School of Mechanical, Aerospace and Automotive Engineering, Coventry University, Coventry, United Kingdom.
Warwick Integrative Synthetic Biology Centre, School of Engineering, University of Warwick, Coventry, United Kingdom.
PLoS Comput Biol. 2020 Mar 16;16(3):e1007671. doi: 10.1371/journal.pcbi.1007671. eCollection 2020 Mar.
The circadian clock orchestrates biological processes so that they occur at specific times of the day, thereby facilitating adaptation to diurnal and seasonal environmental changes. In plants, mathematical modelling has been comprehensively integrated with experimental studies to gain a better mechanistic understanding of the complex genetic regulatory network comprising the clock. However, with an increasing number of circadian genes being discovered, there is a pressing need for methods facilitating the expansion of computational models to incorporate these newly-discovered components. Conventionally, plant clock models have comprised differential equation systems based on Michaelis-Menten kinetics. However, the difficulties associated with modifying interactions using this approach-and the concomitant problem of robustly identifying regulation types-has contributed to a complexity bottleneck, with quantitative fits to experimental data rapidly becoming computationally intractable for models possessing more than ≈50 parameters. Here, we address these issues by constructing the first plant clock models based on the S-System formalism originally developed by Savageau for analysing biochemical networks. We show that despite its relative simplicity, this approach yields clock models with comparable accuracy to the conventional Michaelis-Menten formalism. The S-System formulation also confers several key advantages in terms of model construction and expansion. In particular, it simplifies the inclusion of new interactions, whilst also facilitating the modification of regulation types, thereby making it well-suited to network inference. Furthermore, S-System models mitigate the issue of parameter identifiability. Finally, by applying linear systems theory to the models considered, we provide some justification for the increased use of aggregated protein equations in recent plant clock modelling, replacing the separate cytoplasmic/nuclear protein compartments that were characteristic of the earlier models. We conclude that as well as providing a simplified framework for model development, the S-System formalism also possesses significant potential as a robust modelling method for designing synthetic gene circuits.
生物钟协调生物过程,使其在一天中的特定时间发生,从而促进对昼夜和季节性环境变化的适应。在植物中,数学建模已经与实验研究全面结合,以更好地理解构成生物钟的复杂遗传调控网络的机制。然而,随着越来越多的生物钟基因被发现,迫切需要方法来扩展计算模型,以纳入这些新发现的成分。传统上,植物生物钟模型由基于米氏-门捷列夫动力学的微分方程系统组成。然而,使用这种方法修改相互作用的困难——以及稳健地识别调节类型的问题——导致了一个复杂性瓶颈,对于具有超过 ≈50 个参数的模型,对实验数据的定量拟合很快在计算上变得难以处理。在这里,我们通过构建第一个基于 Savageau 最初为分析生化网络而开发的 S 系统形式主义的植物生物钟模型来解决这些问题。我们表明,尽管它相对简单,但这种方法产生的时钟模型与传统的米氏-门捷列夫形式主义具有相当的准确性。S 系统公式在模型构建和扩展方面也具有几个关键优势。特别是,它简化了新相互作用的纳入,同时也便于调节类型的修改,因此非常适合网络推断。此外,S 系统模型减轻了参数可识别性的问题。最后,通过将线性系统理论应用于所考虑的模型,我们为最近植物生物钟建模中越来越多地使用聚合蛋白方程提供了一些理由,替代了早期模型中细胞质/核蛋白隔室的单独特征。我们的结论是,S 系统形式主义不仅为模型开发提供了简化的框架,而且还具有作为设计合成基因电路的稳健建模方法的巨大潜力。