title: Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory.
abstract: Secondary metabolites are major constituents of plant defense against herbivore attack. Relatively little is known about the cell type-specific formation and antiherbivore activities of secondary compounds in roots despite the substantial impact of root herbivory on plant performance and fitness. Here, we describe the constitutive formation of semivolatile diterpenes called rhizathalenes by the class I terpene synthase (TPS) 08 in roots of Arabidopsis thaliana. The primary enzymatic product of TPS08, rhizathalene A, which is produced from the substrate all-trans geranylgeranyl diphosphate, represents a so far unidentified class of tricyclic diterpene carbon skeletons with an unusual tricyclic spiro-hydrindane structure. Protein targeting and administration of stable isotope precursors indicate that rhizathalenes are biosynthesized in root leucoplasts. TPS08 expression is largely localized to the root stele, suggesting a centric and gradual release of its diterpene products into the peripheral root cell layers. We demonstrate that roots of Arabidopsis tps08 mutant plants, grown aeroponically and in potting substrate, are more susceptible to herbivory by the opportunistic root herbivore fungus gnat (Bradysia spp) and suffer substantial removal of peripheral tissue at larval feeding sites. Our work provides evidence for the in vivo role of semivolatile diterpene metabolites as local antifeedants in belowground direct defense against root-feeding insects.
authors.affiliation: Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061, USA.
authors.forename: Martha M
authors.initials: MM
authors.lastname: Vaughan
authors.forename: Qiang
authors.initials: Q
authors.lastname: Wang
authors.forename: Francis X
authors.initials: FX
authors.lastname: Webster
authors.forename: Dave
authors.initials: D
authors.lastname: Kiemle
authors.forename: Young J
authors.initials: YJ
authors.lastname: Hong
authors.forename: Dean J
authors.initials: DJ
authors.lastname: Tantillo
authors.forename: Robert M
authors.initials: RM
authors.lastname: Coates
authors.forename: Austin T
authors.initials: AT
authors.lastname: Wray
authors.forename: Whitnee
authors.initials: W
authors.lastname: Askew
authors.forename: Christopher
authors.initials: C
authors.lastname: O'Donnell
authors.forename: James G
authors.initials: JG
authors.lastname: Tokuhisa
authors.forename: Dorothea
authors.initials: D
authors.lastname: Tholl
mesh_terms: D019883:Alkyl and Aryl Transferases / Q000737:chemistry*; D000818:Animals; D017360:Arabidopsis / Q000737:chemistry / Q000187:drug effects / Q000201:enzymology* / Q000502:physiology; D061245:Axenic Culture; D003517:Cyclopentanes / Q000494:pharmacology; D004175:Diptera / Q000502:physiology; D004224:Diterpenes / Q000737:chemistry* / Q000276:immunology / Q000302:isolation & purification; D060434:Herbivory / Q000502:physiology*; D007814:Larva / Q000502:physiology; D015394:Molecular Structure; D054883:Oxylipins / Q000494:pharmacology; D059828:Plant Cells / Q000737:chemistry / Q000201:enzymology; D057865:Plant Immunity; D018517:Plant Roots / Q000737:chemistry / Q000201:enzymology*; D018087:Plastids / Q000737:chemistry; D011106:Polyisoprenyl Phosphates / Q000737:chemistry; D013141:Spiro Compounds / Q000737:chemistry* / Q000276:immunology / Q000302:isolation & purification; D055549:Volatile Organic Compounds / Q000737:chemistry
chemical_list: D003517:Cyclopentanes; D004224:Diterpenes; D054883:Oxylipins; D011106:Polyisoprenyl Phosphates; D013141:Spiro Compounds; D055549:Volatile Organic Compounds; C011006:jasmonic acid; D019883:Alkyl and Aryl Transferases; C108877:terpene synthase; C002963:geranylgeranyl pyrophosphate