Abstract
In their defence against pathogens, herbivorous insects, and mites, plants employ many induced responses. One of these responses is the induced emission of volatiles upon herbivory. These volatiles can guide predators or parasitoids to their herbivorous prey, and thus benefit both plant and carnivore. This use of carnivores by plants is termed indirect defence and has been reported for many plant species, including elm, pine, maize, Lima bean, cotton, cucumber, tobacco, tomato, cabbage, and Arabidopsis thaliana. Herbivory activates an intricate signalling web and finally results in defence responses such as increased production of volatiles. Although several components of this signalling web are known (for example the plant hormones jasmonic acid, salicylic acid, and ethylene), our understanding of how these components interact and how other components are involved is still limited. Here we review the knowledge on elicitation and signal transduction of herbivory-induced volatile production. Additionally, we discuss how use of the model plant Arabidopsis thaliana can enhance our understanding of signal transduction in indirect defence and how cross-talk and trade-offs with signal transduction in direct defence against herbivores and pathogens influences plant responses.
Key words
Wounding - tritrophic interactions - oxylipins - elicitors - regurgitant - crucifers - Solanaceae.
References
-
1
Agelopoulos N. G., Keller M. A..
Plant-natural enemy association in the tritrophic system, Cotesia rubecula - Pieris rapae - Brassicaceae (Cruciferae): I. sources of infochemicals.
J. Chem. Ecol..
(1994 a);
20
1725-1734
-
2
Agelopoulos N. G., Keller M. A..
Plant-natural enemy association in the tritrophic system Cotesia rubecula - Pieris rapae-Brassicaceae (Cruciferae): II. Preference of C. rubecula for landing and searching.
J. Chem. Ecol..
(1994 b);
20
1735-1748
-
3
Alborn T., Turlings T. C. J., Jones T. H., Stenhagen G., Loughrin J. H., Tumlinson J. H..
An elicitor of plant volatiles from beet armyworm oral secretion.
Science.
(1997);
276
945-949
-
4
Alméras E., Stolz S., Vollenweider S., Reymond P., Mene-Saffrane L., Farmer E. E..
Reactive electrophile species activate defense gene expression in Arabidopsis.
.
Plant J..
(2003);
34
202-216
-
5
Arimura G., Ozawa R., Nishioka T., Boland W., Koch T., Kühnemann F., Takabayashi J..
Herbivore-induced volatiles induce the emission of ethylene in neighboring Lima bean plants.
Plant J..
(2002);
29
87-98
-
6
Avé D. A., Gregory P., Tingey W. M..
Aphid repellent sesquiterpenes in glandular trichomes of Solanum berthaultii and S. tuberosum.
.
Entomol. Exp. Appl..
(1987);
44
131-138
-
7
Baldwin I. T..
Herbivory simulations in ecological research.
Trends Ecol. Evol..
(1990);
5
91-93
-
8
Baldwin I. T., Zhang Z. P., Diab N., Ohnmeiss T. E., McCloud E. S., Lynds G. Y., Schmelz E. A..
Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris.
.
Planta.
(1997);
201
397-404
-
9
Barbosa P., Saunders J. A., Kemper J., Trumbule R., Olechno J., Martinat P..
Plant allelochemicals and insect parasitoids. Effects of nicotine on Cotesia congregata (Say) (Hymenoptera: Braconidae) and Hyposoter annulipes (Cresson) (Hymenoptera: Ichneumonidae).
J. Chem. Ecol..
(1986);
12
1319-1328
-
10
Bi J. L., Murphy J. B., Felton G. W..
Does salicylic acid act as a signal in cotton for induced resistance to Helicoverpa zea?
.
J. Chem. Ecol..
(1997);
23
1805-1818
-
11
Blaakmeer A., Geervliet J. B. F., Loon v. J. J. A., Posthumus M. A., Beek v. T. A., Groot d. A., Van Loon J. J. A., Van Beek T. A., De Groot A..
Comparative headspace analysis of cabbage plants damaged by two species of Pieris caterpillars: consequences for in-flight host ocation by Cotesia parasitoids.
Entomol. Exp. Appl..
(1994);
73
175-182
-
12
Blechert S., Brodschelm W., Holder S., Kannerer L., Kutcham T., Mueller M. J., Xia Z. Q., Zenk M. H..
The octadecanoic pathway: signal molecules for the regulation of secondary pathways.
Proc. Natl. Acad. Sci. USA.
(1995);
92
4099-4105
-
13
Bohlmann J., Martin D., Oldham N. J., Gershenzon J..
Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization, and functional expression of a myrcene/(E)-beta-ocimene synthase.
Arch. Biochem. Biophys..
(2000);
375
261-269
-
14
Bouwmeester H. J., Verstappen F. W. A., Posthumus M. A., Dicke M..
Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and Lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis.
Plant Physiol..
(1999);
121
173-180
-
15
Cao H., Bowling S. A., Gordon A. S., Dong X. N..
Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.
Plant Cell.
(1994);
6
1583-1592
-
16
Creelman R. A., Mullet J. E..
Biosynthesis and action of jasmonates in plants.
Annu. Rev. Plant Physiol. Plant Mol. Biol..
(1997);
48
355-381
-
17
Croft K. P. C., Juttner F., Slusarenko A. J..
Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv. phaseolicola.
.
Plant Physiol..
(1993);
101
13-24
-
18
De Bruxelles G. L., Roberts M. R..
Signals regulating multiple responses to wounding and herbivores (Vol. 20, pg. 487, 2001).
Crit. Rev. Plant Sci..
(2001);
20
621
-
19
De Moraes C. M., Lewis W. J., Paré P. W., Alborn H. T., Tumlinson J. H..
Herbivore-infested plants selectively attract parasitoids.
Nature.
(1998);
393
570-573
-
20
Degenhardt J., Gershenzon J..
Demonstration and characterization of (E)-nerolidol synthase from maize: a herbivore-inducible terpene synthase participating in (3E)-4,8-dimethyl-1,3,7-nonatriene biosynthesis.
Planta.
(2000);
210
815-822
-
21
Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut Rella M., Kessmann H., Ward E., Ryals J..
A central role of salicylic acid in plant disease resistance.
Science.
(1994);
266
1247-1250
-
22 Dicke M.. Evolution of induced indirect defense of plants. Tollrian, R. and Harvell, C. J., eds. The Ecology And Evolution Of Inducible Defenses. Princeton, New Jersey; Princeton University Press (1999): 62-88
-
23
Dicke M., Van Beek T. A., Posthumus M. A., Ben Dom N., Van Bokhoven H., De Groot A. E..
Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. Involvement of host plant in its production.
J. Chem. Ecol..
(1990 a);
16
381-396
-
24
Dicke M., Gols R., Ludeking D., Posthumus M. A..
Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in Lima bean plants.
J. Chem. Ecol..
(1999);
25
1907-1922
-
25
Dicke M., Groeneveld A..
Hierarchical structure in kairomone preference of the predatory mite Amblyseius potentillae: dietary component indispensable for diapause induction affects prey location behaviour.
Ecol. Entomol..
(1986);
11
131-138
-
26 Dicke M., Sabelis M. W.. Does it pay plants to advertize for bodyguards? Towards a cost-benefit analysis of induced synomone production. Lambers, H., Cambridge, M. L., Konings, H., and Pons, T. L., eds. Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. The Hague; SPB Publishing (1989): 341-358
-
27
Dicke M., Sabelis M. W., Takabayashi J., Bruin J., Posthumus M. A..
Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control.
J. Chem. Ecol..
(1990 b);
16
3091-3118
-
28 Dicke M., Van Poecke R. M. P.. Signaling in plant-insect interactions: signal transduction in direct and indirect plant defence. Scheel, D. and Wasternack, C., eds. Plant Signal Transduction, Vol. 38. Oxford, UK; Oxford University Press (2002): 289-316
-
29
Dicke M., Van Poecke R. M. P., C. de Boer J. G..
Inducible indirect defence of plants: from mechanisms to ecological functions.
Basic Appl. Ecol..
(2003);
4
27-42
-
30 Dicke M., Vet L. E. M.. Plant-carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore. Olff, H., Brown, V. K., and Drent, R. H., eds. Herbivores: Between Plants and Predators. Oxford; Blackwell Science (1999): 483-520
-
31
Du Y. J., Poppy G. M., Powell W..
Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi.
.
J. Chem. Ecol..
(1996);
22
1591-1605
-
32
Fäldt J., Arimura G., Gershenzon J., Takabayashi J., Bohlmann J..
Functional identification of AtTPS03 as (E)-beta-ocimene synthase: a monoterpene synthase catalyzing jasmonate- and wound-induced volatile formation in Arabidopsis thaliana.
.
Planta.
(2003);
216
745-751
-
33
Farag M. A., Paré P. W..
C-6-green leaf volatiles trigger local and systemic VOC emissions in tomato.
Phytochemistry.
(2002);
61
545-554
-
34
Finidori-Logli V., Bagnères A. G., Clément J. L..
Role of plant volatiles in the search for a host by parasitoid Diglyphus isaea (Hymenoptera: Eulophidae).
J. Chem. Ecol..
(1996);
22
541-558
-
35
Frey M., Stettner C., Paré P. W., Schmelz E. A., Tumlinson J. H., Gierl A..
An herbivore elicitor activates the gene for indole emission in maize.
Proc. Natl. Acad. Sci. USA.
(2000);
97
14801-14806
-
36
Fritzsche-Hoballah M. E., Turlings T. C. J..
Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids.
Evol. Ecol. Res..
(2001);
3
553-565
-
37
Geervliet J. B. F., Posthumus M. A., Vet L. E. M., Dicke M..
Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species.
J. Chem. Ecol..
(1997);
23
2935-2954
-
38
Geervliet J. B. F., Vet L. E. M., Dicke M..
Innate responses of the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae) to volatiles from different plantherbivore complexes.
J. Insect. Behav..
(1996);
9
525-538
-
39
Geervliet J. B. F., Vreugdenhil A. I., Dicke M., Vet L. E. M..
Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula.
.
Entomol. Exp. Appl..
(1998);
86
241-252
-
40 Gershenzon J., Croteau R.. Terpenoids. Rosenthal, G. A. and Berenbaum, M. R., eds. Herbivores: Their Interactions with Secondary Plant Metabolites. San Diego; Academic Press (1991): 165-219
-
41
Glazebrook J..
Genes controlling expression of defense responses in Arabidopsis-2001 status.
Curr. Opin. Plant Biol..
(2001);
4
301-308
-
42
Glazebrook J., Chen W. J., Estes B., Chang H. S., Nawrath C., Metraux J. P., Zhu T., Katagiri F..
Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping.
Plant J..
(2003);
34
217-228
-
43
Gols R., Posthumus M. A., Dicke M..
Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis.
.
Entomol. Exp. Appl..
(1999);
93
77-86
-
44
Gouinguené S., Alborn H., Turlings T. C. J..
Induction of volatile emissions in maize by different larval instars of Spodoptera littoralis.
.
J. Chem. Ecol..
(2003);
29
145-162
-
45
Gouinguené S., Degen T., Turlings T. C. J..
Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte).
Chemoecology.
(2001);
11
9-16
-
46
Guerrieri E., Poppy G. M., Powell W., Tremblay E., Pennacchio F..
Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi.
.
J. Chem. Ecol..
(1999);
25
1247-1261
-
47
Halitschke R., Schittko U., Pohnert G., Boland W., Baldwin I. T..
Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses.
Plant Physiol..
(2001);
125
711-717
-
48
Harvey J. A..
Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness.
Ecol. Entomol..
(2000);
25
267-278
-
49
Hilker M., Kobs C., Varma M., Schrank K..
Insect egg deposition induces Pinus sylvestris to attract egg parasitoids.
J. Exp. Biol..
(2002 a);
205
455-461
-
50 Hilker M., Meiners T.. Chemoecology of Insect Eggs and Egg Deposition. London; Blackwell (2002 a)
-
51
Hilker M., Meiners T..
Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison.
Entomol. Exp. Appl..
(2002 b);
104
181-192
-
52 Hilker M., Rohfritsch O., Meiners T.. The Plant's Response towards Insect Egg Deposition. Hilker, M. and Meiners, T., eds. Chemoecology of Insect Eggs and Egg Deposition. London; Blackwell (2002 b): 205-233
-
53
Hopke J., Donath J., Blechert S., Boland W..
Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a beta-glucosidase and jasmonic acid.
FEBS Lett..
(1994);
352
146-150
-
54
Horiuchi J., Arimura G., Ozawa R., Shimoda T., Takabayashi J., Nishioka T..
Exogenous ACC enhances volatiles production mediated by jasmonic acid in Lima bean leaves.
FEBS Lett..
(2001);
509
332-336
-
55
Kahl J., Siemens D. H., Aerts R. J., Gabler R., Kuhnemann F., Preston C. A., Baldwin I. T..
Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore.
Planta.
(2000);
210
336-342
-
56 Karban R., Baldwin I. T.. Induced Responses to Herbivory. Chicago; The University of Chicago Press Ltd. (1997)
-
57
Kendall D. M., Bjostad L. B..
Phytohormone ecology - Herbivory by Thrips tabaci induces greater ethylene production in intact onions than mechanical damage alone.
J. Chem. Ecol..
(1990);
16
981-991
-
58
Kessler A., Baldwin I. T..
Plant responses to insect herbivory: The emerging molecular analysis.
Annu. Rev. Plant Biol..
(2002);
53
299-328
-
59
Koch T., Krumm T., Jung V., Engelberth J., Boland W..
Differential induction of plant volatile biosynthesis in the Lima bean by early and late intermediates of the octadecanoid-signaling pathway.
Plant Physiol..
(1999);
121
153-162
-
60
Koveos D. S., Kouloussis N. A., Broufas G. D..
Olfactory responses of the predatory mite Amblyseius andersoni Chant (Acari, Phytoseiidae) to bean plants infested by the spider mite Tetranychus urticae Koch (Acari, Tetranychidae).
J. Appl. Entomol..
(1995);
119
615-619
-
61
Krischik V. A., Goth R. W., Barbosa P..
Generalized plant defense: effects on multiple species.
Oecologia.
(1991);
85
562-571
-
62
Kruzmane D., Jankevica L., Ievinsh G..
Effect of regurgitant from Leptinotarsa decemlineata on wound responses in Solanum tuberosum and Phaseolus vulgaris.
.
Physiol. Plant..
(2002);
115
577-584
-
63
Kunkel B. N., Brooks D. M..
Cross talk between signaling pathways in pathogen defense.
Curr. Opin. Plant Biol..
(2002);
5
325-331
-
64
Laudert D., Weiler E. W..
Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling.
Plant J..
(1998);
15
675-684
-
65
León J., Rojo E., Sanchez-Serrano J. J..
Wound signalling in plants.
J. Exp. Bot..
(2001);
52
1-9
-
66
Loughrin J. H., Manukian A., Heath R. R., Tumlinson J. H..
Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae.
J. Chem. Ecol..
(1995);
21
1217-1227
-
67
Mattiacci L., Dicke M., Posthumus M. A..
Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor.
J. Chem. Ecol..
(1994);
20
2229-2247
-
68
Mattiacci L., Dicke M., Posthumus M. A..
beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps.
Proc. Natl. Acad. Sci. USA.
(1995);
92
2036-2040
-
69
Mattiacci L., Rocca B. A., Scascighini N., D'Alessandro M., Hern A., Dorn S..
Systemically induced plant volatiles emitted at the time of “danger”.
J. Chem. Ecol..
(2001 a);
27
2233-2252
-
70
Mattiacci L., Rudelli S., Rocca B. A., Genini S., Dorn S..
Systemically-induced response of cabbage plants against a specialist herbivore, Pieris brassicae.
.
Chemoecology.
(2001 b);
11
167-173
-
71
Mauricio R..
Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana.
.
American Naturalist.
(1998);
151
20-28
-
72
McCall P. J., Turlings T. C. J., Lewis W. J., Tumlinson J. H..
Role of plant volatiles in host location by the specialist parasitoid Microplitis croceipes Cresson (Braconidae: Hymenoptera).
J. Insect. Behav..
(1993);
6
625-639
-
73
McCloud E. S., Baldwin I. T..
Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris.
.
Planta.
(1997);
203
430-435
-
74
McConn M., Creelman R. A., Bell E., Mullet J. E., Browse J..
Jasmonate is essential for insect defense Arabidopsis.
.
Proc. Natl. Acad. Sci. USA.
(1997);
94
5473-5477
-
75
Meiners T., Hilker M..
Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaleruca luteola (Coleoptera: Chrysomelidae).
Oecologia.
(1997);
112
87-93
-
76
Meiners T., Hilker M..
Induction of plant synomones by oviposition of a phytophagous insect.
J. Chem. Ecol..
(2000);
26
221-232
-
77
Meiners T., Westerhaus C., Hilker M..
Specificity of chemical cues used by a specialist egg parasitoid during host location.
Entomol. Exp. Appl..
(2000);
95
151-159
-
78
Meinke D. W., Cherry J. M., Dean C., Rounsley S. D., Koornneef M..
Arabidopsis thaliana: A model plant for genome analysis.
Science.
(1998);
282
662-682
-
79
Mitchell-Olds T..
Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution.
Trends Ecol. Evol..
(2001);
16
693-700
-
80
Mitchell-Olds T., Gershenzon J., Baldwin I., Boland W..
Research focus - Chemical ecology in the molecular era.
Trends Plant Sci..
(1998);
3
362-365
-
81
Moran P. J..
Plant-mediated interactions between insects and a fungal plant pathogen and the role of plant chemical responses to infection.
Oecologia.
(1998);
115
523-530
-
82
Moran P. J., Thompson G. A..
Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways.
Plant Physiol..
(2001);
125
1074-1085
-
83
Mumm R., Schrank K., Wegener R., Schulz S., Hilker M..
Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition.
J. Chem. Ecol..
(2003);
29
1235-1252
-
84
Musser R. O., Hum-Musser S. M., Eichenseer H., Peiffer M., Ervin G., Murphy J. B., Felton G. W..
Herbivory: Caterpillar saliva beats plant defences - A new weapon emerges in the evolutionary arms race between plants and herbivores.
Nature.
(2002);
416
599-600
-
85
Neveu N., Grandgirard J., Nenon J. P., Cortesero A. M..
Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L.
J. Chem. Ecol..
(2002);
28
1717-1732
-
86
Obara N., Hasegawa M., Kodama O..
Induced volatiles in elicitor-treated and rice blast fungus- inoculated rice leaves.
Biosci. Biotechnol. Biochem..
(2002);
66
2549-2559
-
87
O'Donnell P., Calvert C., Atzorn R., Wasternack C., Leyser H. M. O., Bowles D. J..
Ethylene as a signal mediating the wound response of tomato plants.
Science.
(1996);
274
1914-1917
-
88
Ozawa R., Arimura G., Takabayashi J., Shimoda T., Nishioka T..
Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants.
Plant Cell Physiol..
(2000);
41
391-398
-
89 Panda N., Khush G. S.. Host Plant Resistance to Insects. Wallingford; CAB International (1995)
-
90
Paré P. W., Tumlinson J. H..
De novo biosynthesis of volatiles induced by insect herbivory in cotton plants.
Plant Physiol..
(1997);
114
1161-1167
-
91
Paré P. W., Tumlinson J. H..
Cotton volatiles synthesized and released distal to the site of insect damage.
Phytochemistry.
(1998);
47
521-526
-
92
Paré P. W., Tumlinson J. H..
Plant volatiles as a defense against insect herbivores.
Plant Physiol..
(1999);
121
325-331
-
93
Piel J., Atzorn R., Gäbler R., Kühnemann F., Boland W..
Cellulysin from the plant parasitic fungus Trichoderma viride elicits volatile biosynthesis in higher plants via the octadecanoid signalling cascade.
FEBS Lett..
(1997);
416
143-148
-
94
Pieterse C. M. J., Ton J., Van Loon L. C..
Cross-talk between plant defence signalling pathways: boost or burden?.
AgBiotechNet.
(2001);
3
1-8
-
95
Pieterse C. M. J., Van Wees S. C. M., Van Pelt J. A., Knoester M., Laan R., Gerrits N., Weisbeek P. J., Van Loon L. C..
A novel signaling pathway controlling induced systemic resistance in Arabidopsis.
.
Plant Cell.
(1998);
10
1571-1580
-
96
Pohnert G., Jung V., Haukioja E., Lempa K., Boland W..
New fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometridae) caterpillars.
Tetrahedron.
(1999);
55
11275-11280
-
97
Potting R. P. J., Vet L. E. M., Dicke M..
Host microhabitat location by stem-borer parasitoid Cotesia flavipes - the role of herbivore volatiles and locally and systemically induced plant volatiles.
J. Chem. Ecol..
(1995);
21
525-539
-
98
Reymond P., Weber H., Damond M., Farmer E. E..
Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis.
.
Plant Cell.
(2000);
12
707-719
-
99
Rieske L. K., Raffa K. F..
Ethylene emission by a deciduous tree, Tilia americana, in response to feeding by introduced basswood thrips, Thrips calcaratus.
.
J. Chem. Ecol..
(1995);
21
187-197
-
100
Rodriguez-Saona C., Crafts-Brandner S. J., Williams L., Paré P. W..
Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants.
J. Chem. Ecol..
(2002);
28
1733-1747
-
101
Röse U. S. R., Lewis W. J., Tumlinson J. H..
Specificity of systemically released cotton volatiles as attractants for specialist and generalist parasitic wasps.
J. Chem. Ecol..
(1998);
24
303-319
-
102
Rostás M., Simon M., Hilker M..
Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi.
Basic Appl. Ecol..
(2003);
4
43-62
-
103 Sabelis M. W., Dicke M.. Long-range dispersal and searching behaviour. Helle, W. and Sabelis, M. W., eds. Spider Mites: Their Biology, Natural Enemies and Control. World Crop Pests 1 A. Amsterdam; Elsevier (1985): 141-160
-
104 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.. The evolution of direct and indirect plant defence against herbivorous arthropods. Olff, H., Brown, V. K., and Drent, R. H., eds. Herbivores Between Plants And Predators. Oxford; Blackwell Science Ltd. (1999): 109-166
-
105
Sabelis M. W., Van der Baan H. E..
Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi.
.
Entomol. Exp. Appl..
(1983);
33
303-314
-
106
Schaller F..
Enzymes of the biosynthesis of octadecanoid-derived signalling molecules.
J. Exp. Bot..
(2001);
52
11-23
-
107 Schaller F., Weiler E. W.. Wound- and mechanical signalling. Scheel, D. and Wasternack, C., eds. Plant Signal Transduction, Vol. 38. Oxford; Oxford University Press (2002): 20-44
-
108 Scheel D., Wasternack C.. Signal transduction in plants: cross-talk with the environment. Scheel, D. and Wasternack, C., eds. Plant Signal Transduction, Vol. 38. Oxford; Oxford University Press (2002): 1-5
-
109
Schenk P. M., Kazan K., Wilson I., Anderson J. P., Richmond T., Somerville S. C., Manners J. M..
Coordinated plant defense responses in Arabidopsis revealed by microarray analysis.
Proc. Natl. Acad. Sci. USA.
(2000);
97
11655-11660
-
110
Schittko U., Preston C. A., Baldwin I. T..
Eating the evidence? Manduca sexta larvae can not disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption.
Planta.
(2000);
210
343-346
-
111
Schmelz E. A., Alborn H. T., Banchio E., Tumlinson J. H..
Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory.
Planta.
(2003 a);
216
665-673
-
112
Schmelz E. A., Alborn H. T., Tumlinson J. H..
The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays.
.
Planta.
(2001);
214
171-179
-
113
Schmelz E. A., Alborn H. T., Tumlinson J. H..
Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays.
.
Physiol. Plant..
(2003 b);
117
403-412
-
114 Schoonhoven L. M., Jermy T., Van Loon J. J. A.. Insect-Plant Biology, from Physiology to Evolution. London; Chapman and Hall (1998)
-
115
Shen B. Z., Zheng Z. W., Dooner H. K..
A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: Characterization of wild-type and mutant alleles.
Proc. Natl. Acad. Sci. USA.
(2000);
97
14807-14812
-
116
Shimoda T., Dicke M..
Attraction of a predator to chemical information related to nonprey: when can it be adaptive?.
Behavioral Ecology.
(2000);
11
606-613
-
117
Shimoda T., Ozawa R., Arimura G., Takabayashi J., Nishioka T..
Olfactory responses of two specialist insect predators of spider mites toward plant volatiles from Lima bean leaves induced by jasmonic acid and/or methyl salicylate.
Appl. Entomol. Zoolog..
(2002);
37
535-541
-
118
Shimoda T., Takabayashi J. W. A., Takafuji A..
Response of predatory insect Scolothrips takahashii toward herbivore-induced plant volatiles under laboratory and field conditions.
J. Chem. Ecol..
(1997);
23
2033-2048
-
119
Siemens D. H., Mitchell-Olds T..
Glucosinolates and herbivory by specialists (Coleoptera: Chrysomelidae, Lepidoptera: Plutellidae): Consequences of concentration and induced resistance.
Environ. Entomol..
(1996);
25
1344-1353
-
120
Staswick P. E., Tiryaki I., Rowe M. L..
Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation.
Plant Cell.
(2002);
14
1405-1415
-
121
Staswick P. E., Yuen G. Y., Lehman C. C..
Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare.
.
Plant J..
(1998);
15
747-754
-
122 Steidle J. L. M., Van Loon J. J. A.. Chemoecology of parasitoid and predator oviposition behaviour. Hilker, M. and Meiners, T., eds. Chemoecology of Insect Eggs and Egg Deposition. London; Blackwell (2002): 291-317
-
123
Stintzi A., Browse J..
The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis.
Proc. Natl. Acad. Sci. USA.
(2000);
97
10625-10630
-
124
Stintzi A., Weber H., Reymond P., Browse J., Farmer E. E..
Plant defense in the absence of jasmonic acid: The role of cyclopentenones.
Proc. Natl. Acad. Sci. USA.
(2001);
98
12837-12842
-
125
Stotz H. U., Koch T., Biedermann A., Weniger K., Boland W., Mitchell-Olds T..
Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways.
Planta.
(2002);
214
648-652
-
126
Stotz H. U., Pittendrigh B. R., Kroymann J., Weniger K., Fritsche J., Bauke A., Mitchell-Olds T..
Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth.
Plant Physiol..
(2000);
124
1007-1017
-
127
Stout M. J., Fidantsef A. L., Duffey S. S., Bostock R. M..
Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum.
.
Physiol. Mol. Plant. Pathol..
(1999);
54
115-130
-
128
Takabayashi J., Dicke M..
Plant-carnivore mutualism through herbivore-induced carnivore attractants.
Trends Plant Sci..
(1996);
1
109-113
-
129
Takabayashi J., Dicke M., Posthumus M. A..
Variation in composition of predatorattracting allelochemical emitted by herbivore-infested plants: relative influence of plant and herbivore.
Chemoecology.
(1991);
1-6
-
130
Takabayashi J., Dicke M., Posthumus M. A..
Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors.
J. Chem. Ecol..
(1994);
20
1329-1354
-
131
Takabayashi J., Takahashi S., Dicke M., Posthumus M. A..
Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants.
J. Chem. Ecol..
(1995);
21
273-287
-
132
Thaler J. S..
Jasmonate-inducible plant defences cause increased parasitism of herbivores.
Nature.
(1999);
399
686-688
-
133
Thaler J. S..
Effect of jasmonate-induced plant responses on the natural enemies of herbivores.
J. Anim. Ecol..
(2002);
71
141-150
-
134
Thaler J. S., Farag M. A., Paré P. W., Dicke M..
Jasmonate-deficient plants have reduced direct and indirect defences against herbivores.
Ecol. Lett..
(2002);
5
764-774
-
135
Thaler J. S., Stout M. J., Karban R., Duffey S. S..
Jasmonate-mediated induced plant resistance affects a community of herbivores.
Ecol. Entomol..
(2001);
26
312-324
-
136
The Arabidopsis Genome Initiative .
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
.
Nature.
(2000);
408
796-815
-
137
Thomma B., Eggermont K., Penninckx I., Mauch Mani B., Vogelsang R., Cammue B. P. A., Broekaert W. F..
Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens.
Proc. Natl. Acad. Sci. USA.
(1998);
95
15107-15111
-
138
Thomma B., Penninckx I., Broekaert W. F., Cammue B. P. A..
The complexity of disease signaling in Arabidopsis.
.
Curr. Opin. Immunol..
(2001);
13
63-68
-
139
Tscharntke T., Thiessen S., Dolch R., Boland W..
Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa.
.
Biochem. Syst. Ecol..
(2001);
29
1025-1047
-
140
Turlings T. C. J., Alborn H. T., Loughrin J. H., Tumlinson J. H..
Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: Isolation and bioactivity.
J. Chem. Ecol..
(2000);
26
189-202
-
141
Turlings T. C. J., Bernasconi M., Bertossa R., Bigler F., Caloz G., Dorn S..
The induction of volatile emissions in maize by three herbivore species with different feeding habits: Possible consequences for their natural enemies.
Biol. Control.
(1998);
11
122-129
-
142
Turlings T. C. J., McCall P. J., Alborn H. T., Tumlinson J. H..
An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps.
J. Chem. Ecol..
(1993 a);
19
411-425
-
143
Turlings T. C. J., Tumlinson J. H..
Systemic release of chemical signals by herbivore-injured corn.
Proc. Natl. Acad. Sci. USA.
(1992);
89
8399-8402
-
144
Turlings T. C. J., Tumlinson J. H., Lewis W. J..
Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.
Science.
(1990);
30
1251-1253
-
145 Turlings T. C. J., Wäckers F. L., Vet L. E. M., Lewis W. J., Tumlinson J. H.. Learning of host-finding cues by Hymenopterous parasitoids. Papaj, D. R. and Lewis, A. C., eds. Insect Learning: Ecological and Evolutionary Perspectives. New York; Chapman & Hall (1993 b): 51-78
-
146
Van den Boom C. E. M., Van Beek T. A., Dicke M..
Attraction of Phytoseiulus persimilis (Acari: Phytoseiidae) towards volatiles from various Tetranychus urticae-infested plant species.
Bull. Entomol. Res..
(2002);
92
539-546
-
147
Van den Boom C. E. M., Van Beek T. A., Posthumus M. A., De Groot A. E., Dicke M..
Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families.
J. Chem. Ecol..
(2004);
30
69-89
-
148
Van Loon J. J. A., de Boer J. G., Dicke M..
Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction.
Entomol. Exp. Appl..
(2000);
97
219-227
-
149 Van Poecke R. M. P.. Indirect Defence of Arabidopsis Against Herbivorous Insects: Combining Parasitoid Behaviour and Chemical Analysis with a Molecular Genetic Approach. Wageningen; Wageningen University (2002)
-
150
Van Poecke R. M. P., Dicke M..
Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway.
J. Exp. Bot..
(2002);
53
1793-1799
-
151
Van Poecke R. M. P., Dicke M..
Signal transduction downstream of salicylic and jasmonic acid in herbivory-induced parasitoid attraction by Arabidopsis is independent of JAR1 and NPR1.
Plant, Cell Environ..
(2003);
26
1541-1548
-
152
Van Poecke R. M. P., Posthumus M. A., Dicke M..
Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: Chemical, behavioral, and gene-expression analysis.
J. Chem. Ecol..
(2001);
27
1911-1928
-
153
Van Poecke R. M. P., Roosje M., Pumarino L., Dicke M..
Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species.
Entomol. Exp. Appl..
(2003);
107
229-236
-
154
Van Wees S. C. M., de Swart E. A. M., Van Pelt J. A., Van Loon L. C., Pieterse C. M. J..
Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana.
.
Proc. Natl. Acad. Sci. USA.
(2000);
97
8711-8716
-
155
Vancanneyt G., Sanz C., Farmaki T., Paneque M., Ortego F., Castanera P., Sanchez Serrano J. J..
Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance.
Proc. Natl. Acad. Sci. USA.
(2001);
98
8139-8144
-
156
Walling L. L..
The myriad plant responses to herbivores.
J. Plant Growth Regul..
(2000);
19
195-216
-
157
Weissbecker B., Van Loon J. J. A., Posthumus M. A., Bouwmeester H. J., Dicke M..
Identification of volatile potato sesquiterpenoids and their olfactory detection by the twospotted stinkbug Perillus bioculatus.
.
J. Chem. Ecol..
(2000);
26
1433-1445
-
158
Zangerl A. R..
Evolution of induced plant responses to herbivores.
Basic Appl. Ecol..
(2003);
4
91-103
-
159
Zhang Y. L., Fan W. H., Kinkema M., Li X., Dong X. N..
Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene.
Proc. Natl. Acad. Sci. USA.
(1999);
96
6523-6528
-
160
Ziegler J., Keinanen M., Baldwin I. T..
Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata.
.
Phytochemistry.
(2001);
58
729-738
R. M. P. van Poecke
Laboratory of Entomology
Wageningen University
P.O. Box 8031
6700 EH Wageningen
The Netherlands
Email: remco@remjet.nl
Section Editor: C. M. J. Pieterse