A Computational Model for the Cold Response Pathway in Plants

Understanding the mechanism by which plants respond to cold stress and strengthen their tolerance to low temperatures is an important and challenging task in plant sciences. Experiments have established that the first step in the perception and transduction of the cold stress signal consists of a transient influx of Ca(2+). This Ca(2+) influx triggers the activation of a cascade of phosphorylation-dephosphorylation reactions that eventually affects the expression of C-repeat-binding factors (CBFs, notably CBF3), which were shown in many plants to control resistance to cold stress by regulating the expression of cold-regulated (COR) genes. Based on experimental observations mostly made on Arabidopsis thaliana, we build a computational model for the cold response pathway in plants, from the transduction of the cold signal via the transient influx of Ca(2+) to the activation of the phosphorylation cascade leading to CBF3 expression. We explore the dynamics of this regulatory network by means of numerical simulations and compare the results with experimental observations on the dynamics of the cold response, both for the wild type and for mutants. The simulations show how, in response to cold stress, a brief Ca(2+) influx, which is over in minutes, is transduced along the successive steps of the network to trigger the expression of cold response genes such as CBF3 within hours. Sometimes, instead of a single Ca(2+) spike the decrease in temperature brings about a train of high-frequency Ca(2+) oscillations. The model is applied to both types of Ca(2+) signaling. We determine the dynamics of the network in response to a series of identical cold stresses, to account for the observation of desensitization and resensitization. The analysis of the model predicts the possibility of an oscillatory expression of CBF3 originating from the negative feedback exerted by ZAT12, a factor itself controlled by CBF3. Finally, we extend the model to incorporate the circadian control of CBF3 expression, to account for the gating of the response to cold stress by the plant circadian clock.