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Plant Cell


Title:Specific decorations of 17-hydroxygeranyllinalool diterpene glycosides solve the autotoxicity problem of chemical defense in Nicotiana attenuata
Author(s):Heiling S; Llorca LC; Li J; Gase K; Schmidt A; Schafer M; Schneider B; Halitschke R; Gaquerel E; Baldwin IT;
Address:"Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Research Group Biosynthesis/NMR, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany. Centre for Organismal Studies Heidelberg, 69120 Heidelberg, Germany. Institut de Biologie Moleculaire des Plantes, CNRS UPR 2357 Universite de Strasbourg, 67084 Strasbourg, France"
Journal Title:Plant Cell
Year:2021
Volume:33
Issue:5
Page Number:1748 - 1770
DOI: 10.1093/plcell/koab048
ISSN/ISBN:1532-298X (Electronic) 1040-4651 (Print) 1040-4651 (Linking)
Abstract:"The native diploid tobacco Nicotiana attenuata produces abundant, potent anti-herbivore defense metabolites known as 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs) whose glycosylation and malonylation biosynthetic steps are regulated by jasmonate signaling. To characterize the biosynthetic pathway of HGL-DTGs, we conducted a genome-wide analysis of uridine diphosphate glycosyltransferases (UGTs) and identified 107 family-1 UGT members. The transcript levels of three UGTs were highly correlated with the transcript levels two key HGL-DTG biosynthetic genes: geranylgeranyl diphosphate synthase (NaGGPPS) and geranyllinalool synthase (NaGLS). NaGLS's role in HGL-DTG biosynthesis was confirmed by virus-induced gene silencing. Silencing the Uridine diphosphate (UDP)-rhamnosyltransferase gene UGT91T1 demonstrated its role in the rhamnosylation of HGL-DTGs. In vitro enzyme assays revealed that UGT74P3 and UGT74P4 use UDP-glucose for the glucosylation of 17-hydroxygeranyllinalool (17-HGL) to lyciumoside I. Plants with stable silencing of UGT74P3 and UGT74P5 were severely developmentally deformed, pointing to a phytotoxic effect of the aglycone. The application of synthetic 17-HGL and silencing of the UGTs in HGL-DTG-free plants confirmed this phytotoxic effect. Feeding assays with tobacco hornworm (Manduca sexta) larvae revealed the defensive functions of the glucosylation and rhamnosylation steps in HGL-DTG biosynthesis. Glucosylation of 17-HGL is therefore a critical step that contributes to the resulting metabolites' defensive function and solves the autotoxicity problem of this potent chemical defense"
Keywords:Acyclic Monoterpenes/chemistry/*metabolism Animals Biosynthetic Pathways Diterpenes/*metabolism Gene Silencing Glycosides/*metabolism Glycosylation Glycosyltransferases/metabolism Herbivory Larva/physiology Manduca/physiology Metabolomics Necrosis Plant L;
Notes:"MedlineHeiling, Sven Llorca, Lucas Cortes Li, Jiancai Gase, Klaus Schmidt, Axel Schafer, Martin Schneider, Bernd Halitschke, Rayko Gaquerel, Emmanuel Baldwin, Ian Thomas eng ERC_/European Research Council/International Research Support, Non-U.S. Gov't England 2021/02/10 Plant Cell. 2021 Jul 2; 33(5):1748-1770. doi: 10.1093/plcell/koab048"

 
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