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)-β-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)-β-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)-β-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.

The sesquiterpene (E)-β-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)-β-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)-β-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)-β-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)-β-caryophyllene production. We argue that the (E)-β-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.

When attacked by herbivorous insects, plants emit volatile compounds that attract natural enemies of the insects. It has been proposed that these volatile signals can be manipulated to improve crop protection. Here, we demonstrate the full potential of this strategy by restoring the emission of a specific belowground signal emitted by insect-damaged maize roots. The western corn rootworm induces the roots of many maize varieties to emit ( E )-β-caryophyllene, which attracts entomopathogenic nematodes that infect and kill the voracious root pest. However, most North American maize varieties have lost the ability to emit ( E )-β-caryophyllene and may therefore receive little protection from the nematodes. To restore the signal, a nonemitting maize line was transformed with a ( E )-β-caryophyllene synthase gene from oregano, resulting in constitutive emissions of this sesquiterpene. In rootworm-infested field plots in which nematodes were released, the ( E )-β-caryophyllene-emitting plants suffered significantly less root damage and had 60% fewer adult beetles emerge than untransformed, nonemitting lines. This demonstration that plant volatile emissions can be manipulated to enhance the effectiveness of biological control agents opens the way for novel and ecologically sound strategies to fight a variety of insect pests.

The emphasis of this review is on the use and potential of entomopathogenic nematodes (EPNs) as biological control agents in sustainable food production across a wide range of agricultural and other commodities. To aid with the understanding of the potential of EPNs in sustainable food production, this review also provides overviews on EPN biology and ecology, mass production and application technology, and interactions with other management tools. First discovered in the 1920s, their commercialization as biopesticides in the 1980s was accompanied and followed by an exponential growth in research on their application, biology, and ecology, followed by a further expansion in more basic research areas since the mid-2000s. This review summarizes significant progress made in the research and application of EPN in insect pest management in important food crops including orchards, small fruit, maize, vegetables, tuber crops, greenhouses, and mushrooms. Significant factors affecting the success of EPN commercialization are also discussed. A growing interest in alternatives to synthetic insecticides and in organic agriculture opens opportunities for EPNs, but EPNs will need to be further improved with respect to efficacy, reduced costs, and ease of use. Moreover, their potential to recycle in host populations beckons to be further exploited for long term pest suppression.