Phloem-feeding whiteflies can fool their host plants, but not their parasitoids

Functional Ecology

Volumn 27, Issue 6, 2013, Pages 1304-1312

  Zhang, Peng Jun ^a   Xu, Cai Xia ^b   Zhang, Jin Ming ^a   Lu, Yao Bin ^a   Wei, Jia Ning ^c   Liu, Yin Quan ^d   David, Anja ^e   Boland, Wilhelm ^e   Turlings, Ted C J ^f  

^a INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^c INSTITUTE OF ZOOLOGY   (China)

^d ZHEJIANG UNIVERSITY   (China)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^f UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Bemisia tabaci; Encarsia formosa; Indirect plant defence; Phloem feeding herbivore; Plant herbivore interactions; Salicylic acid

Indexed keywords

EMISSION; FEEDING; HERBIVORE; HOST LOCATION; HOST PLANT; PARASITOID; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; SALICYLIC ACID; WHITEFLY;

ALEYRODIDAE; ARABIDOPSIS; ARABIDOPSIS THALIANA; BEMISIA TABACI; ENCARSIA FORMOSA;

EID: 84887818643     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12132     Document Type: Article

References (56)

1. Ament, K., Kant, M.R., Sabelis, M.W., Haring, M.A. & Schuurink, R.C. (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiology, 135, 2025-2037.
2. Arimura, G.I., Köpke, S., Kunert, M., Volpe, V., David, A., Brand, P., Dabrowska, P., Maffei, M.E. & Boland, W. (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiology, 146, 965-973.
3. Bell, E., Creelman, R.A. & Mullet, J.E. (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences, USA, 92, 8675-8679.
4. Birkett, M.A., Chamberlain, K., Guerrieri, E., Pickett, J.A., Wadhams, J. & Yasuda, T. (2003) Volatiles from whitefly-infested plants elicit a host-locating response in the parasitoid, Encarsia formosa. Journal of Chemical Ecology, 29, 1589-1600.
5. Blande, J.D., Pickett, J.A. & Poppy, G.M. (2007) A comparison of semiochemically mediated interactions involving specialist and generalist Brassica-feeding aphids and the braconid parasitoid Diaeretiella rapae. Journal of Chemical Ecology, 33, 767-779.
6. Bohlmann, J., Martin, D., Oldham, N.J. & Gershenzon, J. (2002) Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization, and functional expression of a myrcene/(E)-β-ocimene synthase. Archives of Biochemistry & Biophysics, 375, 261-269.
7. Bruce, T.J.A., Matthes, M.C., Chamberlain, K., Woodcock, C.M., Mohib, A., Webster, B., Smart, L.E., Birkett, M.A., Pickett, J.A. & Napier, J.A. (2008) cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proceedings of the National Academy of Sciences, USA, 105, 4553-4558.
8. Bruinsma, M., Posthumus, M.A., Mumm, R., Mueller, M.J., van Loon, J.J.A. & Dicke, M. (2009) Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. Journal of Experimental Botany, 60, 2575-2589.
9. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. & Dong, X.N. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. The Plant Cell, 88, 57-63.
10. Clarke, J.D., Liu, Y., Klessig, D.F. & Dong, X.N. (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. The Plant Cell, 10, 557-569.
11. De Boer, J.G., Posthumus, M.A. & Dicke, M. (2004) Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. Journal of Chemical Ecology, 30, 2215-2230.
12. Delaney, T.P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. & Ryals, J. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
13. Dicke, M. (2009) Behavioural and community ecology of plants that cry for help. Plant Cell & Environment, 32, 654-665.
14. 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 - involvement of host plant in its production. Journal of Chemical Ecology, 16, 381-396.
15. Du, Y., Poppy, G.M., Powell, W., Pickett, J.A., Wadhams, L.J. & Woodcock, C.M. (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. Journal of Chemical Ecology, 24, 1355-1368.
16. Engelberth, J., Koch, T., Schüler, G., Bachmann, N., Rechtenbach, J. & Boland, W. (2001) Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiology, 125, 369-377.
17. Erb, M., Meldau, S. & Howe, G.A. (2012) Role of phytohormones in insect-specific plant reactions. Trends in Plant Science, 17, 250-259.
18. Felton, G.W. & Tumlinson, J.H. (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Current Opinion in Plant Biology, 11, 457-463.
19. Girling, R.D., Hassall, M., Turner, J.G. & Poppy, G.M. (2006) Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae. Entomologia Experimental et Applicata, 120, 1-9.
20. Girling, R.D., Madison, R., Hassall, M., Poppy, G.M. & Turner, J.G. (2008) Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles. Journal of Experimental Botany, 59, 3077-3085.
21. Guzman, P. & Ecker, J.R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. The Plant Cell, 2, 513-523.
22. 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.
23. Heil, M., Koch, T., Hilpert, A., Fiala, B., Boland, W. & Linsenmair, K.E. (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proceedings of the National Academy of Sciences, USA, 98, 1083-1088.
24. Hilker, M. & Meiners, T. (2010) How do plants "notice" attack by herbivorous arthropods? Biological Reviews, 85, 267-280.
25. Hoddle, M.S., Van Driesche, R.G. & Sanderson, J.P. (1998) Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology, 43, 645-669.
26. Janssen, A., Sabelis, M.W. & Bruin, J. (2002) Evolution of herbivore-induced plant volatiles. Oikos, 97, 134-138.
27. Jirage, D., Zhou, N., Cooper, B., Clarke, J.D., Dong, X.N. & Glazebrook, J. (2001) Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4. The Plant Journal, 26, 395-407.
28. Kempema, L.A., Cui, X.P., Holzer, F.M. & Walling, L.L. (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology, 143, 849-865.
29. Kessler, A. & Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science, 291, 2141-2144.
30. Kessler, A. & Heil, M. (2011) The multiple faces of indirect defences and their agents of natural selection. Functional Ecology, 25, 348-357.
31. McKenzie, C.L., Anderson, P.K. & Villarreal, N. (2004) An extensive survey of Bemisia tabaci (Homoptera: Aleyrodidae) in agricultural ecosystems in Florida. The Florida Entomologist, 87, 403-407.
32. Moran, P.J. & Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology, 125, 1074-1085.
33. Ozawa, R., Arimura, G., Takabayashi, J., Shimoda, T. & Nishioka, T. (2000) Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant & Cell Physiology, 41, 391-398.
34. Pieterse, C.M.J., van der Does, D., Zamioudis, C., Leon-Reyes, A. & van Wees, S.C.M. (2012) Hormonal modulation of plant immunity. Annual Review of Cell & Developmental Biology, 28, 489-521.
35. Poelman, E.H., Oduor, A.M.O., Broekgaarden, C., Hordijk, C.A., Jansen, J.J., Van Loon, J.J.A., Van Dam, N.M., Vet, L.E.M. & Dicke, M. (2009) Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Functional Ecology, 23, 951-962.
36. 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.
37. Schaller, F., Biesgen, C., Müssig, C., Altmann, T. & Weiler, E.W. (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme invovled in jasmonate biosynthesis. Planta, 210, 979-984.
38. Schmelz, E.A., Alborn, H.T., Banchio, E. & Tumlinson, J.H. (2003) Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta, 216, 665-673.
39. Schulze, B., Lauchli, R., Sonwa, M.M., Schmidt, A. & Boland, W. (2006) Profiling of structurally labile oxylipins in plants by in situ derivatization with pentafluorobenzyl hydroxylamine. Analytical Biochemistry, 348, 269-283.
40. Schuman, M.C., Barthel, K. & Baldwin, I.T. (2012) Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuate in nature. eLife, 1, e00007.
41. Thaler, J.S. (1999) Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature, 399, 686-688.
42. Thaler, J.S., Farag, M.A., Paré, P.W. & Dicke, M. (2002) Jasmonate-deficient plants have reduced direct and indirect defences against herbivores. Ecology Letters, 5, 764-774.
43. Tjallingii, W.F. & Hogen Esch, T. (1993) Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiological Entomology, 18, 317-328.
44. Turlings, T.C.J., Tumlinson, J.H. & Lewis, W.J. (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science, 250, 1251-1253.
45. Van de Ven, W.T.G., LeVesque, C.S., Perring, T.M. & Walling, L.L. (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. The Plant Cell, 12, 1409-1423.
46. Van Poecke, R.M.P. & Dicke, M. (2002) Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. Journal of Experimental Botany, 53, 1793-1799.
47. Von Malek, B., Van der Graaff, E., Schneitz, K. & Keller, B. (2002) The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta, 216, 187-192.
48. Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation, 19, 195-216.
49. Walling, L.L. (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiology, 146, 859-866.
50. Wei, J.N., Wang, L.H., Zhao, J.H., Li, C.Y., Ge, F. & Kang, L. (2011) Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions. New Phytologist, 189, 557-567.
51. Zarate, S.I., Kempema, L.A. & Walling, L.L. (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology, 143, 866-875.
52. 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, USA, 106, 21202-21207.
53. Zhang, P.J., Zhu, X.Y., Huang, F., Liu, Y., Zhang, J.M., Lu, Y.B. & Ruan, Y.M. (2011) Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccus solenopsis. PLoS ONE, 6, e22378.
54. Zhang, P.J., Broekgaarden, C., Zheng, S.J., Snoeren, T.A.L., van Loon, J.J.A., Gols, R. & Dicke, M. (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytologist, 197, 1291-1299.
55. Zhu, J. & Park, K.C. (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. Journal of Chemical Ecology, 31, 1733-1746.
56. Zhu-Salzman, K., Salzman, R.A., Ahn, J.E. & Koiwa, H. (2004) Transcriptional regulation of sorghum defence determinants against a phloem-feeding aphid. Plant Physiology, 134, 420-431.