Recruitment of entomopathogenic nematodes by insect-damaged maize roots

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)-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.

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Figure 1: Attraction of entomopathogenic nematodes to a WCR-induced root signal.
Figure 2: Attraction of H. megidis to authentic (E)-β-caryophyllene.
Figure 3: The absence of the (E)-β-caryophyllene signal in certain maize genotypes renders these plants unattractive to the nematode.
Figure 4: More WCR larvae were infected with nematodes and fewer adults emerged near Graf plants than near Pactol plants.
Figure 5: Fewer WCR adults emerged near Pactol plants that were spiked with (E)-β-caryophyllene than near Pactol plants that received no (E)-β-caryophyllene.
Figure 6: (E)-β-Caryophyllene diffuses readily through sand and then evaporates rapidly without breakdown or irreversible adsorption.

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Acknowledgements

We thank the members of the group of M. Rahier for their continuous support; and M.-E. Farine for technical assistance; R. Gaugler, J. Tumlinson and R. van Tol for useful feedback; and V. Larraz for rearing the Diabrotica larvae for laboratory experiments. Field sites were provided by the Plant Health Service in Hodmézövásárhely, Hungary. Nematodes were provided, free of charge, by Andermatt Biocontrol AG. The work was supported by the Swiss National Centre of Competence in Research ‘Plant Survival’, the Swiss National Science Foundation, the German National Science Foundation and the Max Planck Society.

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Correspondence to Ted C. J. Turlings.

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Rasmann, S., Köllner, T., Degenhardt, J. et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737 (2005). https://doi.org/10.1038/nature03451

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