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 an...

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Veröffentlicht in:Plant physiology (Bethesda) 2013-11, Vol.163 (3), p.1142-1163
Hauptverfasser: Martins, Marina Camara Mattos, Hejazi, Mahdi, Fettke, Joerg, Steup, Martin, Feil, Regina, Krause, Ursula, Arrivault, Stéphanie, Vosloh, Daniel, Figueroa, Carlos María, Ivakov, Alexander, Yadav, Umesh Prasad, Piques, Maria, Metzner, Daniela, Stitt, Mark, Lunn, John Edward
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container_issue 3
container_start_page 1142
container_title Plant physiology (Bethesda)
container_volume 163
creator Martins, Marina Camara Mattos
Hejazi, Mahdi
Fettke, Joerg
Steup, Martin
Feil, Regina
Krause, Ursula
Arrivault, Stéphanie
Vosloh, Daniel
Figueroa, Carlos María
Ivakov, Alexander
Yadav, Umesh Prasad
Piques, Maria
Metzner, Daniela
Stitt, Mark
Lunn, John Edward
description 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.
doi_str_mv 10.1104/pp.113.226787
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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. 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Psychology ; Glucosyltransferases - metabolism ; Hydrolysis - drug effects ; Immunoblotting ; Leaves ; Maltose - metabolism ; Microscopy, Electron, Scanning ; Phosphates ; Phosphates - metabolism ; Phosphorylation ; Plant Leaves - drug effects ; Plant Leaves - metabolism ; Plant physiology and development ; Plants ; Plants, Genetically Modified ; starch ; Starch - metabolism ; Starch - ultrastructure ; Starches ; sucrose ; Sugar Phosphates - metabolism ; Time Factors ; trehalose ; Trehalose - analogs &amp; derivatives ; Trehalose - metabolism ; Trisaccharides - metabolism</subject><ispartof>Plant physiology (Bethesda), 2013-11, Vol.163 (3), p.1142-1163</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2014 INIST-CNRS</rights><rights>2013 American Society of Plant Biologists. 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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.</description><subject>Arabidopsis</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>BIOCHEMISTRY AND METABOLISM</subject><subject>Biological and medical sciences</subject><subject>Chloroplasts</subject><subject>Chloroplasts - metabolism</subject><subject>Crop harvesting</subject><subject>Cytoplasmic Granules - metabolism</subject><subject>Cytoplasmic Granules - ultrastructure</subject><subject>Cytosol</subject><subject>Cytosol - metabolism</subject><subject>Enzymes</subject><subject>Ethanol</subject><subject>Ethanol - pharmacology</subject><subject>Feedback, Physiological - physiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Glucosyltransferases - metabolism</subject><subject>Hydrolysis - drug effects</subject><subject>Immunoblotting</subject><subject>Leaves</subject><subject>Maltose - metabolism</subject><subject>Microscopy, Electron, Scanning</subject><subject>Phosphates</subject><subject>Phosphates - metabolism</subject><subject>Phosphorylation</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - metabolism</subject><subject>Plant physiology and development</subject><subject>Plants</subject><subject>Plants, Genetically Modified</subject><subject>starch</subject><subject>Starch - metabolism</subject><subject>Starch - ultrastructure</subject><subject>Starches</subject><subject>sucrose</subject><subject>Sugar Phosphates - metabolism</subject><subject>Time Factors</subject><subject>trehalose</subject><subject>Trehalose - analogs &amp; derivatives</subject><subject>Trehalose - metabolism</subject><subject>Trisaccharides - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1rFTEUxYMo9lldulSyEdxMzfdkNkKpthaeKFjX4eZjOqnzJtNkXqH_vWnfs9WVqxPu-XG4Nweh15QcUUrEh3muyo8YU61un6AVlZw1TAr9FK0IqW-idXeAXpRyRQihnIrn6IAJIrgQYoXgNARvwf3C59MQbVximnDq8Y8Fshvwp3CZwcP9NE74OIONPs0lFrwOcBMK_hp8hCV4bG_xRQ4DjKkErJrvQyrzUJ2X6FkPYwmv9nqIfp5-vjj50qy_nZ2fHK8bJ7leGquC7xVjraKgNAfWB0aIY0JZrpiwtpWKEu06qaTspGup1sxx65T3tleCH6KPu9x5azfBuzAtGUYz57iBfGsSRPOvM8XBXKYbwzXlSpAa8H4fkNP1NpTFbGJxYRxhCmlbDLv7P6Jb2v0XpUJoRloqZEWbHepyKiWH_mEjSsxdg2aeq3Kza7Dyb_8-44H-U1kF3u0BKA7GPsPkYnnk2o4KLlnl3uy4q7Kk_Ohz2WlFNf8NmYOs8w</recordid><startdate>20131101</startdate><enddate>20131101</enddate><creator>Martins, Marina Camara Mattos</creator><creator>Hejazi, Mahdi</creator><creator>Fettke, Joerg</creator><creator>Steup, Martin</creator><creator>Feil, Regina</creator><creator>Krause, Ursula</creator><creator>Arrivault, Stéphanie</creator><creator>Vosloh, Daniel</creator><creator>Figueroa, Carlos María</creator><creator>Ivakov, Alexander</creator><creator>Yadav, Umesh Prasad</creator><creator>Piques, Maria</creator><creator>Metzner, Daniela</creator><creator>Stitt, Mark</creator><creator>Lunn, John Edward</creator><general>American Society of Plant Biologists</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20131101</creationdate><title>Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate</title><author>Martins, Marina Camara Mattos ; Hejazi, Mahdi ; Fettke, Joerg ; Steup, Martin ; Feil, Regina ; Krause, Ursula ; Arrivault, Stéphanie ; Vosloh, Daniel ; Figueroa, Carlos María ; Ivakov, Alexander ; Yadav, Umesh Prasad ; Piques, Maria ; Metzner, Daniela ; Stitt, Mark ; Lunn, John Edward</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c538t-b6edf622761a683a2fe200c246b3624bb756108c9565595c71882c3bc6ddbf643</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BIOCHEMISTRY AND METABOLISM</topic><topic>Biological and medical sciences</topic><topic>Chloroplasts</topic><topic>Chloroplasts - metabolism</topic><topic>Crop harvesting</topic><topic>Cytoplasmic Granules - metabolism</topic><topic>Cytoplasmic Granules - ultrastructure</topic><topic>Cytosol</topic><topic>Cytosol - metabolism</topic><topic>Enzymes</topic><topic>Ethanol</topic><topic>Ethanol - pharmacology</topic><topic>Feedback, Physiological - physiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Glucosyltransferases - metabolism</topic><topic>Hydrolysis - drug effects</topic><topic>Immunoblotting</topic><topic>Leaves</topic><topic>Maltose - metabolism</topic><topic>Microscopy, Electron, Scanning</topic><topic>Phosphates</topic><topic>Phosphates - metabolism</topic><topic>Phosphorylation</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - metabolism</topic><topic>Plant physiology and development</topic><topic>Plants</topic><topic>Plants, Genetically Modified</topic><topic>starch</topic><topic>Starch - metabolism</topic><topic>Starch - ultrastructure</topic><topic>Starches</topic><topic>sucrose</topic><topic>Sugar Phosphates - metabolism</topic><topic>Time Factors</topic><topic>trehalose</topic><topic>Trehalose - analogs &amp; derivatives</topic><topic>Trehalose - metabolism</topic><topic>Trisaccharides - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martins, Marina Camara Mattos</creatorcontrib><creatorcontrib>Hejazi, Mahdi</creatorcontrib><creatorcontrib>Fettke, Joerg</creatorcontrib><creatorcontrib>Steup, Martin</creatorcontrib><creatorcontrib>Feil, Regina</creatorcontrib><creatorcontrib>Krause, Ursula</creatorcontrib><creatorcontrib>Arrivault, Stéphanie</creatorcontrib><creatorcontrib>Vosloh, Daniel</creatorcontrib><creatorcontrib>Figueroa, Carlos María</creatorcontrib><creatorcontrib>Ivakov, Alexander</creatorcontrib><creatorcontrib>Yadav, Umesh Prasad</creatorcontrib><creatorcontrib>Piques, Maria</creatorcontrib><creatorcontrib>Metzner, Daniela</creatorcontrib><creatorcontrib>Stitt, Mark</creatorcontrib><creatorcontrib>Lunn, John Edward</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Martins, Marina Camara Mattos</au><au>Hejazi, Mahdi</au><au>Fettke, Joerg</au><au>Steup, Martin</au><au>Feil, Regina</au><au>Krause, Ursula</au><au>Arrivault, Stéphanie</au><au>Vosloh, Daniel</au><au>Figueroa, Carlos María</au><au>Ivakov, Alexander</au><au>Yadav, Umesh Prasad</au><au>Piques, Maria</au><au>Metzner, Daniela</au><au>Stitt, Mark</au><au>Lunn, John Edward</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2013-11-01</date><risdate>2013</risdate><volume>163</volume><issue>3</issue><spage>1142</spage><epage>1163</epage><pages>1142-1163</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><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.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>24043444</pmid><doi>10.1104/pp.113.226787</doi><tpages>22</tpages><oa>free_for_read</oa></addata></record>
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ispartof Plant physiology (Bethesda), 2013-11, Vol.163 (3), p.1142-1163
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source MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Jstor Complete Legacy; Oxford University Press Journals All Titles (1996-Current)
subjects Arabidopsis
Arabidopsis - drug effects
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
BIOCHEMISTRY AND METABOLISM
Biological and medical sciences
Chloroplasts
Chloroplasts - metabolism
Crop harvesting
Cytoplasmic Granules - metabolism
Cytoplasmic Granules - ultrastructure
Cytosol
Cytosol - metabolism
Enzymes
Ethanol
Ethanol - pharmacology
Feedback, Physiological - physiology
Fundamental and applied biological sciences. Psychology
Glucosyltransferases - metabolism
Hydrolysis - drug effects
Immunoblotting
Leaves
Maltose - metabolism
Microscopy, Electron, Scanning
Phosphates
Phosphates - metabolism
Phosphorylation
Plant Leaves - drug effects
Plant Leaves - metabolism
Plant physiology and development
Plants
Plants, Genetically Modified
starch
Starch - metabolism
Starch - ultrastructure
Starches
sucrose
Sugar Phosphates - metabolism
Time Factors
trehalose
Trehalose - analogs & derivatives
Trehalose - metabolism
Trisaccharides - metabolism
title Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate
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