Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene.
Identifieur interne : 002140 ( Main/Exploration ); précédent : 002139; suivant : 002141Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene.
Auteurs : Andrea Ghirardo [Allemagne] ; Louwrance Peter Wright ; Zhen Bi ; Maaria Rosenkranz ; Pablo Pulido ; Manuel Rodríguez-Concepci N ; Ülo Niinemets ; Nicolas Brüggemann ; Jonathan Gershenzon ; Jörg-Peter SchnitzlerSource :
- Plant physiology [ 1532-2548 ] ; 2014.
Descripteurs français
- KwdFr :
- Analyse des flux métaboliques (méthodes), Butadiènes (MeSH), Carbone (métabolisme), Composés organiques du phosphore (métabolisme), Dioxyde de carbone (métabolisme), Feuilles de plante (effets des radiations), Feuilles de plante (métabolisme), Hémiterpènes (biosynthèse), Hémiterpènes (métabolisme), Isotopes du carbone (MeSH), Lumière (MeSH), Marquage isotopique (MeSH), Modèles biologiques (MeSH), Oses phosphates (métabolisme), Pentanes (MeSH), Pigments biologiques (métabolisme), Plastes (effets des radiations), Plastes (enzymologie), Plastes (métabolisme), Populus (effets des radiations), Populus (métabolisme), Régulation négative (effets des radiations), Température (MeSH), Transferases (métabolisme), Érythritol (analogues et dérivés), Érythritol (métabolisme).
- MESH :
- analogues et dérivés : Érythritol.
- biosynthèse : Hémiterpènes.
- effets des radiations : Feuilles de plante, Plastes, Populus, Régulation négative.
- enzymologie : Plastes.
- métabolisme : Carbone, Composés organiques du phosphore, Dioxyde de carbone, Feuilles de plante, Hémiterpènes, Oses phosphates, Pigments biologiques, Plastes, Populus, Transferases, Érythritol.
- méthodes : Analyse des flux métaboliques.
- Butadiènes, Isotopes du carbone, Lumière, Marquage isotopique, Modèles biologiques, Pentanes, Température.
English descriptors
- KwdEn :
- Butadienes (MeSH), Carbon (metabolism), Carbon Dioxide (metabolism), Carbon Isotopes (MeSH), Down-Regulation (radiation effects), Erythritol (analogs & derivatives), Erythritol (metabolism), Hemiterpenes (biosynthesis), Hemiterpenes (metabolism), Isotope Labeling (MeSH), Light (MeSH), Metabolic Flux Analysis (methods), Models, Biological (MeSH), Organophosphorus Compounds (metabolism), Pentanes (MeSH), Pigments, Biological (metabolism), Plant Leaves (metabolism), Plant Leaves (radiation effects), Plastids (enzymology), Plastids (metabolism), Plastids (radiation effects), Populus (metabolism), Populus (radiation effects), Sugar Phosphates (metabolism), Temperature (MeSH), Transferases (metabolism).
- MESH :
- chemical , analogs & derivatives : Erythritol.
- chemical , biosynthesis : Hemiterpenes.
- chemical , metabolism : Carbon, Carbon Dioxide, Erythritol, Hemiterpenes, Organophosphorus Compounds, Pigments, Biological, Sugar Phosphates, Transferases.
- chemical : Butadienes, Carbon Isotopes, Pentanes.
- enzymology : Plastids.
- metabolism : Plant Leaves, Plastids, Populus.
- methods : Metabolic Flux Analysis.
- radiation effects : Down-Regulation, Plant Leaves, Plastids, Populus.
- Isotope Labeling, Light, Models, Biological, Temperature.
Abstract
The plastidic 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway is one of the most important pathways in plants and produces a large variety of essential isoprenoids. Its regulation, however, is still not well understood. Using the stable isotope 13C-labeling technique, we analyzed the carbon fluxes through the MEP pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus×canescens). We assessed the dependence on temperature, light intensity, and atmospheric [CO2]. Isoprene biosynthesis was by far (99%) the main carbon sink of MEP pathway intermediates in mature gray poplar leaves, and its production required severalfold higher carbon fluxes compared with NE leaves with almost zero isoprene emission. To compensate for the much lower demand for carbon, NE leaves drastically reduced the overall carbon flux within the MEP pathway. Feedback inhibition of 1-deoxy-D-xylulose-5-phosphate synthase activity by accumulated plastidic dimethylallyl diphosphate almost completely explained this reduction in carbon flux. Our data demonstrate that short-term biochemical feedback regulation of 1-deoxy-d-xylulose-5-phosphate synthase activity by plastidic dimethylallyl diphosphate is an important regulatory mechanism of the MEP pathway. Despite being relieved from the large carbon demand of isoprene biosynthesis, NE plants redirected only approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. β-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties.
DOI: 10.1104/pp.114.236018
PubMed: 24590857
PubMed Central: PMC4012595
Affiliations:
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last="Brüggemann">Nicolas Brüggemann</name></author><author><name sortKey="Gershenzon, Jonathan" sort="Gershenzon, Jonathan" uniqKey="Gershenzon J" first="Jonathan" last="Gershenzon">Jonathan Gershenzon</name></author><author><name sortKey="Schnitzler, Jorg Peter" sort="Schnitzler, Jorg Peter" uniqKey="Schnitzler J" first="Jörg-Peter" last="Schnitzler">Jörg-Peter Schnitzler</name></author></analytic><series><title level="j">Plant physiology</title><idno type="eISSN">1532-2548</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Butadienes (MeSH)</term><term>Carbon (metabolism)</term><term>Carbon Dioxide (metabolism)</term><term>Carbon Isotopes (MeSH)</term><term>Down-Regulation (radiation effects)</term><term>Erythritol (analogs & derivatives)</term><term>Erythritol (metabolism)</term><term>Hemiterpenes (biosynthesis)</term><term>Hemiterpenes (metabolism)</term><term>Isotope Labeling (MeSH)</term><term>Light (MeSH)</term><term>Metabolic Flux Analysis (methods)</term><term>Models, Biological (MeSH)</term><term>Organophosphorus Compounds (metabolism)</term><term>Pentanes (MeSH)</term><term>Pigments, Biological (metabolism)</term><term>Plant Leaves (metabolism)</term><term>Plant Leaves (radiation effects)</term><term>Plastids (enzymology)</term><term>Plastids (metabolism)</term><term>Plastids (radiation effects)</term><term>Populus (metabolism)</term><term>Populus (radiation effects)</term><term>Sugar Phosphates (metabolism)</term><term>Temperature (MeSH)</term><term>Transferases (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Analyse des flux métaboliques (méthodes)</term><term>Butadiènes (MeSH)</term><term>Carbone (métabolisme)</term><term>Composés organiques du phosphore (métabolisme)</term><term>Dioxyde de carbone (métabolisme)</term><term>Feuilles de plante (effets des radiations)</term><term>Feuilles de plante (métabolisme)</term><term>Hémiterpènes (biosynthèse)</term><term>Hémiterpènes (métabolisme)</term><term>Isotopes du carbone (MeSH)</term><term>Lumière (MeSH)</term><term>Marquage isotopique (MeSH)</term><term>Modèles biologiques (MeSH)</term><term>Oses phosphates (métabolisme)</term><term>Pentanes (MeSH)</term><term>Pigments biologiques (métabolisme)</term><term>Plastes (effets des radiations)</term><term>Plastes (enzymologie)</term><term>Plastes (métabolisme)</term><term>Populus (effets des radiations)</term><term>Populus (métabolisme)</term><term>Régulation négative (effets des radiations)</term><term>Température (MeSH)</term><term>Transferases (métabolisme)</term><term>Érythritol (analogues et dérivés)</term><term>Érythritol (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="analogs & derivatives" xml:lang="en"><term>Erythritol</term></keywords><keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en"><term>Hemiterpenes</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Carbon</term><term>Carbon Dioxide</term><term>Erythritol</term><term>Hemiterpenes</term><term>Organophosphorus Compounds</term><term>Pigments, Biological</term><term>Sugar Phosphates</term><term>Transferases</term></keywords><keywords scheme="MESH" type="chemical" xml:lang="en"><term>Butadienes</term><term>Carbon Isotopes</term><term>Pentanes</term></keywords><keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr"><term>Érythritol</term></keywords><keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr"><term>Hémiterpènes</term></keywords><keywords scheme="MESH" qualifier="effets des radiations" xml:lang="fr"><term>Feuilles de plante</term><term>Plastes</term><term>Populus</term><term>Régulation négative</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Plastes</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Plastids</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Plant Leaves</term><term>Plastids</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Metabolic Flux Analysis</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Carbone</term><term>Composés organiques du phosphore</term><term>Dioxyde de carbone</term><term>Feuilles de plante</term><term>Hémiterpènes</term><term>Oses phosphates</term><term>Pigments biologiques</term><term>Plastes</term><term>Populus</term><term>Transferases</term><term>Érythritol</term></keywords><keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Analyse des flux métaboliques</term></keywords><keywords scheme="MESH" qualifier="radiation effects" xml:lang="en"><term>Down-Regulation</term><term>Plant Leaves</term><term>Plastids</term><term>Populus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Isotope Labeling</term><term>Light</term><term>Models, Biological</term><term>Temperature</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Butadiènes</term><term>Isotopes du carbone</term><term>Lumière</term><term>Marquage isotopique</term><term>Modèles biologiques</term><term>Pentanes</term><term>Température</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The plastidic 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway is one of the most important pathways in plants and produces a large variety of essential isoprenoids. Its regulation, however, is still not well understood. Using the stable isotope 13C-labeling technique, we analyzed the carbon fluxes through the MEP pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus×canescens). We assessed the dependence on temperature, light intensity, and atmospheric [CO2]. Isoprene biosynthesis was by far (99%) the main carbon sink of MEP pathway intermediates in mature gray poplar leaves, and its production required severalfold higher carbon fluxes compared with NE leaves with almost zero isoprene emission. To compensate for the much lower demand for carbon, NE leaves drastically reduced the overall carbon flux within the MEP pathway. Feedback inhibition of 1-deoxy-D-xylulose-5-phosphate synthase activity by accumulated plastidic dimethylallyl diphosphate almost completely explained this reduction in carbon flux. Our data demonstrate that short-term biochemical feedback regulation of 1-deoxy-d-xylulose-5-phosphate synthase activity by plastidic dimethylallyl diphosphate is an important regulatory mechanism of the MEP pathway. Despite being relieved from the large carbon demand of isoprene biosynthesis, NE plants redirected only approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. β-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24590857</PMID><DateCompleted><Year>2014</Year><Month>12</Month><Day>22</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>13</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-2548</ISSN><JournalIssue CitedMedium="Internet"><Volume>165</Volume><Issue>1</Issue><PubDate><Year>2014</Year><Month>May</Month></PubDate></JournalIssue><Title>Plant physiology</Title><ISOAbbreviation>Plant Physiol</ISOAbbreviation></Journal><ArticleTitle>Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene.</ArticleTitle><Pagination><MedlinePgn>37-51</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.114.236018</ELocationID><Abstract><AbstractText>The plastidic 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway is one of the most important pathways in plants and produces a large variety of essential isoprenoids. Its regulation, however, is still not well understood. Using the stable isotope 13C-labeling technique, we analyzed the carbon fluxes through the MEP pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus×canescens). We assessed the dependence on temperature, light intensity, and atmospheric [CO2]. Isoprene biosynthesis was by far (99%) the main carbon sink of MEP pathway intermediates in mature gray poplar leaves, and its production required severalfold higher carbon fluxes compared with NE leaves with almost zero isoprene emission. To compensate for the much lower demand for carbon, NE leaves drastically reduced the overall carbon flux within the MEP pathway. Feedback inhibition of 1-deoxy-D-xylulose-5-phosphate synthase activity by accumulated plastidic dimethylallyl diphosphate almost completely explained this reduction in carbon flux. Our data demonstrate that short-term biochemical feedback regulation of 1-deoxy-d-xylulose-5-phosphate synthase activity by plastidic dimethylallyl diphosphate is an important regulatory mechanism of the MEP pathway. Despite being relieved from the large carbon demand of isoprene biosynthesis, NE plants redirected only approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. β-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ghirardo</LastName><ForeName>Andrea</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Research Unit Environmental Simulation, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, 85764 Neuherberg, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wright</LastName><ForeName>Louwrance Peter</ForeName><Initials>LP</Initials></Author><Author ValidYN="Y"><LastName>Bi</LastName><ForeName>Zhen</ForeName><Initials>Z</Initials></Author><Author ValidYN="Y"><LastName>Rosenkranz</LastName><ForeName>Maaria</ForeName><Initials>M</Initials></Author><Author ValidYN="Y"><LastName>Pulido</LastName><ForeName>Pablo</ForeName><Initials>P</Initials></Author><Author ValidYN="Y"><LastName>Rodríguez-Concepción</LastName><ForeName>Manuel</ForeName><Initials>M</Initials></Author><Author ValidYN="Y"><LastName>Niinemets</LastName><ForeName>Ülo</ForeName><Initials>Ü</Initials></Author><Author ValidYN="Y"><LastName>Brüggemann</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials></Author><Author ValidYN="Y"><LastName>Gershenzon</LastName><ForeName>Jonathan</ForeName><Initials>J</Initials></Author><Author ValidYN="Y"><LastName>Schnitzler</LastName><ForeName>Jörg-Peter</ForeName><Initials>JP</Initials></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>03</Month><Day>03</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Plant Physiol</MedlineTA><NlmUniqueID>0401224</NlmUniqueID><ISSNLinking>0032-0889</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C114232">2-C-methylerythritol 4-phosphate</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D002070">Butadienes</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D002247">Carbon Isotopes</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D045782">Hemiterpenes</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D009943">Organophosphorus Compounds</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010420">Pentanes</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010860">Pigments, Biological</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D013403">Sugar Phosphates</NameOfSubstance></Chemical><Chemical><RegistryNumber>0A62964IBU</RegistryNumber><NameOfSubstance UI="C005059">isoprene</NameOfSubstance></Chemical><Chemical><RegistryNumber>142M471B3J</RegistryNumber><NameOfSubstance UI="D002245">Carbon Dioxide</NameOfSubstance></Chemical><Chemical><RegistryNumber>358-72-5</RegistryNumber><NameOfSubstance UI="C043060">3,3-dimethylallyl pyrophosphate</NameOfSubstance></Chemical><Chemical><RegistryNumber>7440-44-0</RegistryNumber><NameOfSubstance UI="D002244">Carbon</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.-</RegistryNumber><NameOfSubstance UI="D014166">Transferases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 2.2.1.-</RegistryNumber><NameOfSubstance UI="C109461">deoxyxylulose-5-phosphate synthase</NameOfSubstance></Chemical><Chemical><RegistryNumber>RA96B954X6</RegistryNumber><NameOfSubstance UI="D004896">Erythritol</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D002070" MajorTopicYN="N">Butadienes</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002244" MajorTopicYN="N">Carbon</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002245" MajorTopicYN="N">Carbon Dioxide</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002247" MajorTopicYN="N">Carbon Isotopes</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015536" MajorTopicYN="N">Down-Regulation</DescriptorName><QualifierName UI="Q000528" MajorTopicYN="N">radiation 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