Limitation of sucrose biosynthesis shapes carbon partitioning during
plant cold acclimation
Abstract
Cold acclimation is a multigenic process by which many plant species of
the temperate zone increase their freezing tolerance. Stabilization of
photosynthesis and carbohydrate metabolism plays a crucial role in cold
acclimation, and amounts of transient leaf starch, soluble carbohydrates
and secondary metabolites, e.g., flavonoids, show significant
cold-induced dynamics. To study regulation of primary and secondary
metabolite accumulation during cold acclimation of Arabidopsis
thaliana, metabolic mutants with deficiencies in either starch or
flavonoid metabolism were exposed to 4°C over 14 days and sampled before
as well as at early and late time points of cold acclimation.
Photosynthetic activity was determined together with amounts of
carbohydrates, anthocyanins, organic acids and maximum 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, however, 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 metabolism and its
export form source to sink tissue to be limiting for carbon partitioning
in leaf tissue during cold exposure. Together with cold-induced dynamics
of 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.