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

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 n...

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Autores principales: Williamson, Daniel, Tasker-Brown, William, Murray, James A. H., Jones, Angharad R., Band, Leah R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10653611/
https://www.ncbi.nlm.nih.gov/pubmed/37862377
http://dx.doi.org/10.1371/journal.pcbi.1011503
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author Williamson, Daniel
Tasker-Brown, William
Murray, James A. H.
Jones, Angharad R.
Band, Leah R.
author_facet Williamson, Daniel
Tasker-Brown, William
Murray, James A. H.
Jones, Angharad R.
Band, Leah R.
author_sort Williamson, Daniel
collection PubMed
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.
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spelling pubmed-106536112023-10-20 Modelling how plant cell-cycle progression leads to cell size regulation Williamson, Daniel Tasker-Brown, William Murray, James A. H. Jones, Angharad R. Band, Leah R. PLoS Comput Biol Research Article 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. Public Library of Science 2023-10-20 /pmc/articles/PMC10653611/ /pubmed/37862377 http://dx.doi.org/10.1371/journal.pcbi.1011503 Text en © 2023 Williamson et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Williamson, Daniel
Tasker-Brown, William
Murray, James A. H.
Jones, Angharad R.
Band, Leah R.
Modelling how plant cell-cycle progression leads to cell size regulation
title Modelling how plant cell-cycle progression leads to cell size regulation
title_full Modelling how plant cell-cycle progression leads to cell size regulation
title_fullStr Modelling how plant cell-cycle progression leads to cell size regulation
title_full_unstemmed Modelling how plant cell-cycle progression leads to cell size regulation
title_short Modelling how plant cell-cycle progression leads to cell size regulation
title_sort modelling how plant cell-cycle progression leads to cell size regulation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10653611/
https://www.ncbi.nlm.nih.gov/pubmed/37862377
http://dx.doi.org/10.1371/journal.pcbi.1011503
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