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Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size.

ABSTRACT: Mean cell size at division is generally constant for specific conditions and cell types, but the mechanisms coupling cell growth and cell cycle control with cell size regulation are poorly understood in intact tissues. Here we show that the continuously dividing fields of cells within the shoot apical meristem of Arabidopsis show dynamic regulation of mean cell size dependent on developmental stage, genotype and environmental signals. We show cell size at division and cell cycle length is effectively predicted using a two-stage cell cycle model linking cell growth and two sequential cyclin dependent kinase (CDK) activities, and experimental results concur in showing that progression through both G1/S and G2/M is size dependent. This work shows that cell-autonomous co-ordination of cell growth and cell division previously observed in unicellular organisms also exists in intact plant tissues, and that cell size may be an emergent rather than directly determined property of cells.

SUBMITTER: R Jones A

PROVIDER: S-EPMC5414177 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size.

R Jones Angharad A Forero-Vargas Manuel M Withers Simon P SP Smith Richard S RS Traas Jan J Dewitte Walter W Murray James A H JAH

Nature communications 20170427

Mean cell size at division is generally constant for specific conditions and cell types, but the mechanisms coupling cell growth and cell cycle control with cell size regulation are poorly understood in intact tissues. Here we show that the continuously dividing fields of cells within the shoot apical meristem of Arabidopsis show dynamic regulation of mean cell size dependent on developmental stage, genotype and environmental signals. We show cell size at division and cell cycle length is effect ...[more]

PMID: 28447614

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Project description:Populations of cells typically maintain a consistent size, despite cell division rarely being precisely symmetrical. Therefore, cells must possess a mechanism of "size control", whereby the cell volume at birth affects cell-cycle progression. While size control mechanisms have been elucidated in a number of other organisms, it is not yet clear how this mechanism functions in plants. Here, we present a mathematical model of the key interactions in the plant cell cycle. Model simulations reveal that the network of interactions exhibits limit-cycle solutions, with biological switches underpinning both the G1/S and G2/M cell-cycle transitions. Embedding this network model within growing cells, we test hypotheses as to how cell-cycle progression can depend on cell size. We investigate two different mechanisms at both the G1/S and G2/M transitions: (i) differential expression of cell-cycle activator and inhibitor proteins (with synthesis of inhibitor proteins being independent of cell size), and (ii) equal inheritance of inhibitor proteins after cell division. The model demonstrates that both these mechanisms can lead to larger daughter cells progressing through the cell cycle more rapidly, and can thus contribute to cell-size control. To test how these features enable size homeostasis over multiple generations, we then simulated these mechanisms in a cell-population model with multiple rounds of cell division. These simulations suggested that integration of size-control mechanisms at both G1/S and G2/M provides long-term cell-size homeostasis. We concluded that while both size independence and equal inheritance of inhibitor proteins can reduce variations in cell size across individual cell-cycle phases, combining size-control mechanisms at both G1/S and G2/M is essential to maintain size homeostasis over multiple generations. Thus, our study reveals how features of the cell-cycle network enable cell-cycle progression to depend on cell size, and provides a mechanistic understanding of how plant cell populations maintain consistent size over generations.

Dataset Information

Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size.

Publications

Cell-size dependent progression of the cell cycle creates homeostasis and flexibility of plant cell size.

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