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Recruitment of entomopathogenic nematodes by insect-damaged maize roots

Nature volume 434, pages 732–737 (2005)Cite this article

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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References

  1. Karban, R. & Baldwin, I. Induced Responses to Herbivory (Univ. Press Chicago, Chicago, 1997)

    Book  Google Scholar 

  2. Agrawal, A. A., Tuzun, S. & Bent, E. Induced Plant Defenses Against Pathogens and Herbivores (APS Press, St Paul, Minnesota, 1999)

    Google Scholar 

  3. Dicke, M. & Sabelis, M. W. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38, 148–165 (1988)

    Article  Google Scholar 

  4. Turlings, T. C. J., Tumlinson, J. H. & Lewis, W. J. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251–1253 (1990)

    Article  ADS  CAS  Google Scholar 

  5. De Moraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T. & Tumlinson, J. H. Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–573 (1998)

    Article  ADS  CAS  Google Scholar 

  6. Thaler, J. S. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399, 686–688 (1999)

    Article  ADS  CAS  Google Scholar 

  7. Kessler, A. & Baldwin, I. T. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141–2144 (2001)

    Article  ADS  CAS  Google Scholar 

  8. Khan, Z. R. et al. Intercropping increases parasitism of pests. Nature 388, 631–632 (1997)

    Article  ADS  CAS  Google Scholar 

  9. Boff, M. I. C., Zoon, F. C. & Smits, P. H. Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomol. Exp. Appl. 98, 329–337 (2001)

    Article  Google Scholar 

  10. van Tol, R. W. H. M. et al. Plants protect their roots by alerting the enemies of grubs. Ecol. Lett. 4, 292–294 (2001)

    Article  Google Scholar 

  11. Osteen, C. in Agricultural Resources and Environmental Indicators, 2003 (ed. Heimlich, R.) 1–44 (Economic Research Service, Washington DC, 2003)

    Google Scholar 

  12. Krysan, J. L. & Miller, T. A. Methods for the Study of the Pest Diabrotica (Springer, New York, 1986)

    Book  Google Scholar 

  13. Kuhlmann, U. & van der Burgt, W. A. C. M. Possibilities for biological control of the western corn rootworm, Diabrotica virgifera virgifera LeConte, in Central Europe. BioControl 19, 59N–68N (1998)

    Google Scholar 

  14. Kaya, H. K. & Gaugler, R. Entomopathogenic nematodes. Annu. Rev. Entomol. 38, 181–206 (1993)

    Article  Google Scholar 

  15. Gaugler, R. Ecological considerations in the biological-control of soil-inhabiting insects with entomopathogenic nematodes. Agric. Ecosyst. Environ. 24, 351–360 (1988)

    Article  Google Scholar 

  16. Turlings, T. C. J., Lengwiler, U. B., Bernasconi, M. L. & Wechsler, D. Timing of induced volatile emissions in maize seedlings. Planta 207, 146–152 (1998)

    Article  CAS  Google Scholar 

  17. Gouinguene, S., Degen, T. & Turlings, T. C. J. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11, 9–16 (2001)

    Article  CAS  Google Scholar 

  18. Degen, T., Dillmann, C., Marion-Poll, F. & Turlings, T. C. J. High genetic variability in herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol. 135, 1928–1938 (2004)

    Article  CAS  Google Scholar 

  19. Fedoroff, N. V. Prehistoric GM corn. Science 302, 1158–1159 (2003)

    Article  CAS  Google Scholar 

  20. Jaenicke-Despres, V. et al. Early allelic selection in maize as revealed by ancient DNA. Science 302, 1206–1208 (2003)

    Article  ADS  CAS  Google Scholar 

  21. Hammack, L. Single and blended maize volatiles as attractants for diabroticite corn rootworm beetles. J. Chem. Ecol. 27, 1373–1390 (2001)

    Article  CAS  Google Scholar 

  22. O'Halloran, D. M. & Burnell, A. M. An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora . Parasitology 127, 375–385 (2003)

    Article  CAS  Google Scholar 

  23. Grewal, P. S., Lewis, E. E., Gaugler, R. & Campbell, J. F. Host finding behavior as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology 108, 207–215 (1994)

    Article  Google Scholar 

  24. Grewal, P. S., Lewis, E. E. & Gaugler, R. Response of infective stage parasites (Nematoda: Steinernematidae) to volatile cues from infected hosts. J. Chem. Ecol. 23, 503–515 (1997)

    Article  CAS  Google Scholar 

  25. Lewis, E. E., Gaugler, R. & Harrison, R. Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Can. J. Zool. 71, 765–769 (1993)

    Article  Google Scholar 

  26. Lewis, E. E., Grewal, P. S. & Gaugler, R. Hierarchical order of host cues in parasite foraging strategies. Parasitology 110, 207–213 (1995)

    Article  Google Scholar 

  27. Sotelo, A. in Functionality of Food Phytochemicals (eds Jones, T. & Romeo, J.) 89–111 (Plenum, New York, 1997)

    Book  Google Scholar 

  28. Baufeld, P. & Enzian, S. in Western Corn Rootworm: Ecology and Management (eds Vidal, S., Kuhlmann, U. & Edwards, C. R.) 285–302 (CABI, Wallingford, 2005)

    Book  Google Scholar 

  29. Journey, A. M. & Ostlie, K. R. Biological control of the western corn rootworm (Coleoptera: Chrysomelidae) using the entomopathogenic nematode, Steinernema carpocapsae . Environ. Entomol. 29, 822–831 (2000)

    Article  Google Scholar 

  30. Levine, E. & Oloumisadeghi, H. Management of diabroticite rootworms in corn. Annu. Rev. Entomol. 36, 229–255 (1991)

    Article  Google Scholar 

  31. Poinar, G. O., Evans, J. S. & Schuster, E. Field test of the entomogenous nematode, Neoaplectana carpocapsae, for control of corn-rootworm larvae (Diabrotica sp., Coleoptera). Protection Ecol. 5, 337–342 (1983)

    Google Scholar 

  32. Ellsbury, M. M., Jackson, J. J., Woodson, W. D., Beck, D. L. & Stange, K. A. Efficacy, application distribution, and concentration by stemflow of Steinernema carpocapsae (Rhabditida: Steinernematidae) suspensions applied with a lateral-move irrigation system for corn rootworm (Coleoptera: Chrysomelidae) control in maize. J. Econ. Entomol. 89, 74–81 (1996)

    Article  Google Scholar 

  33. Jackson, J. J. Field performance of entomopathogenic nematodes for suppression of western corn rootworm (Coleoptera: Chrysomelidae). J. Econ. Entomol. 89, 366–372 (1996)

    Article  Google Scholar 

  34. van der Putten, W. H., Vet, L. E. M., Harvey, J. A. & Waeckers, F. L. Linking above- and belowground multitrophic interactions. Trends Ecol. Evol. 16, 547–554 (2001)

    Article  Google Scholar 

  35. Wardle, D. A. et al. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633 (2004)

    Article  ADS  CAS  Google Scholar 

  36. Hass, B., Griffin, C. T. & Downes, M. J. Persistence of Heterorhabditis infective juveniles in soil: Comparison of extraction and infectivity measurements. J. Nematol. 31, 508–516 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Curran, J. Influence of application method and pest population-size on the field efficacy of entomopathogenic nematodes. J. Nematol. 24, 631–636 (1992)

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Turlings, T. C. J., Davison, A. C. & Tamo, C. A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol. Entomol. 29, 45–55 (2004)

    Article  Google Scholar 

  39. Köllner, T. G., Schnee, C., Gershenzon, J. & Degenhardt, J. The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65, 1895–1902 (2004)

    Article  Google Scholar 

  40. König, W. A., Bulow, N. & Saritas, Y. Identification of sesquiterpene hydrocarbons by gas phase analytical methods. Flav. Fragr. J. 14, 367–378 (1999)

    Article  Google Scholar 

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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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Authors and Affiliations

  1. University of Neuchâtel, Institute of Zoology, Laboratory of Animal Ecology and Entomology, CP 2, CH-2007, Neuchâtel, Switzerland

    Sergio Rasmann, Ivan Hiltpold & Ted C. J. Turlings

  2. Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany

    Tobias G. Köllner, Jörg Degenhardt & Jonathan Gershenzon

  3. CABI Bioscience Switzerland Centre, Rue des Grillons 1, 2800, Delémont, Switzerland

    Stefan Toepfer & Ulrich Kuhlmann

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  1. Sergio Rasmann
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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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