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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/G 2/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/G 2/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 negativemore » 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.« less

Authors:
ORCiD logo [1];  [2];  [2]
  1. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Duke Univ., Durham, NC (United States)
Publication Date:
Research Org.:
Lawrence Livermore National Lab. (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:
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.
Mayhew, Michael B., Iversen, Edwin S., & Hartemink, Alexander J. Characterization of dependencies between growth and division in budding yeast. United States. doi:10.1098/rsif.2016.0993.
Mayhew, Michael B., Iversen, Edwin S., and Hartemink, Alexander J. Wed . "Characterization of dependencies between growth and division in budding yeast". United States. doi:10.1098/rsif.2016.0993. https://www.osti.gov/servlets/purl/1349007.
@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 = {Interface},
number = 127,
volume = 14,
place = {United States},
year = {2017},
month = {2}
}

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