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Mycorrhiza-Triggered Transcriptomic and Metabolomic Networks Impinge on Herbivore Fitness.

Identifieur interne : 000D73 ( Main/Exploration ); précédent : 000D72; suivant : 000D74

Mycorrhiza-Triggered Transcriptomic and Metabolomic Networks Impinge on Herbivore Fitness.

Auteurs : Moritz Kaling [Allemagne] ; Anna Schmidt [Allemagne] ; Franco Moritz [Allemagne] ; Maaria Rosenkranz [Allemagne] ; Michael Witting [Allemagne] ; Karl Kasper [Allemagne] ; Dennis Janz [Allemagne] ; Philippe Schmitt-Kopplin [Allemagne] ; Jörg-Peter Schnitzler [Allemagne] ; Andrea Polle [Allemagne]

Source :

RBID : pubmed:29439210

Descripteurs français

English descriptors

Abstract

Symbioses between plants and mycorrhizal fungi are ubiquitous in ecosystems and strengthen the plants' defense against aboveground herbivores. Here, we studied the underlying regulatory networks and biochemical mechanisms in leaves induced by ectomycorrhizae that modify herbivore interactions. Feeding damage and oviposition by the widespread poplar leaf beetle Chrysomela populi were reduced on the ectomycorrhizal hybrid poplar Populus × canescens Integration of transcriptomics, metabolomics, and volatile emission patterns via mass difference networks demonstrated changes in nitrogen allocation in the leaves of mycorrhizal poplars, down-regulation of phenolic pathways, and up-regulation of defensive systems, including protease inhibitors, chitinases, and aldoxime biosynthesis. Ectomycorrhizae had a systemic influence on jasmonate-related signaling transcripts. Our results suggest that ectomycorrhizae prime wounding responses and shift resources from constitutive phenol-based to specialized protective compounds. Consequently, symbiosis with ectomycorrhizal fungi enabled poplars to respond to leaf beetle feeding with a more effective arsenal of defense mechanisms compared with nonmycorrhizal poplars, thus demonstrating the importance of belowground plant-microbe associations in mitigating aboveground biotic stress.

DOI: 10.1104/pp.17.01810
PubMed: 29439210
PubMed Central: PMC5884605


Affiliations:


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Le document en format XML

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<term>Animaux (MeSH)</term>
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<term>Populus (parasitologie)</term>
<term>Résistance à la maladie (génétique)</term>
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<term>Maladies des plantes</term>
</keywords>
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<term>Plant Diseases</term>
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<div type="abstract" xml:lang="en">Symbioses between plants and mycorrhizal fungi are ubiquitous in ecosystems and strengthen the plants' defense against aboveground herbivores. Here, we studied the underlying regulatory networks and biochemical mechanisms in leaves induced by ectomycorrhizae that modify herbivore interactions. Feeding damage and oviposition by the widespread poplar leaf beetle
<i>Chrysomela populi</i>
were reduced on the ectomycorrhizal hybrid poplar
<i>Populus</i>
×
<i>canescens</i>
Integration of transcriptomics, metabolomics, and volatile emission patterns via mass difference networks demonstrated changes in nitrogen allocation in the leaves of mycorrhizal poplars, down-regulation of phenolic pathways, and up-regulation of defensive systems, including protease inhibitors, chitinases, and aldoxime biosynthesis. Ectomycorrhizae had a systemic influence on jasmonate-related signaling transcripts. Our results suggest that ectomycorrhizae prime wounding responses and shift resources from constitutive phenol-based to specialized protective compounds. Consequently, symbiosis with ectomycorrhizal fungi enabled poplars to respond to leaf beetle feeding with a more effective arsenal of defense mechanisms compared with nonmycorrhizal poplars, thus demonstrating the importance of belowground plant-microbe associations in mitigating aboveground biotic stress.</div>
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</DateCompleted>
<DateRevised>
<Year>2019</Year>
<Month>04</Month>
<Day>01</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1532-2548</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>176</Volume>
<Issue>4</Issue>
<PubDate>
<Year>2018</Year>
<Month>04</Month>
</PubDate>
</JournalIssue>
<Title>Plant physiology</Title>
<ISOAbbreviation>Plant Physiol</ISOAbbreviation>
</Journal>
<ArticleTitle>Mycorrhiza-Triggered Transcriptomic and Metabolomic Networks Impinge on Herbivore Fitness.</ArticleTitle>
<Pagination>
<MedlinePgn>2639-2656</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1104/pp.17.01810</ELocationID>
<Abstract>
<AbstractText>Symbioses between plants and mycorrhizal fungi are ubiquitous in ecosystems and strengthen the plants' defense against aboveground herbivores. Here, we studied the underlying regulatory networks and biochemical mechanisms in leaves induced by ectomycorrhizae that modify herbivore interactions. Feeding damage and oviposition by the widespread poplar leaf beetle
<i>Chrysomela populi</i>
were reduced on the ectomycorrhizal hybrid poplar
<i>Populus</i>
×
<i>canescens</i>
Integration of transcriptomics, metabolomics, and volatile emission patterns via mass difference networks demonstrated changes in nitrogen allocation in the leaves of mycorrhizal poplars, down-regulation of phenolic pathways, and up-regulation of defensive systems, including protease inhibitors, chitinases, and aldoxime biosynthesis. Ectomycorrhizae had a systemic influence on jasmonate-related signaling transcripts. Our results suggest that ectomycorrhizae prime wounding responses and shift resources from constitutive phenol-based to specialized protective compounds. Consequently, symbiosis with ectomycorrhizal fungi enabled poplars to respond to leaf beetle feeding with a more effective arsenal of defense mechanisms compared with nonmycorrhizal poplars, thus demonstrating the importance of belowground plant-microbe associations in mitigating aboveground biotic stress.</AbstractText>
<CopyrightInformation>© 2018 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Kaling</LastName>
<ForeName>Moritz</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Research Unit Environmental Simulation, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, 85764 Neuherberg, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, 85764 Neuherberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmidt</LastName>
<ForeName>Anna</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Forest Botany and Tree Physiology, University of Goettingen, 37077 Goettingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Moritz</LastName>
<ForeName>Franco</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, 85764 Neuherberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rosenkranz</LastName>
<ForeName>Maaria</ForeName>
<Initials>M</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>Witting</LastName>
<ForeName>Michael</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, 85764 Neuherberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kasper</LastName>
<ForeName>Karl</ForeName>
<Initials>K</Initials>
<Identifier Source="ORCID">0000-0002-6020-8829</Identifier>
<AffiliationInfo>
<Affiliation>Forest Botany and Tree Physiology, University of Goettingen, 37077 Goettingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Janz</LastName>
<ForeName>Dennis</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Forest Botany and Tree Physiology, University of Goettingen, 37077 Goettingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmitt-Kopplin</LastName>
<ForeName>Philippe</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, 85764 Neuherberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schnitzler</LastName>
<ForeName>Jörg-Peter</ForeName>
<Initials>JP</Initials>
<Identifier Source="ORCID">0000-0002-9825-867X</Identifier>
<AffiliationInfo>
<Affiliation>Research Unit Environmental Simulation, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, 85764 Neuherberg, Germany jp.schnitzler@helmholtz-muenchen.de apolle@gwdg.de.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Polle</LastName>
<ForeName>Andrea</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">0000-0001-8697-6394</Identifier>
<AffiliationInfo>
<Affiliation>Forest Botany and Tree Physiology, University of Goettingen, 37077 Goettingen, Germany jp.schnitzler@helmholtz-muenchen.de apolle@gwdg.de.</Affiliation>
</AffiliationInfo>
</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>2018</Year>
<Month>02</Month>
<Day>08</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Plant Physiol</MedlineTA>
<NlmUniqueID>0401224</NlmUniqueID>
<ISSNLinking>0032-0889</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001517" MajorTopicYN="N">Coleoptera</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005247" MajorTopicYN="N">Feeding Behavior</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060434" MajorTopicYN="N">Herbivory</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006823" MajorTopicYN="N">Hybrid Vigor</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006824" MajorTopicYN="N">Hybridization, Genetic</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055432" MajorTopicYN="Y">Metabolomics</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059467" MajorTopicYN="Y">Transcriptome</DescriptorName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
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<Year>2018</Year>
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<Year>2018</Year>
<Month>01</Month>
<Day>18</Day>
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<Year>2018</Year>
<Month>2</Month>
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<Hour>6</Hour>
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<ArticleId IdType="pubmed">14756770</ArticleId>
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</Reference>
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<affiliations>
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<country>
<li>Allemagne</li>
</country>
<region>
<li>Basse-Saxe</li>
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<settlement>
<li>Göttingen</li>
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<tree>
<country name="Allemagne">
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<name sortKey="Kaling, Moritz" sort="Kaling, Moritz" uniqKey="Kaling M" first="Moritz" last="Kaling">Moritz Kaling</name>
</noRegion>
<name sortKey="Janz, Dennis" sort="Janz, Dennis" uniqKey="Janz D" first="Dennis" last="Janz">Dennis Janz</name>
<name sortKey="Kaling, Moritz" sort="Kaling, Moritz" uniqKey="Kaling M" first="Moritz" last="Kaling">Moritz Kaling</name>
<name sortKey="Kasper, Karl" sort="Kasper, Karl" uniqKey="Kasper K" first="Karl" last="Kasper">Karl Kasper</name>
<name sortKey="Moritz, Franco" sort="Moritz, Franco" uniqKey="Moritz F" first="Franco" last="Moritz">Franco Moritz</name>
<name sortKey="Polle, Andrea" sort="Polle, Andrea" uniqKey="Polle A" first="Andrea" last="Polle">Andrea Polle</name>
<name sortKey="Rosenkranz, Maaria" sort="Rosenkranz, Maaria" uniqKey="Rosenkranz M" first="Maaria" last="Rosenkranz">Maaria Rosenkranz</name>
<name sortKey="Schmidt, Anna" sort="Schmidt, Anna" uniqKey="Schmidt A" first="Anna" last="Schmidt">Anna Schmidt</name>
<name sortKey="Schmitt Kopplin, Philippe" sort="Schmitt Kopplin, Philippe" uniqKey="Schmitt Kopplin P" first="Philippe" last="Schmitt-Kopplin">Philippe Schmitt-Kopplin</name>
<name sortKey="Schnitzler, Jorg Peter" sort="Schnitzler, Jorg Peter" uniqKey="Schnitzler J" first="Jörg-Peter" last="Schnitzler">Jörg-Peter Schnitzler</name>
<name sortKey="Witting, Michael" sort="Witting, Michael" uniqKey="Witting M" first="Michael" last="Witting">Michael Witting</name>
</country>
</tree>
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