Mycorrhiza changes plant volatiles to attract spider mite enemies

Functional Ecology

Volumn 26, Issue 2, 2012, Pages 441-449

  Schausberger, Peter ^a   Peneder, Stefan ^a   Jürschik, Simone ^b   Hoffmann, Daniela ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b IONICON Analytik GmbH   (Austria)

Author keywords

Arbuscular mycorrhiza; Herbivore induced plant volatiles; Induced plant defence; Multi trophic interaction; Predatory mites

Indexed keywords

ARBUSCULAR MYCORRHIZA; BIOLOGICAL CONTROL; CARNIVORE; CHEMICAL COMPOSITION; FUNGUS; LEGUME; MASS SPECTROMETRY; MITE; MUTUALISM; NATURAL ENEMY; OLFACTORY CUE; PARASITE INFESTATION; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; TROPHIC INTERACTION; VOLATILE ORGANIC COMPOUND;

ACARI; ARANEAE; ARBUSCULAR; FUNGI; GLOMUS MOSSEAE; PHASEOLUS VULGARIS; PHYTOSEIULUS PERSIMILIS; TETRANYCHIDAE; TETRANYCHUS URTICAE;

EID: 84859069716     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01947.x     Document Type: Article

References (47)

1. Bennett, A.E., Alers-Garcia, J. & Bever, J.D. (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. American Naturalist, 167, 141-152.
2. Bezemer, M. & van Dam, N.M. (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends in Ecology and Evolution, 20, 617-624.
3. Bostock, R.M., Karban, R., Thaler, J.S., Weyman, P.D. & Gilchrist, D. (2002) Signal interactions in induced resistance to pathogens and insect herbivores. European Journal of Plant Pathology, 107, 103-111.
4. Choh, Y. & Takabayashi, J. (2006) Intact lima bean plants exposed to herbivore-induced plant volatiles attract predatory mites and spider mites at different levels according to plant parts. Applied Entomology and Zoology, 42, 537-543.
5. De Boer, J.G., Posthumus, M.A. & Dicke, M. (2004) Identification of volatiles that are used in discrimination between plants infested with prey or non-prey herbivores by a predatory mite. Journal of Chemical Ecology, 30, 2215-2230.
6. De Boer, J.G., Hordijk, C.A., Posthumus, M.A. & Dicke, M. (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. Journal of Chemical Ecology, 34, 281-290.
7. Dicke, M. & Vet, L.E.M. (1999) Plant-carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore. Herbivores. Between Plants and Predators (eds H. Olff, V.K. Brown & R.H. Drent ), pp. 483-520. Blackwell Science, Oxford.
8. Dicke, M., van Beek, T.A., Posthumus, M.A., Ben Dom, N., van Bokhoven, H. & de Groot, A.E. (1990) Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. Journal of Chemical Ecology, 16, 381-396.
9. Erb, M., Ton, J., Degenhardt, J. & Turlings, T.C.J. (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiology, 146, 867-874.
10. Fontana, A., Reichelt, M., Hempel, S., Gershenzon, J. & Unsicker, S.B. (2009) The effects of arbuscular myccorhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. Journal of Chemical Ecology, 35, 833-843.
11. Gehring, C.A. & Whitham, T.G. (2002) Mycorrhizae-herbivore interactions: population and community consequences. Mycorrhizal Ecology (eds M.G.A. van der Heijden & I.R. Sanders ), pp. 295-320. Springer, Berlin.
12. Giovannetti, M. & Mosse, B. (1980) An evaluation of techniques for measuring vesicular arbuscular infection in roots. New Phytologist, 84, 489-500.
13. Guerreri, E., Lingua, G., Digilio, M.C., Massa, N. & Berta, G. (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecological Entomology, 29, 753-756.
14. Hardin, J.W. & Hilbe, J.M. (2003) Generalized Estimating Equations. Chapman & Hall/CRC, Boca Raton, FL, USA.
15. Hare, J.D. (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology, 56, 161-180.
16. Hoeksema, J.D., Chaudhary, V.B., Gehring, C.A., Collins Johnson, N., Karst, J., Koide, R.T., Pringle, A., Zabinski, C., Bever, J.D., Moore, J.C., Wilson, G.W.T., Klironomos, J.N. & Umbanhowar, J. (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters, 13, 394-407.
17. Hoffmann, D., Vierheilig, H. & Schausberger, P. (2011a) Mycorrhiza-induced trophic cascade enhances fitness and population growth of an acarine predator. Oecologia, 166, 141-149.
18. Hoffmann, D., Vierheilig, H. & Schausberger, P. (2011b) Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey-related cues. Physiological Entomology, 36, 90-95.
19. Hoffmann, D., Vierheilig, H., Riegler, P. & Schausberger, P. (2009) Arbuscular mycorrhizal symbiosis increases host plant acceptance and population growth rates of the two-spotted spider mite Tetranychus urticae. Oecologia, 158, 663-671.
20. Hoffmann, D., Vierheilig, H., Peneder, S. & Schausberger, P. (2011) Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant. Ecological Entomology, 36, 574-581.
21. Horiuchi, J., Prithiviraj, B., Bais, H.P., Kimball, B.A. & Vivanco, J.M. (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta, 222, 848-857.
22. Isobe, K. & Tsuboki, Y. (1999) Study on the utilization of arbuscular mycorrhizal fungi in kidney bean cultivation - differences in kidney bean growth resulting from the infection of six species of arbuscular mycorrhizal fungi. Japanese Journal of Crop Science, 68, 112-117.
23. Jordan, A., Haidacher, S., Hanel, G., Hartungen, E., Märk, L., Seehauser, H., Schottkowsky, R., Sulzer, P. & Märk, T.D. (2009) A high resolution and high sensitivity proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS). International Journal of Mass Spectrometry, 286, 122-128.
24. Karban, R. & Baldwin, I. (1997) Induced Responses to Herbivory. Chicago University Press, Chicago.
25. Leitner, M., Kaiser, R., Hause, B., Boland, W. & Mithöfer, A. (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza, 20, 89-101.
26. McMurtry, J.A. & Scriven, G.T. (1965) Insectary production of phytoseiid mites. Journal of Economic Entomology, 58, 282-283.
27. Nachappa, P., Margolies, D.C., Nechols, J.R. & Loughin, T. (2006) Phytoseiulus persimilis response to herbivore-induced plant volatiles as a function of mite-days. Experimental and Applied Acarology, 40, 231-239.
28. Paré, P.W. & Tumlinson, J.H. (1999) Plant volatiles as a defense against herbivores. Plant Physiology, 121, 325-331.
29. Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N. & Weis, A.E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics, 11, 41-65.
30. Rapparini, F., Llusià, J. & Peňuelas, J. (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biology, 10, 108-122.
31. Rasmann, S. & Turlings, T.C.J. (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecology Letters, 10, 926-936.
32. Rasmann, S., Kollner, T.G., Degenhardt, J., Hiltpolt, I., Toepfer, S., Kuhlmann, U., Gershenzon, J. & Turlings, T.C.J. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature, 434, 732-737.
33. Sabelis, M.W. & van de Baan, H.E. (1983) Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomologia Experimentalis et Applicata, 33, 303-314.
34. Sabelis, M.W., van Baalen, M., Bakker, F.M., Bruin, J., Drukker, B., Egas, M., Janssen, A.R.M., Lesna, I.K., Pels, B., van Rijn, P.C.J. & Scutareanu, P. (1999) The evolution of direct and indirect plant defence against herbivorous arthropods. Herbivores. Between Plants and Predators (eds H. Olff, V.K. Brown & R.H. Drent ), pp. 109-166. Blackwell Science, Oxford.
35. Schausberger, P. (1997) Inter- and intraspecific predation on immatures by adult females in Euseius finlandicus, Typhlodromus pyri and Kampimodromus aberrans. Experimental and Applied Acarology, 21, 131-150.
36. Schmelz, E.A., Alborn, H.T. & Tumlinson, J.H. (2003) Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiologia Plantarum, 117, 403-412.
37. Smith, S.E. & Read, D.J. (2008) Mycorrhizal Symbiosis, 3rd edn. Elsevier, New York.
38. Soler, R., Harvey, J.A., Kamp, A.F.D., Vet, L.E.M., van der Putten, W.H., van Dam, N., Stuefer, J.F., Gols, R., Hordijk, C.A. & Bezemer, T.M. (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos, 116, 367-376.
39. Thaler, J.S., Fidantsef, A.L., Duffey, S.S. & Bostock, R.M. (1999) Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. Journal of Chemical Ecology, 25, 1597-1609.
40. Thaler, J.S., Karban, R., Ullman, D.E., Boege, K. & Bostock, R.M. (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia, 131, 227-235.
41. Van der Putten, W.H., Vet, L.E.M., Harvey, J.A. & Wäckers, F. (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens and their antagonists. Trends in Ecology and Evolution, 16, 547-554.
42. Van Oosten, V.R., Bodenhausen, N., Reymond, P., van Pelt, J.A., van Loon, J.C., Dicke, M. & Pieterse, C.M.J. (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 21, 919-930.
43. Vierheilig, H., Coughlan, A.P., Wyss, U. & Piché, Y. (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology, 64, 5004-5007.
44. Walters, D. & Heil, M. (2007) Costs and trade-offs associated with induced resistance. Physiological and Molecular Plant Pathology, 71, 3-17.
45. Wenke, K., Kai, M. & Piechulla, B. (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta, 231, 499-506.
46. Williams, L. III, Rodriguez-Saona, C., Paré, P.W. & Crafts-Brandner, S.J. (2005) The piercing-sucking herbivores Lygus hesperus and Nezara viridula induce volatile emissions in plants. Archives of Insect Biochemistry and Physiology, 58, 84-96.
47. Zhang, P.-J., Zheng, S.-J., van Loon, J.J.A., Boland, W., David, A., Mumm, R. & Dicke, M. (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proceedings of the National Academy of Sciences of the United States of America, 106, 21202-21207.