Limitation of sucrose biosynthesis shapes carbon partitioning during plant cold acclimation

Abstract

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.

Plant cold acclimation and its impact on sensitivity of carbohydrate metabolism

“…In this study we present an in-depth analysis of a condensed dynamic model of the core central carbon metabolism of Arabidopsis thaliana leaves. It is a model that has already been used to identify a role of limitations in sucrose synthesis in carbon partitioning during acclimation (Kitashova et al 2022). Since it has been shown that light intensity is of great importance for the cold acclimation process of plants and there are complex interactions between cold and light signaling (Szalai et al 2018), a dynamic sensitivity analysis was defined, and new experiments were performed to assess its applicability.…”

Natural variation of temperature acclimation of Arabidopsis thaliana

“…Starch and soluble sugars were extracted and determined as described before (Kitashova et al, 2023). In brief, approx.…”

“…Enzyme activities of the central carbohydrate metabolism were quantified photometrically as described before with slight modifications (Kitashova et al, 2023). All enzymes were quantified from the same extract, which consisted of 50 mM HEPES-KOH (pH 7.5), 5 mM MgCl 2 , 2 mM EDTA, 1 mM DTT, 1% (v/v) glycerol, 0.1% (v/v) Triton, and protease inhibitor cocktail for plant cell and tissue extracts in DMSO solution (Sigma-Aldrich ® ).…”

“…When exposed to low temperatures, sucrose metabolism was observed to play a key role in stabilizing photosynthetic efficiency, CO 2 fixation and carbon allocation (Kitashova et al, 2023). It was previously shown that carbon uptake in a low‐temperature regime is limited by the capacity to synthesize sucrose (Strand et al, 2003).…”

A Regulatory Mechanism on Pathways: Modulating Roles of MYC2 and BBX21 in the Flavonoid Network

“…Anthocyanins generated from the pathway are part of flavonoids synthesized in plants, which include also proanthocyanidins, flavonols, flavones, aurones, and others from different branches of the flavonoid network. In Arabidopsis thaliana [ 1 ], transiently enhanced accumulation of the anthocyanin pigments is regularly seen in seedlings between day three and day six after seed germination under normal physiological conditions, and the phenotype can also be induced under adverse conditions [ 2 ]. The transient pigmentation of leaf and stem, commonly observed in other species [ 3 , 4 , 5 ] as well, is considered beneficial to plants for protection against stressful environments [ 6 , 7 ].…”