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Nature Research, Nature, 7034(434), p. 732-737, 2005

DOI: 10.1038/nature03451

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Recruitment of entomopathogenic nematodes by insect-damaged maize roots

This paper is made freely available by the publisher.
This paper is made freely available by the publisher.

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Abstract

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 3–5 . Manipulating these signals can help increase the effectiveness of these natural enemies as control agents 6–8 . 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 attrac-tion. 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.