PoplarV1, Main, Exploration, bibRecord, 000721

Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar.

Identifieur interne : 000721 ( Main/Exploration ); précédent : 000720; suivant : 000722

Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar.

Auteurs : Jan Günther [Allemagne] ; Nathalie D. Lackus [Allemagne] ; Axel Schmidt [Allemagne] ; Meret Huber [Allemagne] ; Heike-Jana Stödtler [Allemagne] ; Michael Reichelt [Allemagne] ; Jonathan Gershenzon [Allemagne] ; Tobias G. Köllner [Allemagne]

Source :

Plant physiology [ 1532-2548 ] ; 2019.

RBID : pubmed:30846485

Descripteurs français

KwdFr :
- Alcool phénéthylique (composition chimique), Alcool phénéthylique (métabolisme), Aldose reductase (métabolisme), Cinétique (MeSH), Famille multigénique (MeSH), Feuilles de plante (métabolisme), Gènes de plante (MeSH), Herbivorie (physiologie), Interférence par ARN (MeSH), Mutation (génétique), Métabolome (MeSH), Phylogenèse (MeSH), Populus (enzymologie), Populus (génétique), Populus (métabolisme), Protéines végétales (génétique), Protéines végétales (métabolisme), Régulation de l'expression des gènes végétaux (MeSH), Régulation négative (génétique), Voies de biosynthèse (MeSH).
MESH :
- composition chimique : Alcool phénéthylique.
- enzymologie : Populus.
- génétique : Mutation, Populus, Protéines végétales, Régulation négative.
- métabolisme : Alcool phénéthylique, Aldose reductase, Feuilles de plante, Populus, Protéines végétales.
- physiologie : Herbivorie.
- Cinétique, Famille multigénique, Gènes de plante, Interférence par ARN, Métabolome, Phylogenèse, Régulation de l'expression des gènes végétaux, Voies de biosynthèse.

English descriptors

KwdEn :
- Aldehyde Reductase (metabolism), Biosynthetic Pathways (MeSH), Down-Regulation (genetics), Gene Expression Regulation, Plant (MeSH), Genes, Plant (MeSH), Herbivory (physiology), Kinetics (MeSH), Metabolome (MeSH), Multigene Family (MeSH), Mutation (genetics), Phenylethyl Alcohol (chemistry), Phenylethyl Alcohol (metabolism), Phylogeny (MeSH), Plant Leaves (metabolism), Plant Proteins (genetics), Plant Proteins (metabolism), Populus (enzymology), Populus (genetics), Populus (metabolism), RNA Interference (MeSH).
MESH :
- chemical , chemistry : Phenylethyl Alcohol.
- chemical , genetics : Plant Proteins.
- chemical , metabolism : Aldehyde Reductase, Phenylethyl Alcohol, Plant Proteins.
- enzymology : Populus.
- genetics : Down-Regulation, Mutation, Populus.
- metabolism : Plant Leaves, Populus.
- physiology : Herbivory.
- Biosynthetic Pathways, Gene Expression Regulation, Plant, Genes, Plant, Kinetics, Metabolome, Multigene Family, Phylogeny, RNA Interference.

Abstract

Upon herbivory, the tree species western balsam poplar (Populus trichocarpa) produces a variety of Phe-derived metabolites, including 2-phenylethylamine, 2-phenylethanol, and 2-phenylethyl-β-d-glucopyranoside. To investigate the formation of these potential defense compounds, we functionally characterized aromatic l-amino acid decarboxylases (AADCs) and aromatic aldehyde synthases (AASs), which play important roles in the biosynthesis of specialized aromatic metabolites in other plants. Heterologous expression in Escherichia coli and Nicotiana benthamiana showed that all five AADC/AAS genes identified in the Ptrichocarpa genome encode active enzymes. However, only two genes, PtAADC1 and PtAAS1, were significantly upregulated after leaf herbivory. Despite a sequence similarity of ∼96%, PtAADC1 and PtAAS1 showed different enzymatic functions and converted Phe into 2-phenylethylamine and 2-phenylacetaldehyde, respectively. The activities of both enzymes were interconvertible by switching a single amino acid residue in their active sites. A survey of putative AADC/AAS gene pairs in the genomes of other plants suggests an independent evolution of this function-determining residue in different plant families. RNA interference -mediated-downregulation of AADC1 in gray poplar (Populus × canescens) resulted in decreased accumulation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside, whereas the emission of 2-phenylethanol was not influenced. To investigate the last step of 2-phenylethanol formation, we identified and characterized two Ptrichocarpa short-chain dehydrogenases, PtPAR1 and PtPAR2, which were able to reduce 2-phenylacetaldehyde to 2-phenylethanol in vitro. In summary, 2-phenylethanol and its glucoside may be formed in multiple ways in poplar. Our data indicate that PtAADC1 controls the herbivore-induced formation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside in planta, whereas PtAAS1 likely contributes to the herbivore-induced emission of 2-phenylethanol.

DOI: 10.1104/pp.19.00059
PubMed: 30846485
PubMed Central: PMC6548255

Affiliations:

Allemagne

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Le document en format XML

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<term>Biosynthetic Pathways (MeSH)</term>
<term>Down-Regulation (genetics)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Genes, Plant (MeSH)</term>
<term>Herbivory (physiology)</term>
<term>Kinetics (MeSH)</term>
<term>Metabolome (MeSH)</term>
<term>Multigene Family (MeSH)</term>
<term>Mutation (genetics)</term>
<term>Phenylethyl Alcohol (chemistry)</term>
<term>Phenylethyl Alcohol (metabolism)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Leaves (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Populus (enzymology)</term>
<term>Populus (genetics)</term>
<term>Populus (metabolism)</term>
<term>RNA Interference (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Alcool phénéthylique (composition chimique)</term>
<term>Alcool phénéthylique (métabolisme)</term>
<term>Aldose reductase (métabolisme)</term>
<term>Cinétique (MeSH)</term>
<term>Famille multigénique (MeSH)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Gènes de plante (MeSH)</term>
<term>Herbivorie (physiologie)</term>
<term>Interférence par ARN (MeSH)</term>
<term>Mutation (génétique)</term>
<term>Métabolome (MeSH)</term>
<term>Phylogenèse (MeSH)</term>
<term>Populus (enzymologie)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Régulation négative (génétique)</term>
<term>Voies de biosynthèse (MeSH)</term>
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</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Aldehyde Reductase</term>
<term>Phenylethyl Alcohol</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr"><term>Alcool phénéthylique</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Down-Regulation</term>
<term>Mutation</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Mutation</term>
<term>Populus</term>
<term>Protéines végétales</term>
<term>Régulation négative</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Plant Leaves</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Alcool phénéthylique</term>
<term>Aldose reductase</term>
<term>Feuilles de plante</term>
<term>Populus</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Herbivorie</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Herbivory</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Biosynthetic Pathways</term>
<term>Gene Expression Regulation, Plant</term>
<term>Genes, Plant</term>
<term>Kinetics</term>
<term>Metabolome</term>
<term>Multigene Family</term>
<term>Phylogeny</term>
<term>RNA Interference</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Cinétique</term>
<term>Famille multigénique</term>
<term>Gènes de plante</term>
<term>Interférence par ARN</term>
<term>Métabolome</term>
<term>Phylogenèse</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Voies de biosynthèse</term>
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<front><div type="abstract" xml:lang="en">Upon herbivory, the tree species western balsam poplar (<i>Populus trichocarpa</i>
) produces a variety of Phe-derived metabolites, including 2-phenylethylamine, 2-phenylethanol, and 2-phenylethyl-β-d-glucopyranoside. To investigate the formation of these potential defense compounds, we functionally characterized aromatic l-amino acid decarboxylases (AADCs) and aromatic aldehyde synthases (AASs), which play important roles in the biosynthesis of specialized aromatic metabolites in other plants. Heterologous expression in <i>Escherichia coli</i>
 and <i>Nicotiana benthamiana</i>
 showed that all five <i>AADC</i>
/<i>AAS</i>
 genes identified in the <i>P</i>
<i>trichocarpa</i>
 genome encode active enzymes. However, only two genes, <i>PtAADC1</i>
 and <i>PtAAS1</i>
, were significantly upregulated after leaf herbivory. Despite a sequence similarity of ∼96%, PtAADC1 and PtAAS1 showed different enzymatic functions and converted Phe into 2-phenylethylamine and 2-phenylacetaldehyde, respectively. The activities of both enzymes were interconvertible by switching a single amino acid residue in their active sites. A survey of putative <i>AADC</i>
/<i>AAS</i>
 gene pairs in the genomes of other plants suggests an independent evolution of this function-determining residue in different plant families. RNA interference -mediated-downregulation of <i>AADC1</i>
 in gray poplar (<i>Populus</i>
 × <i>canescens</i>
) resulted in decreased accumulation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside, whereas the emission of 2-phenylethanol was not influenced. To investigate the last step of 2-phenylethanol formation, we identified and characterized two <i>P</i>
<i>trichocarpa</i>
 short-chain dehydrogenases, PtPAR1 and PtPAR2, which were able to reduce 2-phenylacetaldehyde to 2-phenylethanol in vitro. In summary, 2-phenylethanol and its glucoside may be formed in multiple ways in poplar. Our data indicate that PtAADC1 controls the herbivore-induced formation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside in planta, whereas PtAAS1 likely contributes to the herbivore-induced emission of 2-phenylethanol.</div>
</front>
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<Title>Plant physiology</Title>
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<ArticleTitle>Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar.</ArticleTitle>
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<Abstract><AbstractText>Upon herbivory, the tree species western balsam poplar (<i>Populus trichocarpa</i>
) produces a variety of Phe-derived metabolites, including 2-phenylethylamine, 2-phenylethanol, and 2-phenylethyl-β-d-glucopyranoside. To investigate the formation of these potential defense compounds, we functionally characterized aromatic l-amino acid decarboxylases (AADCs) and aromatic aldehyde synthases (AASs), which play important roles in the biosynthesis of specialized aromatic metabolites in other plants. Heterologous expression in <i>Escherichia coli</i>
 and <i>Nicotiana benthamiana</i>
 showed that all five <i>AADC</i>
/<i>AAS</i>
 genes identified in the <i>P</i>
<i>trichocarpa</i>
 genome encode active enzymes. However, only two genes, <i>PtAADC1</i>
 and <i>PtAAS1</i>
, were significantly upregulated after leaf herbivory. Despite a sequence similarity of ∼96%, PtAADC1 and PtAAS1 showed different enzymatic functions and converted Phe into 2-phenylethylamine and 2-phenylacetaldehyde, respectively. The activities of both enzymes were interconvertible by switching a single amino acid residue in their active sites. A survey of putative <i>AADC</i>
/<i>AAS</i>
 gene pairs in the genomes of other plants suggests an independent evolution of this function-determining residue in different plant families. RNA interference -mediated-downregulation of <i>AADC1</i>
 in gray poplar (<i>Populus</i>
 × <i>canescens</i>
) resulted in decreased accumulation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside, whereas the emission of 2-phenylethanol was not influenced. To investigate the last step of 2-phenylethanol formation, we identified and characterized two <i>P</i>
<i>trichocarpa</i>
 short-chain dehydrogenases, PtPAR1 and PtPAR2, which were able to reduce 2-phenylacetaldehyde to 2-phenylethanol in vitro. In summary, 2-phenylethanol and its glucoside may be formed in multiple ways in poplar. Our data indicate that PtAADC1 controls the herbivore-induced formation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside in planta, whereas PtAAS1 likely contributes to the herbivore-induced emission of 2-phenylethanol.</AbstractText>
<CopyrightInformation>© 2019 American Society of Plant Biologists. All Rights Reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Günther</LastName>
<ForeName>Jan</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">0000-0001-8042-5241</Identifier>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Lackus</LastName>
<ForeName>Nathalie D</ForeName>
<Initials>ND</Initials>
<Identifier Source="ORCID">0000-0002-0419-8937</Identifier>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Schmidt</LastName>
<ForeName>Axel</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Huber</LastName>
<ForeName>Meret</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Stödtler</LastName>
<ForeName>Heike-Jana</ForeName>
<Initials>HJ</Initials>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Reichelt</LastName>
<ForeName>Michael</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">0000-0002-6691-6500</Identifier>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Gershenzon</LastName>
<ForeName>Jonathan</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">0000-0002-1812-1551</Identifier>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Köllner</LastName>
<ForeName>Tobias G</ForeName>
<Initials>TG</Initials>
<Identifier Source="ORCID">0000-0002-7037-904X</Identifier>
<AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany koellner@ice.mpg.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>2019</Year>
<Month>03</Month>
<Day>07</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="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 1.1.1.21</RegistryNumber>
<NameOfSubstance UI="D000449">Aldehyde Reductase</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>ML9LGA7468</RegistryNumber>
<NameOfSubstance UI="D010626">Phenylethyl Alcohol</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Plant Physiol. 2019 Jun;180(2):693-694</RefSource>
<PMID Version="1">31160522</PMID>
</CommentsCorrections>
</CommentsCorrectionsList>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000449" MajorTopicYN="N">Aldehyde Reductase</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D053898" MajorTopicYN="Y">Biosynthetic Pathways</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D015536" MajorTopicYN="N">Down-Regulation</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
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<MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
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<MeshHeading><DescriptorName UI="D017343" MajorTopicYN="N">Genes, Plant</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D060434" MajorTopicYN="N">Herbivory</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D007700" MajorTopicYN="N">Kinetics</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D055442" MajorTopicYN="N">Metabolome</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005810" MajorTopicYN="N">Multigene Family</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D009154" MajorTopicYN="N">Mutation</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010626" MajorTopicYN="N">Phenylethyl Alcohol</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D034622" MajorTopicYN="N">RNA Interference</DescriptorName>
</MeshHeading>
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Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar.

Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar.

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