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Abstract
Many plants accumulate substantial starch reserves in their leaves during the day and remobilize them at night to provide carbon and energy for maintenance and growth. In this paper, we explore the role of a sugar-signaling metabolite, trehalose-6-phosphate (Tre6P), in regulating the accumulation and turnover of transitory starch in Arabidopsis (Arabidopsis thaliana) leaves. Ethanol-induced overexpression of trehalose-phosphate synthase during the day increased Tre6P levels up to 11-fold. There was a transient increase in the rate of starch accumulation in the middle of the day, but this was not linked to reductive activation of ADP-glucose pyrophosphorylase. A 2- to 3-fold increase in Tre6P during the night led to significant inhibition of starch degradation. Maltose and maltotriose did not accumulate, suggesting that Tre6P affects an early step in the pathway of starch degradation in the chloroplasts. Starch granules isolated from induced plants had a higher orthophosphate content than granules from noninduced control plants, consistent either with disruption of the phosphorylation-dephosphorylation cycle that is essential for efficient starch breakdown or with inhibition of starch hydrolysis by β-amylase. Nonaqueous fractionation of leaves showed that Tre6P is predominantly located in the cytosol, with estimated in vivo Tre6P concentrations of 4 to 7 µm in the cytosol, 0.2 to 0.5 µm in the chloroplasts, and 0.05 µm in the vacuole. It is proposed that Tre6P is a component in a signaling pathway that mediates the feedback regulation of starch breakdown by sucrose, potentially linking starch turnover to demand for sucrose by growing sink organs at night.
Highlights
Many plants accumulate substantial starch reserves in their leaves during the day and remobilize them at night to provide carbon and energy for maintenance and growth
Plants induced by spraying with 2% (v/v) ethanol contained an immunoreactive protein of the expected size (53 kD) of the E. coli otsA (Supplemental Fig. S1)
The subcellular location of the Arabidopsis TPS1 has not yet been experimentally determined, there is circumstantial evidence that it is restricted to the cytosol
Summary
Many plants accumulate substantial starch reserves in their leaves during the day and remobilize them at night to provide carbon and energy for maintenance and growth. From the fluctuations in metabolite levels observed in leaves during the diurnal cycle and in vitro studies of enzyme properties, a model was developed to explain how various regulatory mechanisms are integrated to bring about feed-forward or feedback regulation of Suc synthesis and photoassimilate partitioning (for review, see MacRae and Lunn, 2006). This model considers starch to be an “overflow” product. The circadian clock is potentially involved in this anticipatory response, providing information about the expected length of the coming night so that the plant can set an appropriate rate of starch synthesis (Smith and Stitt, 2007; Stitt et al, 2007; Stitt and Zeeman, 2012)
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