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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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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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><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.113.226787</identifier><identifier>PMID: 24043444</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>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</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. All Rights Reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c538t-b6edf622761a683a2fe200c246b3624bb756108c9565595c71882c3bc6ddbf643</citedby><cites>FETCH-LOGICAL-c538t-b6edf622761a683a2fe200c246b3624bb756108c9565595c71882c3bc6ddbf643</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23598618$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23598618$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,777,781,800,882,27905,27906,57998,58231</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27914352$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24043444$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><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><title>Feedback Inhibition of Starch Degradation in Arabidopsis Leaves Mediated by Trehalose 6-Phosphate</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><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.</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 & 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 & 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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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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