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

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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; Huang, Kerwyn Casey; Meyerowitz, Elliot M.; Jönsson, Henrik.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 51, 20.12.2016, p. E8238-E8246.

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Willis, Lisa ; Refahi, Yassin ; Wightman, Raymond ; Landrein, Benoit ; Teles, José ; Huang, Kerwyn Casey ; Meyerowitz, Elliot M. ; Jönsson, Henrik. / Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 51. pp. E8238-E8246.

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TY - JOUR

T1 - Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

AU - Willis, Lisa

AU - Refahi, Yassin

AU - Wightman, Raymond

AU - Landrein, Benoit

AU - Teles, José

AU - Huang, Kerwyn Casey

AU - Meyerowitz, Elliot M.

AU - Jönsson, Henrik

PY - 2016/12/20

Y1 - 2016/12/20

N2 - 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.

AB - 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.

KW - Cell cycle

KW - Cell growth

KW - Cell size

KW - Homeostasis

KW - Plant stem cells

UR - http://www.scopus.com/inward/record.url?scp=85006445859&partnerID=8YFLogxK

U2 - 10.1073/pnas.1616768113

DO - 10.1073/pnas.1616768113

M3 - Article

VL - 113

SP - E8238-E8246

JO - Proceedings of the National Academy of Sciences

T2 - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

SN - 1091-6490

IS - 51

ER -