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Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Willis, Lisa; Refahi, Yassin; Wightman, Raymond; Landrein, Benoit; Teles, José LU ; Huang, Kerwyn Casey; Meyerowitz, Elliot M. and Jönsson, Henrik LU (2016) In Proceedings of the National Academy of Sciences of the United States of America 113(51). p.8238-8246
Abstract

Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3-4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical... (More)

Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3-4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical size. Our data also rule out models in which cells undergo G2/M at a fixed time after birth, or by adding a critical size increment between G2/M transitions. Rather, cell size regulation was intermediate between the critical size and critical increment paradigms, meaning that cell size fluctuations decay by ∼75% in one generation compared with 100% (critical size) and 50% (critical increment). Notably, this behavior was independent of local cell-cell contact topologies and of position within the tissue. Cells grew exponentially throughout the first >80% of the cell cycle, but following an asymmetrical division, the small daughter grew at a faster exponential rate than the large daughter, an observation that potentially challenges present models of growth regulation. These growth and division behaviors place strong constraints on quantitative mechanistic descriptions of the cell cycle and growth control.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Cell cycle, Cell growth, Cell size, Homeostasis, Plant stem cells
in
Proceedings of the National Academy of Sciences of the United States of America
volume
113
issue
51
pages
8238 - 8246
publisher
National Acad Sciences
external identifiers
  • scopus:85006445859
  • wos:000390044900004
ISSN
0027-8424
DOI
10.1073/pnas.1616768113
language
English
LU publication?
yes
id
b150de69-54a8-4bd4-b3ce-ccaa84a267da
date added to LUP
2017-01-11 12:36:40
date last changed
2017-10-01 05:28:36
@article{b150de69-54a8-4bd4-b3ce-ccaa84a267da,
  abstract     = {<p>Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3-4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical size. Our data also rule out models in which cells undergo G2/M at a fixed time after birth, or by adding a critical size increment between G2/M transitions. Rather, cell size regulation was intermediate between the critical size and critical increment paradigms, meaning that cell size fluctuations decay by ∼75% in one generation compared with 100% (critical size) and 50% (critical increment). Notably, this behavior was independent of local cell-cell contact topologies and of position within the tissue. Cells grew exponentially throughout the first &gt;80% of the cell cycle, but following an asymmetrical division, the small daughter grew at a faster exponential rate than the large daughter, an observation that potentially challenges present models of growth regulation. These growth and division behaviors place strong constraints on quantitative mechanistic descriptions of the cell cycle and growth control.</p>},
  author       = {Willis, Lisa and Refahi, Yassin and Wightman, Raymond and Landrein, Benoit and Teles, José and Huang, Kerwyn Casey and Meyerowitz, Elliot M. and Jönsson, Henrik},
  issn         = {0027-8424},
  keyword      = {Cell cycle,Cell growth,Cell size,Homeostasis,Plant stem cells},
  language     = {eng},
  month        = {12},
  number       = {51},
  pages        = {8238--8246},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche},
  url          = {http://dx.doi.org/10.1073/pnas.1616768113},
  volume       = {113},
  year         = {2016},
}