The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes
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- 作者：Ted C. J. Turlings (1) ted.turling@unine.ch
Ivan Hiltpold (2)
Sergio Rasmann (3) - 关键词：Entomopathogenic nematodes – ; Foraging behavior – ; Root volatiles – ; Carbon dioxide – ; Belowground tritrophic interactions
- 刊名：Plant and Soil
- 出版年：2012
- 出版时间：September 2012
- 年：2012
- 卷：358
- 期：1-2
- 页码：51-60
- 全文大小：257.0 KB
- 参考文献：1. Ali JG, Alborn HT, Stelinski LL (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J Chem Ecol 36(4):361–368
2. Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99(1):26–35
3. Baermann G (1917) Eine enifache Methode Zur Auffindung von Anklyostomum (Nematoden) larven in Erdproben. GeneeskTijdschrNed-Indie 57:131–137
4. Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256(1):67–83
5. Boff MIC, Zoon FC, Smits PH (2001) Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomologia Experimentalis et Applicata 98(3):329–337
6. Campbell JF, Lewis EE (2002) Entomopathogenic nematode host- search strategies. In: Lewis EE, Campbell JF, Sukhdeo MVK (eds) The behavioural ecology of parasites. CABI Publishing, Wallingford, pp 13–38
7. Crocoll C, Asbach J, Novak J, Gershenzon J, Degenhardt J (2010) Terpene synthases of oregano (Origanum vulgare L.) and their roles in the pathway and regulation of terpene biosynthesis. Plant Mol Biol 73:587–603
8. Cutler GC, Webster JM (2003) Host-finding ability of three entomopathogenic nematode isolates in the presence of plant roots. Nematology 5:601–608
9. D’Alessandro M, Turlings TCJ (2005) In Situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem Senses 30:739–753
10. D’Alessandro M, Held M, Triponez Y, Turlings TCJ (2006) The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32(12):2733–2748
11. Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135(4):1928–1938
12. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14(2):169–176
13. Degenhardt J, Hiltpold I, K枚llner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci U S A 106(32):13213–13218
14. Dekker T, Geier M, Carde RT (2005) Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J Exp Biol 208(15):2963–2972
15. Dillman AR, Chaston JM, Adams BJ, Ciche TA, Goodrich-Blair H, Stock SP, Sternberg PW (2012) An entomopathogenic nematode by any other name. Plos Pathog 8(3):e1002527. doi:
16. Ferry A, Dugravot S, Delattre T, Christides JP, Auger J, Bagneres AG, Poinsot D, Cortesero AM (2007) Identification of a widespread monomolecular odor differentially attractive to several Delia radicum ground-dwelling predators in the field. J Chem Ecol 33(11):2064–2077
17. Fontana A, Held M, Fantaye CA, Turlings TCJ, Degenhardt J, Gershenzon J (2011) Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). J Chem Ecol 37(6):582–591
18. Gaugler R (2002) Entomopathogenic nematology. CABI Publishing, Wallingford
19. Gaugler R, Campbell JF (1991) Selection for enhanced host-finding of scarab larvae (Coleoptera, Scarabaeidae) in an entomopathogenic nematode. Environ Entomol 20(2):700–706
20. Gaugler R, Lebeck L, Nakagaki B, Boush GM (1980) Orientation of the entomogenous nematode Neoaplectana carpocapsae to carbon-dioxide. Environ Entomol 9(5):649–652
21. Gaugler R, Campbell JF, McGuire TR (1989) Selection for host-finding in Steinernema feltiae. J Invertebr Pathol 54(3):363–372
22. Grewal PS, Ehlers RU, Shapiro DI (2005) Nematodes as biocontrol agents. CABI Publishing, Wallingford
23. Griffin CT, Downes MJ (1994) Selection of Heterorhabditis sp. for improved infectivity at low temperatures. In: Burnell AM, Ehlers RU, Masson JP (eds) Genetics of entomopathogenic nematode-bacterium complexes. European Commission Publication EUR 15681 EN, Luxembourg, pp 120–128
24. Hallem EA, Dillman AR, Hong AV, Zhang YJ, Yano JM, DeMarco SF, Sternberg PW (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21(5):377–383
25. Hass B, Griffin CT, Downes MJ (1999) Persistence of Heterorhabditis infective juveniles in soil: comparison of extraction and infectivity measurements. J Nematol 31(4):508–516
26. Hiltpold I, Turlings TCJ (2008) Belowground chemical signalling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34(5):628–635
27. Hiltpold I, Turlings TCJ (2012) Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pest and to improve crop yield. J Chem Ecol. doi:10.1007/s10886-012-0131-9
28. Hiltpold I, Baroni M, Toepfer S, Kuhlmann U, Turlings TCJ (2010a) Selection of entomopathogenic nematodes for enhanced responsiveness to a volatile root signal helps to control a major root pest. J Exp Biol 213(14):2417–2423
29. Hiltpold I, Baroni M, Toepfer S, Kuhlmann U, Turlings TCJ (2010b) Selective breeding of entomopathogenic nematodes for enhanced attraction to a root signal did not reduce their establishment or persistence after field release. Plant Signal Behav 5(11):1450–1452
30. Hiltpold I, Toepfer S, Kuhlmann U, Turlings TCJ (2010c) How maize root volatiles influence the efficacy of entomopathogenic nematodes against the western corn rootworm? Chemoecology 20(2):155–162
31. Hugot JP, Baujard P, Morand S (2001) Biodiversity in helminths and nematodes as a field of study: an overview. Nematology 3:199–208
32. Kappers IF, Aharoni A, van Herpen T, Luckerhoff LLP, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309(5743):2070–2072
33. Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206
34. K枚llner T, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J (2008) A maize (E)-BETA-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20(2):482–494
35. Koppenh枚fer AM, Fuzy EM (2006) Nematodes for white grub control: effects of soil type and soil moisture on infectivity and persistence. USGA Turfgrass Environ Res Online 5(18):1–10
36. Kruitbos LM, Heritage S, Hapca S, Wilson MJ (2010) The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis. Parasitology 137(2):303–309
37. Lewis EE (2002) Behavioural ecology. In: Gaugler R (ed) Entomopathogenic nematology. CABI International, pp 205–223
38. Lewis EE, Gaugler R, Harrison R (1993) Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Can J Zool-Rev Canadienne De Zool 71(4):765–769
39. Lewis EE, Barbarosa B, Gaugler R (2002) Mating and sexual communication by Steinernema carpocapsae (Nemata: Steinernematidae). J Nematol 34(4):328–331
40. Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310(5750):992–992
41. Mitchell P (2011) Costs and benefits of controllin pest Diabrotica in maize in the United States. Paper presented at the 24th IWG Conference, Freiburg, Germany, 24–26 Oct. 2011
42. Mitreva M, Blaxter ML, Bird DM, McCarter JP (2005) Comparative genomics of nematodes. Trends Genet 21(10):573–581
43. Nuttley WM, Atkinson-Leadbeater KP, van der Kooy D (2002) Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 99(19):12449–12454
44. O’Halloran DM, Burnell AM (2003) An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora. Parasitology 127:375–385
45. Pickett JA, Bruce TJA, Chamberlain K, Hassanali A, Khan ZR, Matthes MC, Napier JA, Smart LE, Wadhams LJ, Woodcock CM (2006) Plant volatiles yielding new ways to exploit plant defence. In: Dicke M, Takken W (eds) Chemical ecology: from gene to ecosystem. Springer, Dordrecht
46. Ramos-Rodriguez O, Campbell JF, Christen JM, Shapiro-Ilan DI, Lewis EE, Ramaswamy SB (2007) Attraction behaviour of three entomopathogenic nematode species towards infected and uninfected hosts. Parasitology 134:729–738
47. Rasmann S, Turlings TCJ (2008) First insights into specificity of below ground tritrophic interactions. Oikos 117:362–369
48. Rasmann S, K枚llner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434(7034):732–737
49. Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99(1):16–25
50. Rasmann S, Ali J, Helder J, van der Putten W (2012) Ecology and evolution of soil nematode chemotaxis. J Chem Ecol. doi:10.1007/s10886-012-0118-6
51. Schnee C, K枚llner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103(4):1129–1134
52. Shapiro-Ilan DI, Gouge DH, Piggott SJ, Fife JP (2006) Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biol Control 38(1):124–133
53. Szalai M, Kom谩romi JP, Bažok R, Barčic JI, Kiss J, Toepfer S (2011) Generational growth rate estimates of Diabrotica virgifera virgifera populations (Coleoptera: Chrysomelidae). J Pest Sci 84(1):133–142
54. Tamo C, Ricard I, Held M, Davison AC, Turlings TCJ (2006) A comparison of naive and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours. Anim Biol 56(2):205–220
55. Toepfer S, Haye T, Erlandson M, Goettel M, Lundgren JG, Kleespies RG, Weber DC, Walsh GC, Peters A, Ehlers RU, Strasser H, Moore D, Keller S, Vidal S, Kuhlmann U (2009) A review of the natural enemies of beetles in the subtribe Diabroticina (Coleoptera: Chrysomelidae): implications for sustainable pest management. Biocontrol Sci Technol 19:1–65
56. Torayama I, Ishihara T, Katsura I (2007) Caenorhabditis elegans integrates the signals of butanone and food to enhance chemotaxis to butanone. J Neurosci 27(4):741–750
57. Torr P, Heritage S, Wilson MJ (2004) Vibrations as a novel signal for host location by parasitic nematodes. Int J Parasitol 34(9):997–999
58. Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opinion Plant Biol 9(4):421–427
59. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250(4985):1251–1253
60. Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207(1):146–152
61. Turlings TCJ, Davison AC, Tam貌 C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomol 29:45–55
62. Turner SL, Li N, Guda T, Githure J, Card茅 RT, Ray A (2011) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474(7349):87–91
63. van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4(4):292–294
64. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172
65. Vidal S, Kuhlmann U, Edwards R (2005) Western corn rootworm: ecology and management. CABI Publishers, Wallingford
66. Wang Y, Gaugler R (1998) Host and penetration site location by entomopathogenic nematodes against Japanese beetle larvae. J Invertebr Pathol 72(3):313–318
67. Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe - the ‘no control’ scenario. J Appl Entomol 134(5):385–394
68. Wilson MJ, Ehlers RU, Glazer I (2012) Entomopathogenic nematode foraging strategies – is Steinernema carpocapsae really an ambush forager? Nematology in press. doi:10.1163/156854111X617428 - 作者单位：1. FARCE Laboratory, Institute of Biology, University of Neuch芒tel, Neuch芒tel, Switzerland2. University of Missouri, 205 Curtis Hall, Columbia, MO 65211-7020, USA3. Institute of Evolution and Ecology, University of Lausanne, Lausanne, Switzerland
- ISSN：1573-5036
文摘
Background Entomopathogenic nematodes (EPNs) are tiny parasitic worms that parasitize insects, in which they reproduce. Their foraging behavior has been subject to numerous studies, most of which have proposed that, at short distances, EPNs use chemicals that are emitted directly from the host as host location cues. Carbon dioxide (CO2) in particular has been implicated as an important cue. Recent evidence shows that at longer distances several EPNs take advantage of volatiles that are specifically emitted by roots in response to insect attack. Studies that have revealed these plant-mediated interactions among three trophic levels have been met with some disbelief.