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Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus trichocarpa.

Identifieur interne : 000905 ( Main/Exploration ); précédent : 000904; suivant : 000906

Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus trichocarpa.

Auteurs : Nathalie D. Lackus [Allemagne] ; Nora P. Petersen [Allemagne] ; Raimund Nagel [États-Unis] ; Axel Schmidt [Allemagne] ; Sandra Irmisch [Canada] ; Jonathan Gershenzon [Allemagne] ; Tobias G. Köllner [Allemagne]

Source :

RBID : pubmed:31261889

Descripteurs français

English descriptors

Abstract

In response to insect herbivory, poplar releases a blend of volatiles that plays important roles in plant defense. Although the volatile bouquet is highly complex and comprises several classes of compounds, it is dominated by mono- and sesquiterpenes. The most common precursors for mono- and sesquiterpenes, geranyl diphosphate (GPP) and (E,E)-farnesyl diphosphate (FPP), respectively, are in general produced by homodimeric or heterodimeric trans-isopentenyl diphosphate synthases (trans-IDSs) that belong to the family of prenyltransferases. To understand the molecular basis of herbivory-induced terpene formation in poplar, we investigated the trans-IDS gene family in the western balsam poplar Populus trichocarpa. Sequence comparisons suggested that this species possesses a single FPP synthase gene (PtFPPS1) and four genes encoding two large subunits (PtGPPS1.LSU and PtGPPS2.LSU) and two small subunits (PtGPPS.SSU1 and PtGPPS.SSU2) of GPP synthases. Transcript accumulation of PtGPPS1.LSU and PtGPPS.SSU1 was significantly upregulated upon leaf herbivory, while the expression of PtFPPS1, PtGPPS2.LSU, and PtGPPS.SSU2 was not influenced by the herbivore treatment. Heterologous expression and biochemical characterization of recombinant PtFPPS1, PtGPPS1.LSU, and PtGPPS2.LSU confirmed their respective IDS activities. Recombinant PtGPPS.SSU1 and PtGPPS.SSU2, however, had no enzymatic activity on their own, but PtGPPS.SSU1 enhanced the GPP synthase activities of PtGPPS1.LSU and PtGPPS2.LSU in vitro. Altogether, our data suggest that PtGPPS1.LSU and PtGPPS2.LSU in combination with PtGPPS.SSU1 may provide the substrate for herbivory-induced monoterpene formation in P. trichocarpa. The sole FPP synthase PtFPPS1 likely produces FPP for both primary and specialized metabolism in this plant species.

DOI: 10.3390/molecules24132408
PubMed: 31261889
PubMed Central: PMC6651613


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-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in
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-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in
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<term>Animals (MeSH)</term>
<term>Dimethylallyltranstransferase (genetics)</term>
<term>Dimethylallyltranstransferase (metabolism)</term>
<term>Gene Expression Regulation, Enzymologic (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Herbivory (MeSH)</term>
<term>Insecta (physiology)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Populus (chemistry)</term>
<term>Populus (enzymology)</term>
<term>Populus (genetics)</term>
<term>Terpenes (chemistry)</term>
<term>Up-Regulation (MeSH)</term>
<term>Volatile Organic Compounds (chemistry)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux (MeSH)</term>
<term>Composés organiques volatils (composition chimique)</term>
<term>Dimethylallyltransferase (génétique)</term>
<term>Dimethylallyltransferase (métabolisme)</term>
<term>Herbivorie (MeSH)</term>
<term>Insectes (physiologie)</term>
<term>Populus (composition chimique)</term>
<term>Populus (enzymologie)</term>
<term>Populus (génétique)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes codant pour des enzymes (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Régulation positive (MeSH)</term>
<term>Terpènes (composition chimique)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Terpenes</term>
<term>Volatile Organic Compounds</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Dimethylallyltranstransferase</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Dimethylallyltranstransferase</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Composés organiques volatils</term>
<term>Populus</term>
<term>Terpènes</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>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Dimethylallyltransferase</term>
<term>Populus</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Dimethylallyltransferase</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Insectes</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Insecta</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Gene Expression Regulation, Enzymologic</term>
<term>Gene Expression Regulation, Plant</term>
<term>Herbivory</term>
<term>Up-Regulation</term>
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<term>Animaux</term>
<term>Herbivorie</term>
<term>Régulation de l'expression des gènes codant pour des enzymes</term>
<term>Régulation de l'expression des gènes végétaux</term>
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<front>
<div type="abstract" xml:lang="en">In response to insect herbivory, poplar releases a blend of volatiles that plays important roles in plant defense. Although the volatile bouquet is highly complex and comprises several classes of compounds, it is dominated by mono- and sesquiterpenes. The most common precursors for mono- and sesquiterpenes, geranyl diphosphate (GPP) and (
<i>E,E</i>
)-farnesyl diphosphate (FPP), respectively, are in general produced by homodimeric or heterodimeric
<i>trans</i>
-isopentenyl diphosphate synthases (
<i>trans</i>
-IDSs) that belong to the family of prenyltransferases. To understand the molecular basis of herbivory-induced terpene formation in poplar, we investigated the
<i>trans-IDS</i>
gene family in the western balsam poplar
<i>Populus trichocarpa</i>
. Sequence comparisons suggested that this species possesses a single FPP synthase gene (
<i>PtFPPS1</i>
) and four genes encoding two large subunits (
<i>PtGPPS1.LSU</i>
and
<i>PtGPPS2.LSU</i>
) and two small subunits (
<i>PtGPPS.SSU1</i>
and
<i>PtGPPS.SSU2</i>
) of GPP synthases. Transcript accumulation of
<i>PtGPPS1.LSU</i>
and
<i>PtGPPS.SSU1</i>
was significantly upregulated upon leaf herbivory, while the expression of
<i>PtFPPS1</i>
,
<i>PtGPPS2.LSU</i>
, and
<i>PtGPPS.SSU2</i>
was not influenced by the herbivore treatment. Heterologous expression and biochemical characterization of recombinant PtFPPS1, PtGPPS1.LSU, and PtGPPS2.LSU confirmed their respective IDS activities. Recombinant PtGPPS.SSU1 and PtGPPS.SSU2, however, had no enzymatic activity on their own, but PtGPPS.SSU1 enhanced the GPP synthase activities of PtGPPS1.LSU and PtGPPS2.LSU in vitro. Altogether, our data suggest that PtGPPS1.LSU and PtGPPS2.LSU in combination with PtGPPS.SSU1 may provide the substrate for herbivory-induced monoterpene formation in
<i>P. trichocarpa</i>
. The sole FPP synthase PtFPPS1 likely produces FPP for both primary and specialized metabolism in this plant species.</div>
</front>
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<ArticleTitle>Identification and Characterization of
<i>trans</i>
-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in
<i>Populus trichocarpa</i>
.</ArticleTitle>
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<AbstractText>In response to insect herbivory, poplar releases a blend of volatiles that plays important roles in plant defense. Although the volatile bouquet is highly complex and comprises several classes of compounds, it is dominated by mono- and sesquiterpenes. The most common precursors for mono- and sesquiterpenes, geranyl diphosphate (GPP) and (
<i>E,E</i>
)-farnesyl diphosphate (FPP), respectively, are in general produced by homodimeric or heterodimeric
<i>trans</i>
-isopentenyl diphosphate synthases (
<i>trans</i>
-IDSs) that belong to the family of prenyltransferases. To understand the molecular basis of herbivory-induced terpene formation in poplar, we investigated the
<i>trans-IDS</i>
gene family in the western balsam poplar
<i>Populus trichocarpa</i>
. Sequence comparisons suggested that this species possesses a single FPP synthase gene (
<i>PtFPPS1</i>
) and four genes encoding two large subunits (
<i>PtGPPS1.LSU</i>
and
<i>PtGPPS2.LSU</i>
) and two small subunits (
<i>PtGPPS.SSU1</i>
and
<i>PtGPPS.SSU2</i>
) of GPP synthases. Transcript accumulation of
<i>PtGPPS1.LSU</i>
and
<i>PtGPPS.SSU1</i>
was significantly upregulated upon leaf herbivory, while the expression of
<i>PtFPPS1</i>
,
<i>PtGPPS2.LSU</i>
, and
<i>PtGPPS.SSU2</i>
was not influenced by the herbivore treatment. Heterologous expression and biochemical characterization of recombinant PtFPPS1, PtGPPS1.LSU, and PtGPPS2.LSU confirmed their respective IDS activities. Recombinant PtGPPS.SSU1 and PtGPPS.SSU2, however, had no enzymatic activity on their own, but PtGPPS.SSU1 enhanced the GPP synthase activities of PtGPPS1.LSU and PtGPPS2.LSU in vitro. Altogether, our data suggest that PtGPPS1.LSU and PtGPPS2.LSU in combination with PtGPPS.SSU1 may provide the substrate for herbivory-induced monoterpene formation in
<i>P. trichocarpa</i>
. The sole FPP synthase PtFPPS1 likely produces FPP for both primary and specialized metabolism in this plant species.</AbstractText>
</Abstract>
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<LastName>Lackus</LastName>
<ForeName>Nathalie D</ForeName>
<Initials>ND</Initials>
<AffiliationInfo>
<Affiliation>Max Planck Institute for Chemical Ecology, Department of Biochemistry, Hans-Knöll-Strasse 8, 07745 Jena, Germany.</Affiliation>
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