Hiltpold, Ivan

2008, Kollner, Tobias G, Held, Matthias, Lenk, Claudia, Hiltpold, Ivan, Turlings, Ted, Gershenzon, Jonathan, Degenhardt, Joerg

The sesquiterpene (E)-beta-caryophyllene is emitted by maize (Zea mays) leaves in response to attack by lepidopteran larvae like Spodoptera littoralis and released from roots after damage by larvae of the coleopteran Diabrotica virgifera virgifera. We identified a maize terpene synthase, Terpene Synthase 23 (TPS23), that produces (E)-beta-caryophyllene from farnesyl diphosphate. The expression of TPS23 is controlled at the transcript level and induced independently by D. v. virgifera damage in roots and S. littoralis damage in leaves. We demonstrate that (E)-beta-caryophyllene can attract natural enemies of both herbivores: entomopathogenic nematodes below ground and parasitic wasps, after an initial learning experience, above ground. The biochemical properties of TPS23 are similar to those of (E)-beta-caryophyllene synthases from dicotyledons but are the result of repeated evolution. The sequence of TPS23 is maintained by positive selection in maize and its closest wild relatives, teosinte (Zea sp) species. The gene encoding TPS23 is active in teosinte species and European maize lines, but decreased transcription in most North American lines resulted in the loss of (E)-beta-caryophyllene production. We argue that the (E)-beta-caryophyllene defense signal was lost during breeding of the North American lines and that its restoration might help to increase the resistance of these lines against agronomically important pests.

2008, Hiltpold, Ivan, Turlings, Ted

Maize roots respond to feeding by larvae of the beetle Diabrotica virgifera virgifera by releasing (E)-beta-caryophyllene. This sesquiterpene, which is not found in healthy maize roots, attracts the entomopathogenic nematode Heterorhabditis megidis. In sharp contrast to the emission of virtually only this single compound by damaged roots, maize leaves emit a blend of numerous volatile organic compounds in response to herbivory. To try to explain this difference between roots and leaves, we studied the diffusion properties of various maize volatiles in sand and soil. The best diffusing compounds were found to be terpenes. Only one other sesquiterpene known for maize, alpha-copaene, diffused better than (E)-beta-caryophyllene, but biosynthesis of the former is far more costly for the plant than the latter. The diffusion of (E)-beta-caryophyllene occurs through the gaseous rather than the aqueous phase, as it was found to diffuse faster and further at low moisture level. However, a water layer is needed to prevent complete loss through vertical diffusion, as was found for totally dry sand. Hence, it appears that maize has adapted to emit a readily diffusing and cost-effective belowground signal from its insect-damaged roots.