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A compact model for cold tolerance entrainment based on the ICE1-CBF-COR pathway in plants

Huang, T.; Wu, Y.; Lv, H.; Shu, Y.; Yu, L.; Yang, H.; Hou, X.; You, X.

2023-02-24 systems biology
10.1101/2023.02.23.529825 bioRxiv
Show abstract

Most temperate plants can tolerate both chilling and freezing temperatures. Plants have developed self-defense mechanisms to perceive cold signal, trigger the cold tolerance for the cold response ICE1-CBF-COR pathway by packing a cascade of kinase phosphorylation/dephosphorylation events into a functional module. Linked to the central ICE1-CBF-COR model, two sub-models were adopted for the second messenSger Ca2+ -- a one-compartment model for Ca2+ transient and a two-compartment model for a train of Ca2+ spikes. Numerical simulation verified the expression patterns of the cold-induced genes as observed in Arabidopsis thaliana, Brassica napa and Solanum lycopersicum, including wild types and mutants. Moreover, the desensitization and resensitization of CBF3 and COR15A were displayed as well as the dynamics in the gradually decreasing temperature response to cold stress. The duration of cold tolerance was predicted for approximate 10 days. Interpreting and predicting the dynamical behaviors of the cold signaling pathway are valuable and time-saving for understanding mechanisms of cold acclimation. Author summaryIn higher organisms, CBF3 transcriptional level are output in a pulse and COR15A transcriptional level are maintained at a high homeostatic level to respond cold stress, which is determined by a complex set of regulatory mechanisms. Feedback loops from Ca2+ perception onto CaM, kinases, cold-acclimated genes in sequence, which have been experimentally reported, are thought to induce COR15A transcript accumulation under cold temperature exposure. The cold response pathway has been modeled based on a computational model. However, protein kinase cascades made the model relatively complicated and the cold-response gene COR15A was absent. Here, we develop a compact model with cold tolerance target gene COR15A. We show that this model could reproduce the temporal dynamics and characteristics of the core gene variables in different plants with wild type and mutant. Reduction of CaM proportion and augment of negative feedback control by ZAT12 in the model results in the desensitization of CBF3 and COR15A. Less than 24-hr warm treatment loses the ability of resensitization of CBF3 and COR15A after 14-day cold exposure. We further predict that the duration of cold tolerance is maintained at about 10 days in our model.

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