Limitation of sucrose biosynthesis shapes carbon partitioning during plant cold acclimation

• Published in: Plant, cell and environment cell and environment, 2023-02, Vol.46 (2), p.464-478
• Main Authors: Kitashova, Anastasia, Adler, Stephan O., Richter, Andreas S., Eberlein, Svenja, Dziubek, Dejan, Klipp, Edda, Nägele, Thomas
• Format: Article
• Language: English
• Subjects: Acclimation; Acclimatization; Acclimatization - physiology; Accumulation; Anthocyanins; Anthocyanins - metabolism; Arabidopsis - metabolism; Arabidopsis thaliana; Biosynthesis; Carbohydrate Metabolism; Carbohydrates; Carbon; Carbon - metabolism; Cold; Cold acclimation; Cold Temperature; Cold tolerance; Enzymatic activity; Flavonoids; Freezing; kinetic modelling; Low temperature; Mathematical models; Metabolism; Mutants; Organic acids; Partitioning; Photosynthesis; Plant Leaves - metabolism; Plant species; Plant tissues; Plants (botany); Plants - metabolism; Signal transduction; Starch; Starch - metabolism; Sucrose; Sucrose - metabolism; Sucrose phosphate synthase
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14483

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°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. Summary Statement Regulation at the interface of plant primary and secondary metabolism during cold acclimation was analysed by kinetic modelling. Our findings suggest that cold‐induced limitation of sucrose biosynthesis regulates substrate availability for the coordinated accumulation of starch and anthocyanins.