Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes.
Identifieur interne : 000200 ( Main/Corpus ); précédent : 000199; suivant : 000201Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes.
Auteurs : Marc Behr ; Fabien Baldacci-Cresp ; Annegret Kohler ; Kris Morreel ; Geert Goeminne ; Rebecca Van Acker ; Claire Veneault-Fourrey ; Adeline Mol ; Gilles Pilate ; Wout Boerjan ; Janice De Almeida Engler ; Mondher El Jaziri ; Marie BaucherSource :
- Mycorrhiza [ 1432-1890 ] ; 2020.
English descriptors
- KwdEn :
- MESH :
- chemical : Lignin.
- Animals, Gene Expression Regulation, Plant, Mycorrhizae, Nematoda, Populus, Symbiosis.
Abstract
This study investigates the impact of the alteration of the monolignol biosynthesis pathway on the establishment of the in vitro interaction of poplar roots either with a mutualistic ectomycorrhizal fungus or with a pathogenic root-knot nematode. Overall, the five studied transgenic lines downregulated for caffeoyl-CoA O-methyltransferase (CCoAOMT), caffeic acid O-methyltransferase (COMT), cinnamoyl-CoA reductase (CCR), cinnamyl alcohol dehydrogenase (CAD) or both COMT and CAD displayed a lower mycorrhizal colonisation percentage, indicating a lower ability for establishing mutualistic interaction than the wild-type. The susceptibility to root-knot nematode infection was variable in the five lines, and the CAD-deficient line was found to be less susceptible than the wild-type. We discuss these phenotypic differences in the light of the large shifts in the metabolic profile and gene expression pattern occurring between roots of the CAD-deficient line and wild-type. A role of genes related to trehalose metabolism, phytohormones, and cell wall construction in the different mycorrhizal symbiosis efficiency and nematode sensitivity between these two lines is suggested. Overall, these results show that the alteration of plant metabolism caused by the repression of a single gene within phenylpropanoid pathway results in significant alterations, at the root level, in the response towards mutualistic and pathogenic associates. These changes may constrain plant fitness and biomass production, which are of economic importance for perennial industrial crops such as poplar.
DOI: 10.1007/s00572-020-00976-6
PubMed: 32647969
Links to Exploration step
pubmed:32647969Le document en format XML
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uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name><affiliation><nlm:affiliation>Unité Mixte de Recherche 1136, Interactions Arbres-Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRAE Grand-Est-Nancy, INRAE-Université de Lorraine, 54280, Champenoux, France.</nlm:affiliation></affiliation></author><author><name sortKey="Morreel, Kris" sort="Morreel, Kris" uniqKey="Morreel K" first="Kris" last="Morreel">Kris Morreel</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Goeminne, Geert" sort="Goeminne, Geert" uniqKey="Goeminne G" first="Geert" last="Goeminne">Geert Goeminne</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, 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France.</nlm:affiliation></affiliation></author><author><name sortKey="Mol, Adeline" sort="Mol, Adeline" uniqKey="Mol A" first="Adeline" last="Mol">Adeline Mol</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Pilate, Gilles" sort="Pilate, Gilles" uniqKey="Pilate G" first="Gilles" last="Pilate">Gilles Pilate</name><affiliation><nlm:affiliation>BioForA, ONF, INRAE, F-45075, Orléans, France.</nlm:affiliation></affiliation></author><author><name sortKey="Boerjan, Wout" sort="Boerjan, Wout" uniqKey="Boerjan W" first="Wout" last="Boerjan">Wout Boerjan</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="De Almeida Engler, Janice" sort="De Almeida Engler, Janice" uniqKey="De Almeida Engler J" first="Janice" last="De Almeida Engler">Janice De Almeida Engler</name><affiliation><nlm:affiliation>Université Côte d'Azur, CNRS, ISA, INRAE, 06903, Sophia Antipolis, France.</nlm:affiliation></affiliation></author><author><name sortKey="El Jaziri, Mondher" sort="El Jaziri, Mondher" uniqKey="El Jaziri M" first="Mondher" last="El Jaziri">Mondher El Jaziri</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Baucher, Marie" sort="Baucher, Marie" uniqKey="Baucher M" first="Marie" last="Baucher">Marie Baucher</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium. mbaucher@ulb.ac.be.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32647969</idno><idno type="pmid">32647969</idno><idno type="doi">10.1007/s00572-020-00976-6</idno><idno type="wicri:Area/Main/Corpus">000200</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000200</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes.</title><author><name sortKey="Behr, Marc" sort="Behr, Marc" uniqKey="Behr M" first="Marc" last="Behr">Marc Behr</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Baldacci Cresp, Fabien" sort="Baldacci Cresp, Fabien" uniqKey="Baldacci Cresp F" first="Fabien" last="Baldacci-Cresp">Fabien Baldacci-Cresp</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name><affiliation><nlm:affiliation>Unité Mixte de Recherche 1136, Interactions Arbres-Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRAE Grand-Est-Nancy, INRAE-Université de Lorraine, 54280, Champenoux, France.</nlm:affiliation></affiliation></author><author><name sortKey="Morreel, Kris" sort="Morreel, Kris" uniqKey="Morreel K" first="Kris" last="Morreel">Kris Morreel</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Goeminne, Geert" sort="Goeminne, Geert" uniqKey="Goeminne G" first="Geert" last="Goeminne">Geert Goeminne</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>VIB Metabolomics Core, 9052, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Van Acker, Rebecca" sort="Van Acker, Rebecca" uniqKey="Van Acker R" first="Rebecca" last="Van Acker">Rebecca Van Acker</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name><affiliation><nlm:affiliation>Unité Mixte de Recherche 1136, Interactions Arbres-Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRAE Grand-Est-Nancy, INRAE-Université de Lorraine, 54280, Champenoux, France.</nlm:affiliation></affiliation></author><author><name sortKey="Mol, Adeline" sort="Mol, Adeline" uniqKey="Mol A" first="Adeline" last="Mol">Adeline Mol</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Pilate, Gilles" sort="Pilate, Gilles" uniqKey="Pilate G" first="Gilles" last="Pilate">Gilles Pilate</name><affiliation><nlm:affiliation>BioForA, ONF, INRAE, F-45075, Orléans, France.</nlm:affiliation></affiliation></author><author><name sortKey="Boerjan, Wout" sort="Boerjan, Wout" uniqKey="Boerjan W" first="Wout" last="Boerjan">Wout Boerjan</name><affiliation><nlm:affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="De Almeida Engler, Janice" sort="De Almeida Engler, Janice" uniqKey="De Almeida Engler J" first="Janice" last="De Almeida Engler">Janice De Almeida Engler</name><affiliation><nlm:affiliation>Université Côte d'Azur, CNRS, ISA, INRAE, 06903, Sophia Antipolis, France.</nlm:affiliation></affiliation></author><author><name sortKey="El Jaziri, Mondher" sort="El Jaziri, Mondher" uniqKey="El Jaziri M" first="Mondher" last="El Jaziri">Mondher El Jaziri</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Baucher, Marie" sort="Baucher, Marie" uniqKey="Baucher M" first="Marie" last="Baucher">Marie Baucher</name><affiliation><nlm:affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium. mbaucher@ulb.ac.be.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Mycorrhiza</title><idno type="eISSN">1432-1890</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Lignin (MeSH)</term><term>Mycorrhizae (MeSH)</term><term>Nematoda (MeSH)</term><term>Populus (MeSH)</term><term>Symbiosis (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" xml:lang="en"><term>Lignin</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Gene Expression Regulation, Plant</term><term>Mycorrhizae</term><term>Nematoda</term><term>Populus</term><term>Symbiosis</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">This study investigates the impact of the alteration of the monolignol biosynthesis pathway on the establishment of the in vitro interaction of poplar roots either with a mutualistic ectomycorrhizal fungus or with a pathogenic root-knot nematode. Overall, the five studied transgenic lines downregulated for caffeoyl-CoA O-methyltransferase (CCoAOMT), caffeic acid O-methyltransferase (COMT), cinnamoyl-CoA reductase (CCR), cinnamyl alcohol dehydrogenase (CAD) or both COMT and CAD displayed a lower mycorrhizal colonisation percentage, indicating a lower ability for establishing mutualistic interaction than the wild-type. The susceptibility to root-knot nematode infection was variable in the five lines, and the CAD-deficient line was found to be less susceptible than the wild-type. We discuss these phenotypic differences in the light of the large shifts in the metabolic profile and gene expression pattern occurring between roots of the CAD-deficient line and wild-type. A role of genes related to trehalose metabolism, phytohormones, and cell wall construction in the different mycorrhizal symbiosis efficiency and nematode sensitivity between these two lines is suggested. Overall, these results show that the alteration of plant metabolism caused by the repression of a single gene within phenylpropanoid pathway results in significant alterations, at the root level, in the response towards mutualistic and pathogenic associates. These changes may constrain plant fitness and biomass production, which are of economic importance for perennial industrial crops such as poplar.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Automated" Owner="NLM"><PMID Version="1">32647969</PMID><DateCompleted><Year>2020</Year><Month>08</Month><Day>10</Day></DateCompleted><DateRevised><Year>2020</Year><Month>08</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1432-1890</ISSN><JournalIssue CitedMedium="Internet"><Volume>30</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>Sep</Month></PubDate></JournalIssue><Title>Mycorrhiza</Title><ISOAbbreviation>Mycorrhiza</ISOAbbreviation></Journal><ArticleTitle>Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes.</ArticleTitle><Pagination><MedlinePgn>555-566</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1007/s00572-020-00976-6</ELocationID><Abstract><AbstractText>This study investigates the impact of the alteration of the monolignol biosynthesis pathway on the establishment of the in vitro interaction of poplar roots either with a mutualistic ectomycorrhizal fungus or with a pathogenic root-knot nematode. Overall, the five studied transgenic lines downregulated for caffeoyl-CoA O-methyltransferase (CCoAOMT), caffeic acid O-methyltransferase (COMT), cinnamoyl-CoA reductase (CCR), cinnamyl alcohol dehydrogenase (CAD) or both COMT and CAD displayed a lower mycorrhizal colonisation percentage, indicating a lower ability for establishing mutualistic interaction than the wild-type. The susceptibility to root-knot nematode infection was variable in the five lines, and the CAD-deficient line was found to be less susceptible than the wild-type. We discuss these phenotypic differences in the light of the large shifts in the metabolic profile and gene expression pattern occurring between roots of the CAD-deficient line and wild-type. A role of genes related to trehalose metabolism, phytohormones, and cell wall construction in the different mycorrhizal symbiosis efficiency and nematode sensitivity between these two lines is suggested. Overall, these results show that the alteration of plant metabolism caused by the repression of a single gene within phenylpropanoid pathway results in significant alterations, at the root level, in the response towards mutualistic and pathogenic associates. These changes may constrain plant fitness and biomass production, which are of economic importance for perennial industrial crops such as poplar.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Behr</LastName><ForeName>Marc</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-5907-9185</Identifier><AffiliationInfo><Affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baldacci-Cresp</LastName><ForeName>Fabien</ForeName><Initials>F</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7402-2638</Identifier><AffiliationInfo><Affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kohler</LastName><ForeName>Annegret</ForeName><Initials>A</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-9575-9567</Identifier><AffiliationInfo><Affiliation>Unité Mixte de Recherche 1136, Interactions Arbres-Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRAE Grand-Est-Nancy, INRAE-Université de Lorraine, 54280, Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Morreel</LastName><ForeName>Kris</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Goeminne</LastName><ForeName>Geert</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>VIB Metabolomics Core, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Van Acker</LastName><ForeName>Rebecca</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Veneault-Fourrey</LastName><ForeName>Claire</ForeName><Initials>C</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-9778-2659</Identifier><AffiliationInfo><Affiliation>Unité Mixte de Recherche 1136, Interactions Arbres-Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRAE Grand-Est-Nancy, INRAE-Université de Lorraine, 54280, Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mol</LastName><ForeName>Adeline</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pilate</LastName><ForeName>Gilles</ForeName><Initials>G</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-4802-8849</Identifier><AffiliationInfo><Affiliation>BioForA, ONF, INRAE, F-45075, Orléans, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Boerjan</LastName><ForeName>Wout</ForeName><Initials>W</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1495-510X</Identifier><AffiliationInfo><Affiliation>VIB Center for Plant Systems Biology, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>de Almeida Engler</LastName><ForeName>Janice</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Université Côte d'Azur, CNRS, ISA, INRAE, 06903, Sophia Antipolis, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>El Jaziri</LastName><ForeName>Mondher</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-5787-6319</Identifier><AffiliationInfo><Affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baucher</LastName><ForeName>Marie</ForeName><Initials>M</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-2404-8573</Identifier><AffiliationInfo><Affiliation>Laboratoire de Biotechnologie Végétale, Université libre de Bruxelles (ULB), Rue des Professeurs Jeener et Brachet 12, B-6041, Gosselies, Belgium. mbaucher@ulb.ac.be.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>T.0004.14</GrantID><Agency>Fonds De La Recherche Scientifique - FNRS</Agency><Country></Country></Grant><Grant><GrantID>270089</GrantID><Agency>Seventh Framework Programme</Agency><Country></Country></Grant><Grant><GrantID>ANR-11_LABX-0002-01</GrantID><Agency>Agence Nationale de la Recherche</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>09</Day></ArticleDate></Article><MedlineJournalInfo><Country>Germany</Country><MedlineTA>Mycorrhiza</MedlineTA><NlmUniqueID>100955036</NlmUniqueID><ISSNLinking>0940-6360</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>9005-53-2</RegistryNumber><NameOfSubstance UI="D008031">Lignin</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008031" MajorTopicYN="N">Lignin</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D038821" MajorTopicYN="Y">Mycorrhizae</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009348" MajorTopicYN="Y">Nematoda</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="Y">Populus</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Ectomycorrhiza</Keyword><Keyword MajorTopicYN="N">Monolignol</Keyword><Keyword MajorTopicYN="N">Root-knot nematode</Keyword><Keyword MajorTopicYN="N">Secondary metabolites</Keyword><Keyword MajorTopicYN="N">Transcriptomics</Keyword><Keyword MajorTopicYN="N">Transgenic poplar</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>07</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>11</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32647969</ArticleId><ArticleId 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