Abstract
Plant volatile analysis may be the oldest form of what now is called plant “metabolomic”
analysis. A wide array of volatile organic compounds (VOCs), such as alkanes, alcohols,
isoprenoids, and esters, can be collected simultaneously from the plant headspace,
either within the laboratory or in the field. Increasingly faster and more sensitive
analysis techniques allow detection of an ever-growing number of compounds in decreasing
concentrations. However, the myriads of data becoming available from such experiments
do not automatically increase our ecological and evolutionary understanding of the
roles these VOCs play in plant-insect interactions. Herbivores and parasitoids responding
to changes in VOC emissions are able to perceive minute changes within a complex VOC
background. Plants modified in genes involved in VOC synthesis may be valuable for
the evaluation of changes in plant-animal interactions compared to tests with synthetic
compounds, as they allow changes to be made within the context of a more complex profile.
We argue that bioinformatics is an essential tool to integrate statistical analysis
of plant VOC profiles with insect behavioural data. The implementation of statistical
techniques such as multivariate analysis (MVA) and meta-analysis is of the utmost
importance to interpreting changes in plant VOC mixtures. MVA focuses on differences
in volatile patterns rather than in single compounds. Therefore, it more closely resembles
the information processing in insects that base their behavioural decisions on differences
in VOC profiles between plants. Meta-analysis of different datasets will reveal general
patterns pertaining to the ecological role of VOC in plant-insect interactions. Successful
implementation of bioinformatics in VOC research also includes the development of
MVA that integrate time-resolved chemical and behavioural analyses, as well as databases
that link plant VOCs to their effects on insects.
Key words
Chemical ecology - induced responses - insect-plant interactions - plant metabolomics
- multitrophic interactions - multivariate analysis - natural enemies - plant volatile
analysis - volatile organic compounds
References
- 1
Aharoni A., Jongsma M. A., Bouwmeester H. J..
Volatile science? Metabolic engineering of terpenoids in plants.
Trends in Plant Science.
(2005);
10
594-602
- 2
Arimura G., Ozawa G., Shimoda T., Nishioka T., Boland W., Takabayashi J..
Herbivory-induced volatiles elicit defence genes in lima bean leaves.
Nature.
(2000);
406
512-515
- 3
Beale M. H., Birkett M. A., Bruce T. J. A., Chamberlain K., Field L. M., Huttly A. K.,
Martin J. L., Parker R., Phillips A. L., Pickett J. A., Prosser I. M., Shewry P. R.,
Smart L. E., Wadhams L. J., Woodcock C. M., Zhang Y. H..
Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior.
Proceedings of the National Academy of Sciences of the USA.
(2006);
103
10509-10513
- 4
Bezemer T. M., van Dam N. M..
Linking aboveground and belowground interactions via induced plant defenses.
Trends in Ecology and Evolution.
(2005);
20
617-624
- 5
Bolter C. J., Dicke M., Van Loon J. J. A., Visser J. H., Posthumus M. A..
Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory
and after its termination.
Journal of Chemical Ecology.
(1997);
23
1003-1023
- 6
Bruce T. J. A., Wadhams L. J., Woodcock C. M..
Insect host location: a volatile situation.
Trends in Plant Science.
(2005);
10
269-274
- 7
Choi Y. H., Kim H. K., Hazekamp A., Erkelens C., Lefeber A. W. M., Verpoorte R..
Metabolomic differentiation of Cannabis sativa cultivars using H‐1 NMR spectroscopy and principal component analysis.
Journal of Natural Products.
(2004);
67
953-957
- 8
D'Alessandro M., Turlings T. C. J..
In situ modification of herbivore-induced plant odors: a novel approach to study the
attractiveness of volatile organic compounds to parasitic wasps.
Chemical Senses.
(2005);
30
739-753
- 9
de Boer J. G., Posthumus M. A., Dicke M..
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.
(2004);
30
2215-2230
- 10
De Moraes C. M., Lewis W. J., Pare P. W., Alborn H. T., Tumlinson J. H..
Herbivore-infested plants selectively attract parasitoids.
Nature.
(1998);
393
570-573
- 11
Degen T., Dillmann C., Marion-Poll F., Turlings T. C. J..
High genetic variability of herbivore-induced volatile emission within a broad range
of maize inbred lines.
Plant Physiology.
(2004);
135
1928-1938
- 12
Dicke M., de Boer J. G., Hofte M., Rocha-Granados M. C..
Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous
arthropods.
Oikos.
(2003);
101
38-48
- 13
Dicke M., Gols R., Ludeking D., Posthumus M. A..
Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles
in lima bean plants.
Journal of Chemical Ecology.
(1999);
25
1907-1922
- 14
Dicke M., Sabelis M. W..
Infochemical terminology: based on cost-benefit analysis rather than origin of compounds?.
Functional Ecology.
(1988);
2
131-139
- 15 Dicke M., Sabelis M. W..
Does it pay for plants to advertise 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 Academic
Publishing (1989): 341-358
- 16
Dudareva N., Pichersky E., Gershenzon J..
Biochemistry of plant volatiles.
Plant Physiology.
(2004);
135
1893-1902
- 17
Firn R. D., Jones C. G..
Do we need a new hypothesis to explain plant VOC emissions?.
Trends in Plant Science.
(2006 a);
11
112-113
- 18
Firn R. D., Jones C. G..
Response to Pichersky et al.: Correcting a misconception about the screening hypothesis.
Trends in Plant Science.
(2006 b);
11
422
- 19
Girling R. D., Hassall M., Turner J. G., Poppy G. M..
Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae.
Entomologia Experimentalis et Applicata.
(2006);
120
1-9
- 20
González-Coloma A., Martín-Benito D., Mohamed N., García-Vallejo M. C., Soria A. C..
Antifeedant effects and chemical composition of essential oils from different populations
of Lavandula luisieri L.
Biochemical Systematics and Ecology.
(2006);
34
609-616
- 21
Gouinguené S., Alborn H., Turlings T. C. J..
Induction of volatile emissions in maize by different larval instars of Spodoptera littoralis.
Journal of Chemical Ecology.
(2003);
29
145-162
- 22
Hartmann T..
Diveristy and variability of plant secondary metabolism: a mechanistic view.
Entomologia Experimentalis et Applicata.
(1996);
80
177-188
- 23
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.
Ecological Entomology.
(2000);
25
267-278
- 24
Heiden A. C., Hoffmann T., Kahl J., Kley D., Klockow D., Langebartels C., Mehlhorn H.,
Sandermann H., Schraudner M., Schuh G., Wildt J..
Emission of volatile organic compounds from ozone-exposed plants.
Ecological Applications.
(1999);
9
1160-1167
- 25
Hemerik L., Gort G., Brussaard L..
Food preference of wireworms analyzed with multinomial Logit models.
Journal of Insect Behavior.
(2003);
16
647-665
- 26 Hilker M., Meiners T..
Chemical cues mediating interactions between Chrysomelids and parasitoids. Cox, M. L., ed. Advances in Crysomelidae Biology, Vol. 1. Leiden, The Netherlands;
Backhuys Publishers (1999): 197-216
- 27
Holopainen J. K..
Multiple functions of inducible plant volatiles.
Trends in Plant Science.
(2004);
9
529-533
- 28
Hunter M. D..
A breath of fresh air: beyond laboratory studies of plant volatile-natural enemy interactions.
Agricultural and Forest Entomology.
(2002);
4
1-6
- 29
Ibrahim M. A., Nissinen A., Holopainen J. K..
Response of Plutella xylostella and its parasitoid Cotesia plutellae to volatile compounds.
Journal of Chemical Ecology.
(2005);
31
1969-1984
- 30
Jansen J. J., Hoefsloot H. C. J., van der Greef J., Timmerman M. E., Smilde A. K..
Multilevel component analysis of time-resolved metabolic fingerprinting data.
Analytica Chimica Acta.
(2005 a);
530
173-183
- 31
Jansen J. J., Hoefsloot H. C. J., van der Greef J., Timmerman M. E., Westerhuis J. A.,
Smilde A. K..
ASCA: analysis of multivariate data obtained from an experimental design.
Journal of Chemometrics.
(2005 b);
19
469-481
- 32
Jones C. G., Firn R. D..
On the evolution of plant secondary chemical diversity.
Philosophical Transactions of the Royal Society of London B, Biological Sciences.
(1991);
333
273-280
- 33
Kappers I. F., Aharoni A., van Herpen T., Luckerhoff L. L. P., Dicke M., Bouwmeester H. J..
Genetic engineering of terpenoid metabolism attracts, bodyguards to Arabidopsis.
Science.
(2005);
309
2070-2072
- 34
Kessler A., Baldwin I. T..
Defensive function of herbivore-induced plant volatile emissions in nature.
Science.
(2001);
291
2141-2144
- 35
Konstantopoulou M. A., Krokos F. D., Mazomenos B. E..
Chemical composition of corn leaf essential oils and their role in the oviposition
behavior of Sesamia nonagrioides females.
Journal of Chemical Ecology.
(2004);
30
2243-2256
- 36
Koricheva J., Nykanen H., Gianoli E..
Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades,
masters of all?.
American Naturalist.
(2004);
163
E64-E75
- 37
Kost C., Heil M..
Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants.
Journal of Ecology.
(2006);
94
619-628
- 38
Mattiacci L., Dicke M., Posthumus M. A..
Beta-glucosidase – an elicitor of herbivore-induced plant odor that attracts host-searching
parasitic wasps.
Proceedings of the National Academy of Sciences of the USA.
(1995);
92
2036-2040
- 39
Meiners T., Wackers F., Lewis W. J..
Associative learning of complex odours in parasitoid host location.
Chemical Senses.
(2003);
28
231-236
- 40
Mildner-Szkudlarz S., Jelen H. H., Zawirska-Wojtasiak R., Wasowicz E..
Application of headspace – solid phase microextraction and multivariate analysis for
plant oils differentiation.
Food Chemistry.
(2003);
83
515-522
- 41
Mitchell-Olds T., Clauss M. J..
Plant evolutionary genomics.
Current Opinion in Plant Biology.
(2002);
5
74-79
- 42
Mithöfer A., Wanner G., Boland W..
Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding
is sufficient to elicit herbivory-related volatile emission.
Plant Physiology.
(2005);
137
1160-1168
- 43
Mumm R., Hilker M..
The significance of background odour for an egg parasitoid to detect plants with host
eggs.
Chemical Senses.
(2005);
30
337-343
- 44
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.
Journal of Chemical Ecology.
(2002);
28
1717-1732
- 45
Nykänen H., Koricheva J..
Damage-induced changes in woody plants and their effects on insect herbivore performance:
a meta-analysis.
Oikos.
(2004);
104
247-268
- 46
Ober D..
Seeing double: gene duplication and diversification in plant secondary metabolism.
Trends in Plant Science.
(2005);
10
444-449
- 47
Olson D. M., Rains G. C., Meiners T., Takasu K., Tertuliano M., Tumlinson J. H., Wackers F. L.,
Lewis W. J..
Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors.
Chemical Senses.
(2003);
28
545-549
- 48
Owen S. M., Peñuelas J..
Opportunistic emissions of volatile isoprenoids.
Trends in Plant Science.
(2005);
10
420-426
- 49
Owen S. M., Peñuelas J..
Response to Firn and Jones: Volatile isoprenoids, a special case of secondary metabolism.
Trends in Plant Science.
(2006 a);
11
113-114
- 50
Owen S. M., Peñuelas J..
Response to Pichersky et al.: Plant volatile isoprenoids and their opportunistic functions.
Trends in Plant Science.
(2006 b);
11
423
- 51
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 and Cell Physiology.
(2000);
41
391-398
- 52
Peñuelas J., Filella I., Stefanescu C., Llusia J..
Caterpillars of Euphydryas aurinia (Lepidoptera: Nymphalidae) feeding on Succisa pratensis leaves induce large foliar emissions of methanol.
New Phytologist.
(2005);
167
851-857
- 53
Peñuelas J., Munne-Bosch S..
Isoprenoids: an evolutionary pool for photoprotection.
Trends in Plant Science.
(2005);
10
166-169
- 54
Pichersky E., Sharkey T. D., Gershenzon J..
Plant volatiles: lack of function or lack of knowledge?.
Trends in Plant Science.
(2006);
11
421
- 55
Pitarokili D., Tzakou O., Loukis A., Harvala C..
Volatile metabolites from Salvia fruticosa as antifungal agents in soilborne pathogens.
Journal of Agricultural and Food Chemistry.
(2003);
51
3294-3301
- 85 Poppy G. M., Powell W..
Genetic manipulation of parasitoids – can we improve biological control by manipulating
the parasitoid and/or the plant?. Ehler, L., ed. The Genetics and Evolution of Biological Control Agents. Oxford;
CABI Publishing (2004): 219-233
- 86 Poppy G. M., Wilkinson M. J.. Gene Flow from GM Plants – A Manual for Assessing,
Measuring and Managing the Risks. Oxford; Blackwell Publishing (2005): 241pp
- 56
Price P. W., Bouton C. E., Gross P., McPheron B. A., Thompson J. N., Weis A. E..
Interactions among 3 trophic levels – influence of plants on interactions between
insect herbivores and natural enemies.
Annual Review of Ecology and Systematics.
(1980);
11
41-65
- 57
Raguso R. A..
Flowers as sensory billboards: progress towards an integrated understanding of floral
advertisement.
Current Opinion in Plant Biology.
(2004);
7
434-440
- 58
Rasmann S., Kollner T. G., Degenhardt J., Hiltpold I., Toepfer S., Kuhlmann U., Gershenzon J.,
Turlings T. C. J..
Recruitment of entomopathogenic nematodes by insect-damaged maize roots.
Nature.
(2005);
434
732-737
- 59
Reddy G. V. P., Holopainen J. K., Guerrero A..
Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles.
Journal of Chemical Ecology.
(2002);
28
131-143
- 60
Rennenberg H., Loreto F., Polle A., Brilli F., Fares S., Beniwal R. S., Gessler A..
Physiological responses of forest trees to heat and drought.
Plant Biology.
(2006);
8
556-571
- 61
Rinnan R., Rinnan A., Holopainen T., Holopainen J. K., Pasanen P..
Emission of non-methane volatile organic compounds (VOCs) from boreal peatland microcosms
– effects of ozone exposure.
Atmospheric Environment.
(2005);
39
921-930
- 62
Rohloff J., Bones A. M..
Volatile profiling of Arabidopsis thaliana – putative olfactory compounds in plant communication.
Phytochemistry.
(2005);
66
1941
- 63
Röse U. S. R., Manukian A., Heath R. R., Tumlinson J. H..
Volatile semiochemicals released from undamaged cotton leaves – a systemic response
of living plants to caterpillar damage.
Plant Physiology.
(1996);
111
487-495
- 64
Runyon J. B., Mescher M. C., De Moraes C. M..
Volatile chemical cues guide host location and host selection by parasitic plants.
Science.
(2006);
313
1964-1967
- 65 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. London;
Blackwell Science (1999): 109-166
- 66
Saez F..
Volatile oil variability in Thymus serpylloides ssp gadorensis growing wild in Southeastern
Spain.
Biochemical Systematics and Ecology.
(2001);
29
189-198
- 67
Scascighini N., Mattiacci L., D'Alessandro M., Hern A., Sybille Rott A., Dorn S..
New insights in analysing parasitoid attracting synomones: early volatile emission
and use of stir bar sorptive extraction.
Chemoecology.
(2005);
15
97-104
- 68
Schnee C., Kollner T. G., Held M., Turlings T. C. J., Gershenzon J., Degenhardt J..
The products of a single maize sesquiterpene synthase form a volatile defense signal
that attracts natural enemies of maize herbivores.
Proceedings of the National Academy of Sciences of the USA.
(2006);
103
1129-1134
- 69 Schoonhoven L. M., Jermy T., van Loon J. J. A.. Insect-Plant Biology. From Physiology
to Evolution. 1st ed. London; Chapmann and Hall (1998)
- 70
Smid H. A., van Loon J. J. A., Posthumus M. A., Vet L. E. M..
GC‐EAG-analysis of volatiles from Brussels sprouts plants damaged by two species of
Pieris caterpillars: olfactory receptive range of a specialist and a generalist parasitoid
wasp species.
Chemoecology.
(2002);
12
169-176
- 71
Steeghs M., Bais H. P., de Gouw J., Goldan P., Kuster W., Northway M., Fall R., Vivanco J. M..
Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of
root-secreted volatile organic compounds in Arabidopsis.
Plant Physiology.
(2004);
135
47-58
- 72
Stewart-Jones A., Poppy G. M..
Comparison of glass vessels and plastic bags for enclosing living plant parts for
headspace analysis.
Journal of Chemical Ecology.
(2006);
32
845-864
- 73
Sumner L. W., Mendes P., Dixon R. A..
Plant metabolomics: large-scale phytochemistry in the functional genomics era.
Phytochemistry.
(2003);
62
817-836
- 74
Takabayashi J., Takahashi S., Dicke M., Posthumus M. A..
Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants.
Journal of Chemical Ecology.
(1995);
21
273-287
- 75
Tattersall D. B., Bak S., Jones P. R., Olsen C. E., Nielsen J. K., Hansen M. L., Hoj P. B.,
Moller B. L..
Resistance to an herbivore through engineered cyanogenic glucoside synthesis.
Science.
(2001);
293
1826-1828
- 76
Tholl D., Boland W., Hansel A., Loreto F., Rose U. S. R., Schnitzler J.-P..
Practical approaches to plant volatile analysis.
The Plant Journal.
(2006);
45
540-560
- 77
Tikunov Y., Lommen A., de Vos C. H. R., Verhoeven H. A., Bino R. J., Hall R. D., Bovy A. G..
A novel approach for nontargeted data analysis for metabolomics. Large-scale profiling
of tomato fruit volatiles.
Plant Physiology.
(2005);
139
1125-1137
- 87
Tinbergen N..
On aims and methods of ethology.
Zeitschrift für Tierphysiologie, Tiernahrung und Futtermittelkunde.
(1953);
20
410-433
- 78
Turlings T. C. J., Tumlinson J. H., Lewis W. J..
Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.
Science.
(1990);
250
1251-1253
- 79
van der Meijden E., Klinkhamer P. G. L..
Conflicting interests of plants and the natural enemies of herbivores.
Oikos.
(2000);
89
202-208
- 80
van Loon J. A., de Boer J. G., Dicke M..
Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction.
Entomologia Experimentalis et Applicata.
(2000);
V97
219
- 81
van Tol R., Visser J. H., Sabelis M. W..
Olfactory responses of the vine weevil, Otiorhynchus sulcatus, to tree odours.
Physiological Entomology.
(2002);
27
213-222
- 82
Vet L. E. M..
From chemical to population ecology: infochemical use in an evolutionary context.
Journal of Chemical Ecology.
(1999);
25
31-49
- 83
Vet L. E. M., Wäckers F. L., Dicke M..
How to hunt for hiding hosts – the reliability-detectability problem in foraging parasitoids.
Netherlands Journal of Zoology.
(1991);
41
202-213
- 84
Voelckel C., Schittko U., Baldwin I. T..
Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced
defenses of Nicotiana attenuata.
Oecologia.
(2001);
127
274-280
N. M. van Dam
Netherlands Institute of Ecology (NIOO-KNAW)
Multitrophic Interactions Department
P.O. Box 40
6666 ZG Heteren
The Netherlands
eMail: n.vandam@nioo.knaw.nl
Guest Editor: F. Loreto