Modelling how plant cell-cycle progression leads to cell size regulation.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 06 03 2023
accepted: 07 09 2023
revised: 16 11 2023
medline: 20 11 2023
pubmed: 20 10 2023
entrez: 20 10 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 37862377
doi: 10.1371/journal.pcbi.1011503
pii: PCOMPBIOL-D-23-00356
pmc: PMC10653611
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011503

Informations de copyright

Copyright: © 2023 Williamson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Daniel Williamson (D)

Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham, United Kingdom.

William Tasker-Brown (W)

Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, United Kingdom.

James A H Murray (JAH)

Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, United Kingdom.

Angharad R Jones (AR)

Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, United Kingdom.

Leah R Band (LR)

Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham, United Kingdom.
Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, United Kingdom.

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