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Feedback inhibition of starch degradation in arabidopsis leaves mediated by trehalose 6-phosphate

  • 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,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 beta-amylase. Nonaqueous fractionation of leaves showed that Tre6P is predominantly located in the cytosol, with estimated in vivo Tre6P concentrations of 4 to 7 mu M in the cytosol, 0.2 to 0.5 mu M in the chloroplasts, and 0.05 mu M 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.show moreshow less

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Author details:Marina Camara Mattos Martins, Mahdi Hejazi, Jörg FettkeORCiDGND, Martin SteupORCiDGND, Regina FeilORCiD, Ursula Krause, Stephanie Arrivault, Daniel Vosloh, Carlos Maria Figueroa, Alexander Ivakov, Umesh Prasad Yadav, Maria Piques, Daniela Metzner, Mark StittORCiDGND, John Edward LunnORCiD
DOI:https://doi.org/10.1104/pp.113.226787
ISSN:0032-0889
ISSN:1532-2548
Title of parent work (English):Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants
Publisher:American Society of Plant Physiologists
Place of publishing:Rockville
Publication type:Article
Language:English
Year of first publication:2013
Publication year:2013
Release date:2017/03/26
Volume:163
Issue:3
Number of pages:22
First page:1142
Last Page:1163
Funding institution:Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior Brazil [BEX2762/07-2]; Deutscher Akademischer Austauschdienst [A/07/70615]; Deutsche Forschungsgemeinschaft [SFB 429]; European Commission [245142]; Max Planck Society
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
Peer review:Referiert
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