Limitation of sucrose biosynthesis shapes carbon partitioning during plant cold acclimation

Cold acclimation is a multigenic process by which many plant species increase their freezing tolerance. Stabilization of photosynthesis and carbohydrate metabolism plays a crucial role in cold acclimation. To study regulation of primary and secondary metabolism during cold acclimation of Arabidopsis thaliana, metabolic mutants with deficiencies in either starch or flavonoid metabolism were exposed to 4 degrees C. Photosynthesis was determined together with amounts of carbohydrates, anthocyanins, organic acids and enzyme activities of the central carbohydrate metabolism. Starch deficiency was found to significantly delay soluble sugar accumulation during cold acclimation, while starch overaccumulation did not affect accumulation dynamics but resulted in lower total amounts of \sucrose and glucose. Anthocyanin amounts were lowered in both starch deficient and overaccumulating mutants. Vice versa, flavonoid deficiency did not result in a changed starch amount, which suggested a unidirectional signalling link between starch and flavonoid metabolism. Mathematical modelling of carbon metabolism indicated kinetics of sucrose biosynthesis to be limiting for carbon partitioning in leaf tissue during cold exposure. Together with cold-induced dynamics of citrate, fumarate and malate amounts, this provided evidence for a central role of sucrose phosphate synthase activity in carbon partitioning between biosynthetic and dissimilatory pathways which stabilizes photosynthesis and metabolism at low temperature.

Automated summary

Cold acclimation is a complex process involving multiple genes in plants, which helps them increase their tolerance to freezing temperatures. The stabilization of photosynthesis and carbohydrate metabolism is crucial for this process. This study examined the regulation of primary and secondary metabolism in Arabidopsis thaliana during cold acclimation by exposing metabolic mutants with deficiencies in starch or flavonoid metabolism to 4 degrees C. The results showed that starch deficiency delayed the accumulation of soluble sugars during cold acclimation, while starch overaccumulation led to lower total amounts of sucrose and glucose. Additionally, anthocyanin amounts were decreased in both starch-deficient and starch-overaccumulating mutants. Mathematical modelling indicated that sucrose biosynthesis kinetics played a limiting role in carbon partitioning during cold exposure, suggesting the central role of sucrose phosphate synthase activity in stabilizing photosynthesis and metabolism at low temperatures.