Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham, United Kingdom.
Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, United Kingdom.
PLoS Comput Biol. 2023 Oct 20;19(10):e1011503. doi: 10.1371/journal.pcbi.1011503. eCollection 2023 Oct.
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.
细胞群体通常维持一致的大小,尽管细胞分裂很少精确对称。因此,细胞必须具有“大小控制”机制,即出生时的细胞体积影响细胞周期进程。虽然在其他一些生物体中已经阐明了大小控制机制,但目前尚不清楚该机制在植物中如何发挥作用。在这里,我们提出了一个植物细胞周期关键相互作用的数学模型。模型模拟结果表明,相互作用网络表现出极限环解,生物开关为 G1/S 和 G2/M 细胞周期转变提供了基础。将这个网络模型嵌入到正在生长的细胞中,我们测试了细胞周期进程如何取决于细胞大小的假设。我们在 G1/S 和 G2/M 转变处研究了两种不同的机制:(i)细胞周期激活剂和抑制剂蛋白的差异表达(抑制剂蛋白的合成与细胞大小无关),以及(ii)细胞分裂后抑制剂蛋白的均等遗传。该模型表明,这两种机制都可以导致较大的子细胞更快地通过细胞周期,从而有助于细胞大小控制。为了测试这些特征如何在多代中实现大小稳态,我们然后在具有多轮细胞分裂的细胞群体模型中模拟了这些机制。这些模拟表明,在 G1/S 和 G2/M 处整合大小控制机制可以提供长期的细胞大小稳态。我们得出结论,虽然抑制剂蛋白的大小独立性和均等遗传都可以减少细胞大小在单个细胞周期阶段的变化,但在 G1/S 和 G2/M 处整合大小控制机制对于多代维持大小稳态至关重要。因此,我们的研究揭示了细胞周期网络的特征如何使细胞周期进程取决于细胞大小,并提供了对植物细胞群体如何在多代中维持一致大小的机制理解。