Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E )-b-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E )-b-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-b-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.Plants are not simply passive victims of attacking herbivores; they have evolved an arsenal of physical and chemical defences to protect themselves. Often these defences are mobilized only in response to herbivory 1,2 . Among the proposed inducible defences is the production and release of volatile chemicals that could serve as signals to attract natural enemies of the herbivores [3][4][5] . Manipulating these signals can help increase the effectiveness of these natural enemies as control agents [6][7][8] . The induced emission of chemical signals is not limited solely to aboveground plant parts. The entomopathogenic nematode Heterorhabditis megidis was found to be attracted to exudates emitted by plant roots after damage by weevil larvae 9,10 , but the nature of the attractants involved is unknown. Here we show that maize roots damaged by larvae of the economically important coleopteran pest Diabrotica virgifera virgifera LeConte are attractive to entomopathogenic nematodes, and we identify the chemical compound responsible for the attraction. D. v. virgifera or Western corn rootworm (WCR) is a voracious pest of maize that is responsible for the use of the bulk of pesticides applied in the cultivation of this crop in the USA 11 . The recent introduction and rapid spread of WCR into Europe has caused major concern for maize production on this continent and has stimulated the search for new methods of maize protection 12,13 . The use of nematodes to control WCR is an ecologically sound option 14,15 , especially if researchers can optimize their efficacy at finding and killing WCR. Attraction of nematodes by WCR-damaged rootsTo determine whether or not WCR-infested maiz...
Plants can defend themselves against herbivores by attracting natural enemies of the herbivores. The cues for attraction are often complex mixtures of herbivore-induced plant volatiles, making it difficult to demonstrate the role of specific compounds. After herbivory by lepidopteran larvae, maize releases a mixture of volatiles that is highly attractive to females of various parasitic wasp species. We identified the terpene synthase TPS10 that forms (E)--farnesene, (E)-␣-bergamotene, and other herbivory-induced sesquiterpene hydrocarbons from the substrate farnesyl diphosphate. The corresponding gene is expressed in response to herbivore attack and is regulated at the transcript level. Overexpression of tps10 in Arabidopsis thaliana resulted in plants emitting high quantities of TPS10 sesquiterpene products identical to those released by maize. Using these transgenic Arabidopsis plants as odor sources in olfactometer assays showed that females of the parasitoid Cotesia marginiventris learn to exploit the TPS10 sesquiterpenes to locate their lepidopteran hosts after prior exposure to these volatiles in association with hosts. This dissection of the herbivore-induced volatile blend demonstrates that a single gene such as tps10 can be sufficient to mediate the indirect defense of maize against herbivore attack.parasitoid attraction ͉ plant defense signal ͉ terpene biosynthesis ͉ volatile terpenes I n the last two decades, researchers have frequently observed that herbivore damage to certain plants induces the emission of volatile organic compounds that attract natural enemies of the herbivores. Termed ''indirect defense,'' this phenomenon has been reported in Ͼ15 different plant species to date (1-4). For example, after damage by lepidopteran larvae to maize foliage, the plant releases a complex mixture of volatiles containing a large number of mono-and sesquiterpenes, lipoxygenase pathway products, and indole (5), with the mixture varying among cultivars and between maize and related species of the Poaceae (6, 7). The high number of compounds that make up this and other herbivore-induced volatile mixtures has so far impeded the identification of the compound(s) actually responsible for signaling herbivore enemies. Attempts to dissect the volatile signal emitted by herbivore-damaged leaves of lima bean (1) and maize (8), for instance, could not identify a specific compound responsible for enemy attraction, suggesting that mixtures constitute the active signal. However, the application of individual plant volatiles, such as methyl salicylate and the sesquiterpene alcohol nerolidol, in behavioral assays have been occasionally reported to attract parasitoids (9) and predatory mites (10-12).The volatile signal emitted by maize seedlings after attack by lepidopteran larvae attracts females of the parasitic braconid wasp Cotesia marginiventris (Hymenoptera), which oviposit in the larvae (5). To determine the role of specific volatiles in attracting C. marginiventris, we sought to learn more about the regulation of vola...
The sesquiterpene (E)-b-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)-b-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)-b-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)-b-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)-b-caryophyllene production. We argue that the (E)-b-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.
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