Location: Chemistry ResearchTitle: 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 ) Author
Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/4/2013
Publication Date: 3/31/2012
Citation: Vaughan, M.M., Webster, F.X., Kiemle, D., Hong, Y.J., Tantillo, D.J., Wang, Q., Coates, R.M., Wray, A.T., Askew, W., O'Donnell, C., Tokuhisa, J.G., Tholl, D. 2012. 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 . The Plant Cell. 1-18. Interpretive Summary: Root herbivores are among the most destructive agricultural pests and are even capable of influencing the abundance, diversity and succession of natural ecosystems. Despite the significant impact of root herbivory on plant growth and survival, relatively little is known about the defensive compounds or secondary metabolites in roots. Scientists at the USDA-ARS Center for Medical, Agricultural and Veterinary Entomology in Gainesville, Florida in collaboration with the University of Virginia Tech have identified a previously un-described class of diterpene carbon skeletons, called rhizathalenes, which have an unusual tricyclic spiro-hydrindane structure. These unique semivolatile diterpenes are formed by the class I terpenesythase TPS08 in the roots of Arabidopsis thaliana in the mustard family. Experiments with protein targeting and labeled precursors indicated that the rhizathalenes are synthesized in the leucoplast of the root cells. TPS08 expression is restricted to the root tips and central part of the root tissue. Furthermore, Arabidopsis tps08 mutant plants, lacking the formation of rhizathalenes are more susceptible to damage by the root-herbivore Bradysia spp. (fungus gnat). This work describes novel root specific tricyclic diterpene metabolites that function as local antifeedants in belowground direct defense against root-feeding insects. Understanding the defensive potential of plants against root herbivores can be transferred to agricultural applications in an effort to control belowground herbivore damage and reduced the economic losses.
Technical Abstract: Secondary metabolites are major constituents of plant defense against herbivore attack. Relatively little is known about the cell type-specific formation and anti-herbivore 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 TPS08 in roots of Arabidopsis thaliana. The primary enzymatic product of TPS08, rhizathalene A, which is produced from the substrate alltrans GGPP, 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 specifically localized to the root tips and 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 Bradysia spp. (fungus gnat) 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.