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Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1.

Identifieur interne : 001442 ( Main/Exploration ); précédent : 001441; suivant : 001443

Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1.

Auteurs : Rebecca Van Acker [Belgique] ; Annabelle Déjardin [France] ; Sandrien Desmet [Belgique] ; Lennart Hoengenaert [Belgique] ; Ruben Vanholme [Belgique] ; Kris Morreel [Belgique] ; Françoise Laurans [France] ; Hoon Kim [États-Unis] ; Nicholas Santoro [États-Unis] ; Cliff Foster [États-Unis] ; Geert Goeminne [Belgique] ; Frédéric Légée [France] ; Catherine Lapierre [France] ; Gilles Pilate [France] ; John Ralph [États-Unis] ; Wout Boerjan [Belgique]

Source :

RBID : pubmed:28878036

Descripteurs français

English descriptors

Abstract

In the search for renewable energy sources, genetic engineering is a promising strategy to improve plant cell wall composition for biofuel and bioproducts generation. Lignin is a major factor determining saccharification efficiency and, therefore, is a prime target to engineer. Here, lignin content and composition were modified in poplar (Populus tremula × Populus alba) by specifically down-regulating CINNAMYL ALCOHOL DEHYDROGENASE1 (CAD1) by a hairpin-RNA-mediated silencing approach, which resulted in only 5% residual CAD1 transcript abundance. These transgenic lines showed no biomass penalty despite a 10% reduction in Klason lignin content and severe shifts in lignin composition. Nuclear magnetic resonance spectroscopy and thioacidolysis revealed a strong increase (up to 20-fold) in sinapaldehyde incorporation into lignin, whereas coniferaldehyde was not increased markedly. Accordingly, ultra-high-performance liquid chromatography-mass spectrometry-based phenolic profiling revealed a more than 24,000-fold accumulation of a newly identified compound made from 8-8 coupling of two sinapaldehyde radicals. However, no additional cinnamaldehyde coupling products could be detected in the CAD1-deficient poplars. Instead, the transgenic lines accumulated a range of hydroxycinnamate-derived metabolites, of which the most prominent accumulation (over 8,500-fold) was observed for a compound that was identified by purification and nuclear magnetic resonance as syringyl lactic acid hexoside. Our data suggest that, upon down-regulation of CAD1, coniferaldehyde is converted into ferulic acid and derivatives, whereas sinapaldehyde is either oxidatively coupled into S'(8-8)S' and lignin or converted to sinapic acid and derivatives. The most prominent sink of the increased flux to hydroxycinnamates is syringyl lactic acid hexoside. Furthermore, low-extent saccharification assays, under different pretreatment conditions, showed strongly increased glucose (up to +81%) and xylose (up to +153%) release, suggesting that down-regulating CAD1 is a promising strategy for improving lignocellulosic biomass for the sugar platform industry.

DOI: 10.1104/pp.17.00834
PubMed: 28878036
PubMed Central: PMC5664467


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Le document en format XML

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<name sortKey="Goeminne, Geert" sort="Goeminne, Geert" uniqKey="Goeminne G" first="Geert" last="Goeminne">Geert Goeminne</name>
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<name sortKey="Ralph, John" sort="Ralph, John" uniqKey="Ralph J" first="John" last="Ralph">John Ralph</name>
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<name sortKey="Boerjan, Wout" sort="Boerjan, Wout" uniqKey="Boerjan W" first="Wout" last="Boerjan">Wout Boerjan</name>
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<title xml:lang="en">Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1.</title>
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<name sortKey="Morreel, Kris" sort="Morreel, Kris" uniqKey="Morreel K" first="Kris" last="Morreel">Kris Morreel</name>
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<nlm:affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</nlm:affiliation>
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<nlm:affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</nlm:affiliation>
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<nlm:affiliation>AGPF, INRA, 45075 Orléans, France.</nlm:affiliation>
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<name sortKey="Kim, Hoon" sort="Kim, Hoon" uniqKey="Kim H" first="Hoon" last="Kim">Hoon Kim</name>
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<nlm:affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</nlm:affiliation>
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<region type="state">Wisconsin</region>
</placeName>
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<nlm:affiliation>Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53726-4084.</nlm:affiliation>
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<region type="state">Wisconsin</region>
</placeName>
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<nlm:affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</nlm:affiliation>
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<region type="state">Wisconsin</region>
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<author>
<name sortKey="Foster, Cliff" sort="Foster, Cliff" uniqKey="Foster C" first="Cliff" last="Foster">Cliff Foster</name>
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<nlm:affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</nlm:affiliation>
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<region type="state">Wisconsin</region>
</placeName>
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</affiliation>
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<name sortKey="Goeminne, Geert" sort="Goeminne, Geert" uniqKey="Goeminne G" first="Geert" last="Goeminne">Geert Goeminne</name>
<affiliation wicri:level="4">
<nlm:affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
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<orgName type="university">Université de Gand</orgName>
<placeName>
<settlement type="city">Gand</settlement>
<region>Région flamande</region>
<region type="district" nuts="2">Province de Flandre-Orientale</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</nlm:affiliation>
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</affiliation>
</author>
<author>
<name sortKey="Legee, Frederic" sort="Legee, Frederic" uniqKey="Legee F" first="Frédéric" last="Légée">Frédéric Légée</name>
<affiliation wicri:level="3">
<nlm:affiliation>INRA/AgroParisTech, UMR1318, Saclay Plant Science, Jean-Pierre Bourgin Institute, Versailles, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA/AgroParisTech, UMR1318, Saclay Plant Science, Jean-Pierre Bourgin Institute, Versailles</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Versailles</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Lapierre, Catherine" sort="Lapierre, Catherine" uniqKey="Lapierre C" first="Catherine" last="Lapierre">Catherine Lapierre</name>
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<nlm:affiliation>INRA/AgroParisTech, UMR1318, Saclay Plant Science, Jean-Pierre Bourgin Institute, Versailles, France.</nlm:affiliation>
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<wicri:regionArea>INRA/AgroParisTech, UMR1318, Saclay Plant Science, Jean-Pierre Bourgin Institute, Versailles</wicri:regionArea>
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<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Versailles</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Pilate, Gilles" sort="Pilate, Gilles" uniqKey="Pilate G" first="Gilles" last="Pilate">Gilles Pilate</name>
<affiliation wicri:level="3">
<nlm:affiliation>AGPF, INRA, 45075 Orléans, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<placeName>
<region type="region" nuts="2">Centre-Val de Loire</region>
<region type="old region" nuts="2">Région Centre</region>
<settlement type="city">Orléans</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Ralph, John" sort="Ralph, John" uniqKey="Ralph J" first="John" last="Ralph">John Ralph</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Wisconsin</region>
</placeName>
<wicri:cityArea>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Boerjan, Wout" sort="Boerjan, Wout" uniqKey="Boerjan W" first="Wout" last="Boerjan">Wout Boerjan</name>
<affiliation wicri:level="4">
<nlm:affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium wout.boerjan@ugent.vib.be.</nlm:affiliation>
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<wicri:regionArea>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent</wicri:regionArea>
<orgName type="university">Université de Gand</orgName>
<placeName>
<settlement type="city">Gand</settlement>
<region>Région flamande</region>
<region type="district" nuts="2">Province de Flandre-Orientale</region>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>VIB Center for Plant Systems Biology, 9052 Ghent</wicri:regionArea>
<wicri:noRegion>9052 Ghent</wicri:noRegion>
</affiliation>
</author>
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<series>
<title level="j">Plant physiology</title>
<idno type="eISSN">1532-2548</idno>
<imprint>
<date when="2017" type="published">2017</date>
</imprint>
</series>
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<term>Acrolein (analogs & derivatives)</term>
<term>Acrolein (chemistry)</term>
<term>Acrolein (metabolism)</term>
<term>Alcohol Oxidoreductases (metabolism)</term>
<term>Alkalies (pharmacology)</term>
<term>Biomass (MeSH)</term>
<term>Carbohydrate Metabolism (MeSH)</term>
<term>Cell Wall (metabolism)</term>
<term>Lignin (chemistry)</term>
<term>Lignin (metabolism)</term>
<term>Magnetic Resonance Spectroscopy (MeSH)</term>
<term>Metabolic Networks and Pathways (MeSH)</term>
<term>Methanol (chemistry)</term>
<term>Models, Molecular (MeSH)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Phenols (metabolism)</term>
<term>Phenotype (MeSH)</term>
<term>Pigmentation (MeSH)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Populus (genetics)</term>
<term>Solubility (MeSH)</term>
<term>Tandem Mass Spectrometry (MeSH)</term>
<term>Tracheophyta (enzymology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acroléine (analogues et dérivés)</term>
<term>Acroléine (composition chimique)</term>
<term>Acroléine (métabolisme)</term>
<term>Alcalis (pharmacologie)</term>
<term>Alcohol oxidoreductases (métabolisme)</term>
<term>Biomasse (MeSH)</term>
<term>Lignine (composition chimique)</term>
<term>Lignine (métabolisme)</term>
<term>Modèles moléculaires (MeSH)</term>
<term>Métabolisme glucidique (MeSH)</term>
<term>Méthanol (composition chimique)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Paroi cellulaire (métabolisme)</term>
<term>Phénols (métabolisme)</term>
<term>Phénotype (MeSH)</term>
<term>Pigmentation (MeSH)</term>
<term>Populus (génétique)</term>
<term>Solubilité (MeSH)</term>
<term>Spectrométrie de masse en tandem (MeSH)</term>
<term>Spectroscopie par résonance magnétique (MeSH)</term>
<term>Tracheobionta (enzymologie)</term>
<term>Voies et réseaux métaboliques (MeSH)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
</keywords>
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<term>Acrolein</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Acrolein</term>
<term>Lignin</term>
<term>Methanol</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Acrolein</term>
<term>Alcohol Oxidoreductases</term>
<term>Lignin</term>
<term>Phenols</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Alkalies</term>
</keywords>
<keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr">
<term>Acroléine</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Acroléine</term>
<term>Lignine</term>
<term>Méthanol</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Tracheobionta</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Tracheophyta</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Cell Wall</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Acroléine</term>
<term>Alcohol oxidoreductases</term>
<term>Lignine</term>
<term>Paroi cellulaire</term>
<term>Phénols</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Alcalis</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Biomass</term>
<term>Carbohydrate Metabolism</term>
<term>Magnetic Resonance Spectroscopy</term>
<term>Metabolic Networks and Pathways</term>
<term>Models, Molecular</term>
<term>Oxidation-Reduction</term>
<term>Phenotype</term>
<term>Pigmentation</term>
<term>Plants, Genetically Modified</term>
<term>Solubility</term>
<term>Tandem Mass Spectrometry</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Biomasse</term>
<term>Modèles moléculaires</term>
<term>Métabolisme glucidique</term>
<term>Oxydoréduction</term>
<term>Phénotype</term>
<term>Pigmentation</term>
<term>Solubilité</term>
<term>Spectrométrie de masse en tandem</term>
<term>Spectroscopie par résonance magnétique</term>
<term>Voies et réseaux métaboliques</term>
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<front>
<div type="abstract" xml:lang="en">In the search for renewable energy sources, genetic engineering is a promising strategy to improve plant cell wall composition for biofuel and bioproducts generation. Lignin is a major factor determining saccharification efficiency and, therefore, is a prime target to engineer. Here, lignin content and composition were modified in poplar (
<i>Populus tremula</i>
×
<i>Populus alba</i>
) by specifically down-regulating
<i>CINNAMYL ALCOHOL DEHYDROGENASE1</i>
(
<i>CAD1</i>
) by a hairpin-RNA-mediated silencing approach, which resulted in only 5% residual
<i>CAD1</i>
transcript abundance. These transgenic lines showed no biomass penalty despite a 10% reduction in Klason lignin content and severe shifts in lignin composition. Nuclear magnetic resonance spectroscopy and thioacidolysis revealed a strong increase (up to 20-fold) in sinapaldehyde incorporation into lignin, whereas coniferaldehyde was not increased markedly. Accordingly, ultra-high-performance liquid chromatography-mass spectrometry-based phenolic profiling revealed a more than 24,000-fold accumulation of a newly identified compound made from 8-8 coupling of two sinapaldehyde radicals. However, no additional cinnamaldehyde coupling products could be detected in the CAD1-deficient poplars. Instead, the transgenic lines accumulated a range of hydroxycinnamate-derived metabolites, of which the most prominent accumulation (over 8,500-fold) was observed for a compound that was identified by purification and nuclear magnetic resonance as syringyl lactic acid hexoside. Our data suggest that, upon down-regulation of
<i>CAD1</i>
, coniferaldehyde is converted into ferulic acid and derivatives, whereas sinapaldehyde is either oxidatively coupled into S'(8-8)S' and lignin or converted to sinapic acid and derivatives. The most prominent sink of the increased flux to hydroxycinnamates is syringyl lactic acid hexoside. Furthermore, low-extent saccharification assays, under different pretreatment conditions, showed strongly increased glucose (up to +81%) and xylose (up to +153%) release, suggesting that down-regulating
<i>CAD1</i>
is a promising strategy for improving lignocellulosic biomass for the sugar platform industry.</div>
</front>
</TEI>
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<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">28878036</PMID>
<DateCompleted>
<Year>2018</Year>
<Month>07</Month>
<Day>03</Day>
</DateCompleted>
<DateRevised>
<Year>2019</Year>
<Month>12</Month>
<Day>10</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>175</Volume>
<Issue>3</Issue>
<PubDate>
<Year>2017</Year>
<Month>Nov</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1.</ArticleTitle>
<Pagination>
<MedlinePgn>1018-1039</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.17.00834</ELocationID>
<Abstract>
<AbstractText>In the search for renewable energy sources, genetic engineering is a promising strategy to improve plant cell wall composition for biofuel and bioproducts generation. Lignin is a major factor determining saccharification efficiency and, therefore, is a prime target to engineer. Here, lignin content and composition were modified in poplar (
<i>Populus tremula</i>
×
<i>Populus alba</i>
) by specifically down-regulating
<i>CINNAMYL ALCOHOL DEHYDROGENASE1</i>
(
<i>CAD1</i>
) by a hairpin-RNA-mediated silencing approach, which resulted in only 5% residual
<i>CAD1</i>
transcript abundance. These transgenic lines showed no biomass penalty despite a 10% reduction in Klason lignin content and severe shifts in lignin composition. Nuclear magnetic resonance spectroscopy and thioacidolysis revealed a strong increase (up to 20-fold) in sinapaldehyde incorporation into lignin, whereas coniferaldehyde was not increased markedly. Accordingly, ultra-high-performance liquid chromatography-mass spectrometry-based phenolic profiling revealed a more than 24,000-fold accumulation of a newly identified compound made from 8-8 coupling of two sinapaldehyde radicals. However, no additional cinnamaldehyde coupling products could be detected in the CAD1-deficient poplars. Instead, the transgenic lines accumulated a range of hydroxycinnamate-derived metabolites, of which the most prominent accumulation (over 8,500-fold) was observed for a compound that was identified by purification and nuclear magnetic resonance as syringyl lactic acid hexoside. Our data suggest that, upon down-regulation of
<i>CAD1</i>
, coniferaldehyde is converted into ferulic acid and derivatives, whereas sinapaldehyde is either oxidatively coupled into S'(8-8)S' and lignin or converted to sinapic acid and derivatives. The most prominent sink of the increased flux to hydroxycinnamates is syringyl lactic acid hexoside. Furthermore, low-extent saccharification assays, under different pretreatment conditions, showed strongly increased glucose (up to +81%) and xylose (up to +153%) release, suggesting that down-regulating
<i>CAD1</i>
is a promising strategy for improving lignocellulosic biomass for the sugar platform industry.</AbstractText>
<CopyrightInformation>© 2017 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
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<Author ValidYN="Y">
<LastName>Van Acker</LastName>
<ForeName>Rebecca</ForeName>
<Initials>R</Initials>
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<AffiliationInfo>
<Affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Déjardin</LastName>
<ForeName>Annabelle</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-7576-5476</Identifier>
<AffiliationInfo>
<Affiliation>AGPF, INRA, 45075 Orléans, France.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Desmet</LastName>
<ForeName>Sandrien</ForeName>
<Initials>S</Initials>
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<AffiliationInfo>
<Affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
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<LastName>Hoengenaert</LastName>
<ForeName>Lennart</ForeName>
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<AffiliationInfo>
<Affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
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<AffiliationInfo>
<Affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
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<AffiliationInfo>
<Affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
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</AffiliationInfo>
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</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Kim</LastName>
<ForeName>Hoon</ForeName>
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<AffiliationInfo>
<Affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53726-4084.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Santoro</LastName>
<ForeName>Nicholas</ForeName>
<Initials>N</Initials>
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<AffiliationInfo>
<Affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</Affiliation>
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</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Lapierre</LastName>
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<AffiliationInfo>
<Affiliation>INRA/AgroParisTech, UMR1318, Saclay Plant Science, Jean-Pierre Bourgin Institute, Versailles, France.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Pilate</LastName>
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<AffiliationInfo>
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</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ralph</LastName>
<ForeName>John</ForeName>
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<AffiliationInfo>
<Affiliation>Department of Energy Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, Madison, Wisconsin 53726-4084.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Boerjan</LastName>
<ForeName>Wout</ForeName>
<Initials>W</Initials>
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<AffiliationInfo>
<Affiliation>Ghent University, Department of Plant Biotechnology and Bioinformatics, 9052 Ghent, Belgium wout.boerjan@ugent.vib.be.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>VIB Center for Plant Systems Biology, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
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<Month>09</Month>
<Day>06</Day>
</ArticleDate>
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<Chemical>
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<li>Centre-Val de Loire</li>
<li>Province de Flandre-Orientale</li>
<li>Région Centre</li>
<li>Région flamande</li>
<li>Wisconsin</li>
<li>Île-de-France</li>
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<li>Gand</li>
<li>Orléans</li>
<li>Versailles</li>
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<li>Université de Gand</li>
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<name sortKey="Morreel, Kris" sort="Morreel, Kris" uniqKey="Morreel K" first="Kris" last="Morreel">Kris Morreel</name>
<name sortKey="Van Acker, Rebecca" sort="Van Acker, Rebecca" uniqKey="Van Acker R" first="Rebecca" last="Van Acker">Rebecca Van Acker</name>
<name sortKey="Vanholme, Ruben" sort="Vanholme, Ruben" uniqKey="Vanholme R" first="Ruben" last="Vanholme">Ruben Vanholme</name>
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