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Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus trichocarpa.
Molecules 2019; 24(13)M

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.

Authors+Show Affiliations

Max Planck Institute for Chemical Ecology, Department of Biochemistry, Hans-Knöll-Strasse 8, 07745 Jena, Germany.Max Planck Institute for Chemical Ecology, Department of Biochemistry, Hans-Knöll-Strasse 8, 07745 Jena, Germany.Iowa State University, Roy J. Carver Department of Biochemistry, Biophysics and Molecular Biology, 4254 Molecular Biology Building, 2437 Pammel Drive, Ames, IA 50011, USA.Max Planck Institute for Chemical Ecology, Department of Biochemistry, Hans-Knöll-Strasse 8, 07745 Jena, Germany.Michael Smith Laboratories, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.Max Planck Institute for Chemical Ecology, Department of Biochemistry, Hans-Knöll-Strasse 8, 07745 Jena, Germany.Max Planck Institute for Chemical Ecology, Department of Biochemistry, Hans-Knöll-Strasse 8, 07745 Jena, Germany. koellner@ice.mpg.de.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31261889

Citation

Lackus, Nathalie D., et al. "Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus Trichocarpa." Molecules (Basel, Switzerland), vol. 24, no. 13, 2019.
Lackus ND, Petersen NP, Nagel R, et al. Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus trichocarpa. Molecules. 2019;24(13).
Lackus, N. D., Petersen, N. P., Nagel, R., Schmidt, A., Irmisch, S., Gershenzon, J., & Köllner, T. G. (2019). Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus trichocarpa. Molecules (Basel, Switzerland), 24(13), doi:10.3390/molecules24132408.
Lackus ND, et al. Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus Trichocarpa. Molecules. 2019 Jun 29;24(13) PubMed PMID: 31261889.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Identification and Characterization of trans-Isopentenyl Diphosphate Synthases Involved in Herbivory-Induced Volatile Terpene Formation in Populus trichocarpa. AU - Lackus,Nathalie D, AU - Petersen,Nora P, AU - Nagel,Raimund, AU - Schmidt,Axel, AU - Irmisch,Sandra, AU - Gershenzon,Jonathan, AU - Köllner,Tobias G, Y1 - 2019/06/29/ PY - 2019/05/29/received PY - 2019/06/17/revised PY - 2019/06/26/accepted PY - 2019/7/3/entrez PY - 2019/7/3/pubmed PY - 2019/7/3/medline KW - Lymantria dispar KW - Populus trichocarpa KW - isoprenyl diphosphate synthase KW - monoterpene KW - prenyl transferase KW - sesquiterpene KW - volatile organic compound (VOC) JF - Molecules (Basel, Switzerland) JO - Molecules VL - 24 IS - 13 N2 - 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. SN - 1420-3049 UR - https://www.unboundmedicine.com/medline/citation/31261889/Identification_and_Characterization_of_trans_Isopentenyl_Diphosphate_Synthases_Involved_in_Herbivory_Induced_Volatile_Terpene_Formation_in_Populus_trichocarpa_ L2 - http://www.mdpi.com/resolver?pii=molecules24132408 DB - PRIME DP - Unbound Medicine ER -