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.
Highlights
Plant specialized metabolites provide protection against herbivores by acting as toxins and feeding deterrents and by serving as defensive signals
Our data suggest that PtGPPS1.large subunit (LSU) and PtGPPS2.LSU in combination with PtGPPS.SSU1 may provide the substrate for herbivory-induced monoterpene formation in P. trichocarpa
Molecules 2019, 24, 2408 including terpenes, green leaf volatiles, aromatic compounds, and nitrogen-containing amino acid derivatives [3]. Their qualitative and quantitative composition differs between plant species, herbivory-induced volatile blends are often dominated by monoterpenes and sesquiterpenes [1]
Summary
Plant specialized metabolites provide protection against herbivores by acting as toxins and feeding deterrents and by serving as defensive signals. Molecules 2019, 24, 2408 including terpenes, green leaf volatiles, aromatic compounds, and nitrogen-containing amino acid derivatives [3] Their qualitative and quantitative composition differs between plant species, herbivory-induced volatile blends are often dominated by monoterpenes and sesquiterpenes [1]. IDS enzymes catalyze condensations of the basic C5 terpene building blocks, isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP), to generate C10 , C15 , C20 , and larger prenyl diphosphates [4,7,8] These monoterpene, sesquiterpene, and diterpene precursors, geranyl diphosphate (GPP), (E,E)-farnesyl diphosphate (FPP), and (E,E,E)-geranylgeranyl diphosphate (GGPP), respectively, are produced by short-chain trans-IDS enzymes that are designated as geranyl diphosphate synthases (GPPSs), farnesyl diphosphate synthases (FPPSs), and geranylgeranyl diphosphate synthases (GGPPSs) according to their major product. Analysis of IDS gene expression by RNAseq and quantitative real-time PCR showed that the formation of GPP is likely catalyzed by two GPPSs and increases upon herbivory, while FPP is constitutively produced by a single FPPS in P. trichocarpa leaves
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