A systems biology approach for the analysis of carbohydrate dynamics during acclimation to low temperature in Arabidopsis thaliana.

Low temperature is an important environmental factor affecting the performance and distribution of plants. During the so-called process of cold acclimation, many plants are able to develop low-temperature tolerance, associated with the reprogramming of a large part of their metabolism. In this study, we present a systems biology approach based on mathematical modelling to determine interactions between the reprogramming of central carbohydrate metabolism and the development of freezing tolerance in two accessions of Arabidopsis thaliana. Different regulation strategies were observed for (a) photosynthesis, (b) soluble carbohydrate metabolism and (c) enzyme activities of central metabolite interconversions. Metabolism of the storage compound starch was found to be independent of accession-specific reprogramming of soluble sugar metabolism in the cold. Mathematical modelling and simulation of cold-induced metabolic reprogramming indicated major differences in the rates of interconversion between the pools of hexoses and sucrose, as well as the rate of assimilate export to sink organs. A comprehensive overview of interconversion rates is presented, from which accession-specific regulation strategies during exposure to low temperature can be derived. We propose this concept as a tool for predicting metabolic engineering strategies to optimize plant freezing tolerance. We confirm that a significant improvement in freezing tolerance in plants involves multiple regulatory instances in sucrose metabolism, and provide evidence for a pivotal role of sucrose-hexose interconversion in increasing the cold acclimation output.