cross, F. R.; Blake, C. M.
Molecular and Cellular Biology, Vol. 13, Issue 6
DOI: 10.1128/MCB.13.6.3266

A single-cell pedigree analysis of alternative stochastic lymphocyte fates
journal, July 2009

Hawkins, E. D.; Markham, J. F.; McGuinness, L. P.
Proceedings of the National Academy of Sciences, Vol. 106, Issue 32
DOI: 10.1073/pnas.0905629106

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
DOI: 10.1038/nature14908

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
DOI: 10.1016/j.cub.2015.11.067

Cell-size maintenance: universal strategy revealed
text, January 2015

Jun, Suckjoon; Taheri-Araghi, Sattar
arXiv
DOI: 10.48550/arxiv.1504.00043

Cell-Size Control and Homeostasis in Bacteria
journal, February 2015

Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T.
Current Biology, Vol. 25, Issue 3
DOI: 10.1016/j.cub.2014.12.009

The critical size is set at a single-cell level by growth rate to attain homeostasis and adaptation
journal, January 2012

Ferrezuelo, Francisco; Colomina, Neus; Palmisano, Alida
Nature Communications, Vol. 3, Issue 1
DOI: 10.1038/ncomms2015

On being the right (cell) size
journal, May 2015

Ginzberg, M. B.; Kafri, R.; Kirschner, M.
Science, Vol. 348, Issue 6236
DOI: 10.1126/science.1245075

Bayes Factors
journal, June 1995

Kass, Robert E.; Raftery, Adrian E.
Journal of the American Statistical Association, Vol. 90, Issue 430
DOI: 10.2307/2291091

An Outline of the Pattern of Bacterial Generation Times
journal, April 1958

Powell, E. O.
Journal of General Microbiology, Vol. 18, Issue 2
DOI: 10.1099/00221287-18-2-382

Saccharomyces cerevisiae cell cycle.
journal, January 1974

Hartwell, L. H.
Bacteriological Reviews, Vol. 38, Issue 2
DOI: 10.1128/MMBR.38.2.164-198.1974

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
DOI: 10.1016/0014-4827(77)90154-9

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
DOI: 10.1101/gad.1777309

Bayes factors
journal, November 2006

O'Hagan, Tony
Significance, Vol. 3, Issue 4
DOI: 10.1111/j.1740-9713.2006.00204.x

Principles of multilevel modelling
journal, February 2000

Greenland, Sander
International Journal of Epidemiology, Vol. 29, Issue 1
DOI: 10.1093/ije/29.1.158

The Cell-Cycle State of Stem Cells Determines Cell Fate Propensity
journal, March 2014

Pauklin, Siim; Vallier, Ludovic
Cell, Vol. 156, Issue 6
DOI: 10.1016/j.cell.2014.02.044

The Cell-Cycle State of Stem Cells Determines Cell Fate Propensity
journal, September 2013

Pauklin, Siim; Vallier, Ludovic
Cell, Vol. 155, Issue 1
DOI: 10.1016/j.cell.2013.08.031

Extensions of the bifurcating autoregressive model for cell lineage studies
journal, December 1999

Huggins, R. M.; Basawa, I. V.
Journal of Applied Probability, Vol. 36, Issue 4
DOI: 10.1239/jap/1032374768

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
DOI: 10.1073/pnas.0809227106

Do Cells Cycle?
journal, April 1973

Smith, J. A.; Martin, L.
Proceedings of the National Academy of Sciences, Vol. 70, Issue 4
DOI: 10.1073/pnas.70.4.1263

Coordination of Growth and Cell Division in the Drosophila Wing
journal, June 1998

Neufeld, Thomas P.; de la Cruz, Aida Flor A.; Johnston, Laura A.
Cell, Vol. 93, Issue 7
DOI: 10.1016/S0092-8674(00)81462-2

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
DOI: 10.1083/jcb.75.2.422

Cell Size Control in Yeast
journal, May 2012

Turner, Jonathan J.; Ewald, Jennifer C.; Skotheim, Jan M.
Current Biology, Vol. 22, Issue 9
DOI: 10.1016/j.cub.2012.02.041

Cell-size maintenance: universal strategy revealed
journal, January 2015

Jun, Suckjoon; Taheri-Araghi, Sattar
Trends in Microbiology, Vol. 23, Issue 1
DOI: 10.1016/j.tim.2014.12.001

Bayesian Data Analysis
book, November 2013

Gelman, Andrew; Carlin, John B.; Stern, Hal S.
DOI: 10.1201/b16018

Mathematical Contributions to the Theory of Evolution. III. Regression, Heredity, and Panmixia
journal, January 1896

Pearson, K.
Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 187, Issue 0
DOI: 10.1098/rsta.1896.0007

Yeast Vacuole Inheritance and Dynamics
journal, December 2003

Weisman, Lois S.
Annual Review of Genetics, Vol. 37, Issue 1
DOI: 10.1146/annurev.genet.37.050203.103207

The yeast Cln3 protein is an unstable activator of Cdc28
journal, June 1993

Cross, F. R.; Blake, C. M.
Molecular and Cellular Biology, Vol. 13, Issue 6
DOI: 10.1128/mcb.13.6.3266-3271.1993

A Constant Size Extension Drives Bacterial Cell Size Homeostasis
journal, December 2014

Campos, Manuel; Surovtsev, Ivan V.; Kato, Setsu
Cell, Vol. 159, Issue 6
DOI: 10.1016/j.cell.2014.11.022

Derivation and experimental comparison of cell-division probability densities
journal, October 2014

Leander, R.; Allen, E. J.; Garbett, S. P.
Journal of Theoretical Biology, Vol. 359
DOI: 10.1016/j.jtbi.2014.06.004

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
DOI: 10.1038/nature06072

The Bifurcating Autoregression Model in Cell Lineage Studies
journal, December 1986

Cowan, Richard; Staudte, Robert
Biometrics, Vol. 42, Issue 4
DOI: 10.2307/2530692

Stretched cell cycle model for proliferating lymphocytes
journal, April 2014

Dowling, M. R.; Kan, A.; Heinzel, S.
Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
DOI: 10.1073/pnas.1322420111

Natural inheritance. By Francis Galton.
book, January 1889

Galton, Francis
London, Macmillan
DOI: 10.5962/bhl.title.32181

Variability in individual cell cycles of Saccharomyces cerevisiae
journal, August 1981

Lord, P. G.; Wheals, A. E.
Journal of Cell Science, Vol. 50, Issue 1
DOI: 10.1242/jcs.50.1.361

Precocious S-Phase Entry in Budding Yeast Prolongs Replicative State and Increases Dependence Upon Rad53 for Viability
journal, January 2002

Sidorova, Julia M.; Breeden, Linda L.
Genetics, Vol. 160, Issue 1
DOI: 10.1093/genetics/160.1.123

Works referencing / citing this record:

Details Matter: Noise and Model Structure Set the Relationship between Cell Size and Cell Cycle Timing
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Barber, Felix; Ho, Po-Yi; Murray, Andrew W.
Frontiers in Cell and Developmental Biology, Vol. 5
DOI: 10.3389/fcell.2017.00092

Multiple inputs ensure yeast cell size homeostasis during cell cycle progression
journal, July 2018

Garmendia-Torres, Cecilia; Tassy, Olivier; Matifas, Audrey
eLife, Vol. 7
DOI: 10.7554/elife.34025

Multiple inputs ensure yeast cell size homeostasis during cell cycle progression
posted_content, January 2018

Garmendia-Torres, Cecilia; Tassy, Olivier; Matifas, Audrey
DOI: 10.1101/226803

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Supplementary Text from Characterization of dependencies between growth and division in budding yeast
text, January 2017

Mayhew, Michael B.; Iversen, Edwin S.; Hartemink, Alexander J.
The Royal Society
DOI: 10.6084/m9.figshare.4680811
This text is a supplement to the current record

Supplementary material from "Characterization of dependencies between growth and division in budding yeast"
dataset, February 2017

Mayhew, Michael; Iversen, Edwin; Hartemink, Alexander
figshare-Supplementary information for journal article at DOI: 10.1098/rsif.2016.0993, 1 PDF file (1.5 MB)
DOI: 10.6084/m9.figshare.c.3700066.v1
This dataset is a supplement to the current record

Supplementary Text from Characterization of dependencies between growth and division in budding yeast
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DOI: 10.6084/m9.figshare.4680811.v1
This text is a supplement to the current record

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DOI: 10.6084/m9.figshare.c.3700066
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Title: Characterization of dependencies between growth and division in budding yeast

Abstract

Citation Formats

Bayes Factors journal, June 1995

Swe1p Responds to Cytoskeletal Perturbation, Not Bud Size, in S. cerevisiae journal, December 2005

Involvement of an Actomyosin Contractile Ring in Saccharomyces cerevisiae Cytokinesis text, January 1998

Nutritional Control of Growth and Development in Yeast journal, September 2012

Aging and Death in an Organism That Reproduces by Morphologically Symmetric Division journal, February 2005

G1 Compartmentalization and Cell Fate Coordination journal, September 2013

Checking cell size in yeast journal, September 2002

Cell-Size Control and Homeostasis in Bacteria journal, May 2017

Bayesian Adaptive Sampling for Variable Selection and Model Averaging journal, January 2011

A Stochastic Model Correctly Predicts Changes in Budding Yeast Cell Cycle Dynamics upon Periodic Expression of CLN2 journal, May 2014

Extensions of the bifurcating autoregressive model for cell lineage studies journal, December 1999

Involvement of an Actomyosin Contractile Ring in Saccharomyces cerevisiae Cytokinesis journal, September 1998

Applications and implications of the exponentially modified gamma distribution as a model for time variabilities related to cell proliferation and gene expression journal, March 2016

The yeast Cln3 protein is an unstable activator of Cdc28. journal, June 1993

A single-cell pedigree analysis of alternative stochastic lymphocyte fates journal, July 2009

Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size journal, September 2015

Single-Cell Analysis of Growth in Budding Yeast and Bacteria Reveals a Common Size Regulation Strategy journal, February 2016

Cell-size maintenance: universal strategy revealed text, January 2015

Cell-Size Control and Homeostasis in Bacteria journal, February 2015

The critical size is set at a single-cell level by growth rate to attain homeostasis and adaptation journal, January 2012

On being the right (cell) size journal, May 2015

Bayes Factors journal, June 1995

An Outline of the Pattern of Bacterial Generation Times journal, April 1958

Saccharomyces cerevisiae cell cycle. journal, January 1974

Coordination of growth with cell division in the yeast journal, March 1977

The rate of cell growth is governed by cell cycle stage journal, June 2009

Bayes factors journal, November 2006

Principles of multilevel modelling journal, February 2000

The Cell-Cycle State of Stem Cells Determines Cell Fate Propensity journal, March 2014

The Cell-Cycle State of Stem Cells Determines Cell Fate Propensity journal, September 2013

Extensions of the bifurcating autoregressive model for cell lineage studies journal, December 1999

Forced periodic expression of G1 cyclins phase-locks the budding yeast cell cycle journal, April 2009

Do Cells Cycle? journal, April 1973

Coordination of Growth and Cell Division in the Drosophila Wing journal, June 1998

Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division journal, November 1977

Cell Size Control in Yeast journal, May 2012

Cell-size maintenance: universal strategy revealed journal, January 2015

Bayesian Data Analysis book, November 2013

Mathematical Contributions to the Theory of Evolution. III. Regression, Heredity, and Panmixia journal, January 1896

Yeast Vacuole Inheritance and Dynamics journal, December 2003

The yeast Cln3 protein is an unstable activator of Cdc28 journal, June 1993

A Constant Size Extension Drives Bacterial Cell Size Homeostasis journal, December 2014

Derivation and experimental comparison of cell-division probability densities journal, October 2014

The effects of molecular noise and size control on variability in the budding yeast cell cycle journal, August 2007

The Bifurcating Autoregression Model in Cell Lineage Studies journal, December 1986

Stretched cell cycle model for proliferating lymphocytes journal, April 2014

Natural inheritance. By Francis Galton. book, January 1889

Variability in individual cell cycles of Saccharomyces cerevisiae journal, August 1981

Precocious S-Phase Entry in Budding Yeast Prolongs Replicative State and Increases Dependence Upon Rad53 for Viability journal, January 2002

Details Matter: Noise and Model Structure Set the Relationship between Cell Size and Cell Cycle Timing journal, November 2017

Multiple inputs ensure yeast cell size homeostasis during cell cycle progression journal, July 2018

Multiple inputs ensure yeast cell size homeostasis during cell cycle progression posted_content, January 2018

Bayes Factors
journal, June 1995

Swe1p Responds to Cytoskeletal Perturbation, Not Bud Size, in S. cerevisiae
journal, December 2005

Involvement of an Actomyosin Contractile Ring in Saccharomyces cerevisiae Cytokinesis
text, January 1998

Nutritional Control of Growth and Development in Yeast
journal, September 2012

Aging and Death in an Organism That Reproduces by Morphologically Symmetric Division
journal, February 2005

G1 Compartmentalization and Cell Fate Coordination
journal, September 2013

Checking cell size in yeast
journal, September 2002

Cell-Size Control and Homeostasis in Bacteria
journal, May 2017

Bayesian Adaptive Sampling for Variable Selection and Model Averaging
journal, January 2011

A Stochastic Model Correctly Predicts Changes in Budding Yeast Cell Cycle Dynamics upon Periodic Expression of CLN2
journal, May 2014

Extensions of the bifurcating autoregressive model for cell lineage studies
journal, December 1999

Involvement of an Actomyosin Contractile Ring in Saccharomyces cerevisiae Cytokinesis
journal, September 1998

Applications and implications of the exponentially modified gamma distribution as a model for time variabilities related to cell proliferation and gene expression
journal, March 2016

The yeast Cln3 protein is an unstable activator of Cdc28.
journal, June 1993

A single-cell pedigree analysis of alternative stochastic lymphocyte fates
journal, July 2009

Dilution of the cell cycle inhibitor Whi5 controls budding-yeast cell size
journal, September 2015

Single-Cell Analysis of Growth in Budding Yeast and Bacteria Reveals a Common Size Regulation Strategy
journal, February 2016

Cell-size maintenance: universal strategy revealed
text, January 2015

Cell-Size Control and Homeostasis in Bacteria
journal, February 2015

The critical size is set at a single-cell level by growth rate to attain homeostasis and adaptation
journal, January 2012

On being the right (cell) size
journal, May 2015

Bayes Factors
journal, June 1995

An Outline of the Pattern of Bacterial Generation Times
journal, April 1958

Saccharomyces cerevisiae cell cycle.
journal, January 1974

Coordination of growth with cell division in the yeast
journal, March 1977

The rate of cell growth is governed by cell cycle stage
journal, June 2009

Bayes factors
journal, November 2006

Principles of multilevel modelling
journal, February 2000

The Cell-Cycle State of Stem Cells Determines Cell Fate Propensity
journal, March 2014

The Cell-Cycle State of Stem Cells Determines Cell Fate Propensity
journal, September 2013

Extensions of the bifurcating autoregressive model for cell lineage studies
journal, December 1999

Forced periodic expression of G1 cyclins phase-locks the budding yeast cell cycle
journal, April 2009

Do Cells Cycle?
journal, April 1973

Coordination of Growth and Cell Division in the Drosophila Wing
journal, June 1998

Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division
journal, November 1977

Cell Size Control in Yeast
journal, May 2012

Cell-size maintenance: universal strategy revealed
journal, January 2015

Bayesian Data Analysis
book, November 2013

Mathematical Contributions to the Theory of Evolution. III. Regression, Heredity, and Panmixia
journal, January 1896

Yeast Vacuole Inheritance and Dynamics
journal, December 2003

The yeast Cln3 protein is an unstable activator of Cdc28
journal, June 1993

A Constant Size Extension Drives Bacterial Cell Size Homeostasis
journal, December 2014

Derivation and experimental comparison of cell-division probability densities
journal, October 2014

The effects of molecular noise and size control on variability in the budding yeast cell cycle
journal, August 2007

The Bifurcating Autoregression Model in Cell Lineage Studies
journal, December 1986

Stretched cell cycle model for proliferating lymphocytes
journal, April 2014

Natural inheritance. By Francis Galton.
book, January 1889

Variability in individual cell cycles of Saccharomyces cerevisiae
journal, August 1981

Precocious S-Phase Entry in Budding Yeast Prolongs Replicative State and Increases Dependence Upon Rad53 for Viability
journal, January 2002

Details Matter: Noise and Model Structure Set the Relationship between Cell Size and Cell Cycle Timing
journal, November 2017

Multiple inputs ensure yeast cell size homeostasis during cell cycle progression
journal, July 2018

Multiple inputs ensure yeast cell size homeostasis during cell cycle progression
posted_content, January 2018