Chem. Senses 27: 143-152,
2002
© Oxford University Press 2002
Receptor Neuron Discrimination of the Germacrene D Enantiomers in the Moth Helicoverpa armigera
Department of Zoology, Norwegian University of Science and Technology, Trondheim, Norway 1 Department of Chemistry, Organic Chemistry, Ecological Chemistry Group, The Royal Institute of Technology, Stockholm, Sweden
Correspondence to be sent to: Hanna Mustaparta, Department of Zoology, Norwegian University of Science and Technology, N-7489 Trondheim, Norway. e-mail: Hanna.Mustaparta{at}chembio.ntnu.no
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Abstract |
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Plants release complex mixtures of volatiles, including chiral constituents. In the search for the biologically relevant plant odorants, gas chromatography linked to electrophysiological recordings from single receptor neurons has been employed. In heliothine moths, including the females of the Eurasian cotton bollworm moth Helicoverpa armigera, a major type of receptor neurons is identified, showing high sensitivity and selectivity for the sesquiterpene germacrene D. In the present study, gas chromatography with a chiral column linked to single cell recordings were performed. It was found that all germacrene D neurons belonged to one type; all responded to both enantiomers, but (-)-germacrene D had
10 times stronger effect than
(+)-germacrene D. Parallel dose—response curves for the two enantiomers
were obtained by direct stimulations. The enantiomeric composition of
germacrene D, which differed in six plant species and in different individuals
of one species, was determined on the basis of the neuron responses. The
results, showing the presence of one neuron type for receiving the information
about germacrene D in the various plants, suggests that the two enantiomers
mediate the same kind of information to the moth, but with different
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Introduction |
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Chiral recognition of organic molecules is considered to be one of the most important criteria of biological activity, based on the fact that about half of all active chemicals have a chiral centre (Ohloff, 1994
). Since the
early confirmation of the ability of humans to discriminate between
enantiomers of the taste stimulant asparagine
(Piutti, 1886), many examples
on enantioselectivity have been shown in taste as well as in olfaction. A well
known example is the different smell of (+)- and (-)-carvone, caraway and
peppermint, respectively (Friedman and
Miller, 1971). Interesting discoveries of enantioselectivity in
the insect communication systems were made by Lanier et al.
(Lanier et al.,
1980), showing that geographically isolated populations of bark
beetles (Ips pini) used different ratios of the two enantiomers, (+)-
and (-)-ipsdienol (2-methyl-6-methylene-2,7-octadien-4-ol), as aggregation
pheromones. In fact, the major enantiomer used by one population inhibited the
attraction of the other, a phenomenon that was shown to be important for the
isolation from a sympatric species (Birch
et al., 1980). The receptor neuron responses underlying
the behavioural discrimination of enantiomers were demonstrated in these
species of bark beetles by the identification of two neuron types, one tuned
to (+)-ipsdienol and the other to (-)-ipsdienol
(Mustaparta et al.,
1980). Other studies of various insect species have also
demonstrated the use of chiral compounds in intraspecific and interspecific
communication, showing synergistic as well as antagonistic effects of
enantiomers on the behaviour (Tumlinson
et al., 1977; Silverstein,
1979,
1988;
Tumlinson, 1979;
Hansen et al., 1983).
Accordingly, distinct types of enantioselective receptor neurons have been
shown in some of these species (Hansen
et al., 1983; Hansen,
1984; Mustaparta,
1990; Wojtasek et
al., 1998). Whether one species possesses one or two types of
neurons for enantiomers correlates well with the specific message the signals
mediate. In the case where only one enantiomer is produced by the insects, one
enantioselective receptor neuron type is found, e.g. neurons with
enantioselectivity exclusively for (-)-ipsenol
(2-methyl-6-methylene-7-octen-4-ol) in bark beetle species (Mustparta et
al., 1980).
The other important group of odorants for herbivorous insects is
plant-produced volatiles. In spite of the significance of these odours for
host finding, knowledge is still scarce about which of the hundreds of plant
volatiles are biologically relevant in the various species. Progress is being
made by the use of gas chromatography linked to electrophysiology
(Guerin et al., 1983;
Baur et al., 1993;
Blight et al., 1995;
Wibe and Mustaparta, 1996;
Wibe et al., 1998;
Barata et al., 2000;
Røstelien et al.,
2000a,
b) (M. Stranden et
al., unpublished data). In heliothine moths 12 types of receptor
neurons have been identified that responded selectively to monoterpenes and
sesquiterpenes (Røstelien et al.,
2000a,
b) (M. Stranden et
al., unpublished data). Of particular interest was the finding of a
receptor neuron type with high sensitivity to and selectivity for the
sesquiterpene germacrene D (7-iso-propyl-10-methyl-4-methylene-cyclodeca-5,
10-diene) (Røstelien et
al., 2000b). This neuron type was obtained in 80% of all
recordings from the females of the tobacco budworm moth Heliothis
virescens, and responses to germacrene D were shown in tests of many
plant mixtures. The presence of a major neuron type with the same sensitivity
and selectivity for germacrene D has also been demonstrated in females of
another heliothine species, the Eurasian cotton bollworm moth, Helicoverpa
armigera (M. Stranden et al., unpublished data).
Like most sesquiterpenes, germacrene D is a chiral compound synthesized as
one or both enantiomers in various plants, fungi and animals. It is considered
as an important intermediate in the formation of many sesquiterpenes, which
are biosynthesised via cyclization of farnesyl diphosphate catalysed by
synthases (Yoshihara et al.,
1969; Cane, 1990;
Bülow and
König, 2000). In higher plants the
(-)-configuration of germacrene D is shown to be the most common enantiomer
(Beechan et al., 1978;
Lorimer and Weavers, 1987;
König et
al., 1996;
Bülow,
1998;
Bülow and
König, 2000). However, exceptions
have been found in Solidago species, in which the synthesis of both
enantiomers is controlled by two enantioselective synthases
(Niwa et al., 1980;
Schmidt et al., 1998,
1999).
In principle, two plant compounds that give different messages to the animal would be expected to activate different receptor neuron types. An interesting question is whether the two germacrene D enantiomers, produced by different enzymes, are perceived as different odour qualities. Which kind of message the heliothine moth species receives in the detection of the germacrene D enantiomers, is not yet clear. However, the large number of germacrene D neurons indicates that the compound is of particular importance in the host location by H. armigera females. The presence of one, possibly two, types of receptor neurons would indicate how well the moth may discriminate between (+)- and (-)-germacrene D. The objective of the present study was (i) to determine the enantioselectivity of the germacrene D receptor neurons in the female moth Helicoverpa armigera, and (ii) to find out whether the moth possesses one or two types of neurons tuned to each of the enantiomers.
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Materials and methods |
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Insects
Females of Helicoverpa armigera originated from a laboratory
culture at the Agricultural Research Organisation, The Volcani Centre, Bet
Dagan, Israel. They arrived as pupae and were kept as previously described by
Røstelien et al.
(Røstelien et al.,
2000a). When eclosed, they were placed in separate boxes marked
with eclosing date and given honey water and pure water ad libitum.
Insects aged 2-5 days old were used in the experiments.
Chemicals
As the sesquiterpene germacrene D was not available commercially as pure material, it was tested as constituent in essential oils, extracts and headspace samples of plant material as well as in isolated fractions.
Extracts and headspace samples
One hexane extract was made from materials of a dried root of ginger
(Zingiber sp.). In addition, pentane extracts of leaf tissues of
sunflower (Helianthus annuus), Canadian goldenrod (Solidago
canadensis) and yarrow (Achillea millefolium), were included as
test material. The extract of sunflower (cultivated plants) and yarrow were
made of leaves from several plants, whereas the two extracts of Canadian
goldenrod were each made from one individual. The plant materials were
collected in the area of Stockholm, Sweden (in October, outdoor temperature
1°C). The ginger extract was made of the cut root material, which was
stirred for 4.5 h with hexane. The other extracts were made of freshly cut
leaves washed several times with pentane. One headspace extract of wild briar
(Rosea dumalis) collected in the Trondheim area was also included in
this study [procedure as described by Røstelien et al.
(Røstelien et al.,
2000a)].
Fraction containing (-)-ß-caryophyllene and germacrene D
A fraction containing (-)-ß-caryophyllene (42.5%) and germacrene D
(46%) was isolated from a sesquiterpene fraction of cubebe pepper (Piper
cubeba) essential oil (20 g) containing <2% of germacrene D
(Schmaus, 1988). The isolation
procedure is described in Røstelien et al.
(Røstelien et al.,
2000b), and involves several parallel series of medium pressure
liquid chromatography (MPLC), first on a column loaded with silica gel and
then on one with silver nitrate (AgNO3) impregnated silica gel. The
solvent gradient was made of n-hexane and methyl acetate in different
proportions. The fractions were followed by thin layer chromatography and gas
chromatography mass spectrometry (GC-MS). The fractions containing germacrene
D were pooled and a second AgNO3-MPLC run with dried
n-hexane only was performed, which resulted in the fraction
containing (-)-ß-caryophyllene and germacrene D (1 ng/µl for both
compounds). Further isolation of germacrene D using MPLC was unsuccessful.
Isolated enantiomers
Reference samples of defined germacrene D enantiomers were kindly provided
by Dr W.A. König (University of Hamburg,
Germany). The samples were obtained by hydro distillation from two Canadian
goldenrod (Solidago canadensis) individuals, one containing
mainly the (+)-enantiomer and the other mainly the (-)-enantiomer. The
volatiles were collected in hexane and the concentrations of the samples were
10 µg/µl and 0.1 µg/µl for (+)-germacrene D and
(-)-germacrene D, respectively. The purity of the samples were 86% for the
(+)-enantiomer and 75% for the (-)-enantiomer. Both samples contained
10% of the opposite isomer, the optical purity being 79% ee
(enantiomeric excess) for the (+)-sample and 76% ee for the
(-)-sample. From these samples, dilution in hexane (>99%) were made in
decade steps down to 1 ng/µl for (+)-germacrene D and 10 pg/µl for
(-)-germacrene D. Test cartridges with the enantiomers were made by inserting
in each tube a piece of filter paper on which 1 µl of a dilution was
applied.
Linked gas chromatography single cell recording (GC-SCR)
The insect preparation and the electrophysiological recordings of nerve
impulses from single olfactory receptor neurons on the antennae were carried
out as described by Røstelien et al.
(Røstelien et al.,
2000a). Contact with the neuron was made with the tungsten
microelectrode positioned into the base of the sensillum. The neuron was then
tested for sensitivity to germacrene D by direct stimulation with the
different mixtures, i.e. by blowing air through a cartridge containing a small
sample of each solution on a filter paper. If a cell responded, we further
tested its selectivity by injection of the mixtures into the GC-column. A
split at the end of the column led half of the effluent to the GC-detector and
the other half over the insect antennae, resulting in simultaneously recorded
gas chromatograms and responses to the separated compounds. Each neuron was
tested in sequence via two capillary columns installed in parallel in the GC,
one polar DB-wax column (30 m, i.d. 0.25 mm, film thickness 0.25 µm,) and
one chiral column [25 m, i.d. 0.25 mm, Heptakis
(6-O-t-Butyldimethylsilyl-2,
3-di-O-methyl)-ß-cyclodextrin (50% in OV1701)]
(Schmidt et al.,
1998;
König et
al., 1999). Separation in the polar column was performed from
the initial temperature 80°C with an increase rate of 6°C/min to
180°C, and a further increase rate of 15°C/min to 220°C. In the
chiral column, enantiomeric separation of germacrene D was found to be optimal
at the isothermal temperature 125°C. The detection limit for the columns
were found for (-)-ß-caryophyllene (Fluka, 99%); between 0.1 and 0.01
ng/µl for DBwax and 1 ng/µl for the chiral column.
(-)-ß-Caryophyllene was used as a standard for determining the
concentrations of the germacrene D enantiomers.
Direct stimulation with different concentrations of (+)-and (-)-germacrene D were performed by blowing an air stream (3.3 ml/s) through the test cartridges and over the insect antenna. The stimulations were performed from low to high concentrations, alternating stimulation with the (+)-and the (-)-enantiomers. Each cartridge was tested twice in the dynamic area. Between the stimulations, purified air was blown over the antenna. The interstimulus intervals were 1 min for the low concentrations and longer for the high concentrations, depending on the response strength. Spike activity was recorded on an analogue tape recorder in parallel with the computer program Electro Antenno Detection (version 2.3, Synthec NL, Hilversum, The Netherlands), and analysed in the computer program AutoSpike-32 (Synthec NL). The response strength of the receptor neuron to the enantiomers was plotted as numbers of spikes per 0.5 s for each concentration, resulting in dose—response curves for each enantiomer.
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Results |
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The results are based on seven receptor neurons in seven females of Helicoverpa armigera; all responding with high selectivity and sensitivity to germacrene D. Six neurons were tested individually up to 28 times via the polar as well as the chiral GC-column (Table 1). When tested for the same mixture, all neurons showed the same response characteristics. The seventh neuron, which was not tested via the GC, was characterized by direct stimulation with the reference samples of germacrene D enantiomers. When stimulated via the polar GC-column, each of the six neurons showed a strong excitatory response to germacrene D. Injection of the samples into the chiral column displayed chromatograms with two well-separated GC-peaks of (+)- and (-)-germacrene D, both eliciting responses in all six neurons. This is exemplified in Figure 1A showing separation of the germacrene D enantiomers in the cubebe oil fraction containing 35% of the (+)-enantiomer and 65% of the (-)-enantiomer. Both enantiomers were eluted after (-)-ß-caryophyllene. The simultaneous electrophysiological recording from the germacrene D neuron showed selectively strong responses to both enantiomers. The increased spike activity of the neuron during the elution of (+)- and (-)-germacrene D is shown in Figure 1B. Histogram conversions of the spike amplitudes and selected spike classes presented as overlays show that the responses to the enantiomers were based on one population of spikes with uniform amplitudes and waveforms.
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Dose-dependent responses to both enantiomers were demonstrated for all
neurons by injecting dilutions of the cubebe oil fraction in decade steps down
to 1:1000. This is shown in Figure
1C (same neuron as in Figure
1A), where a decrease of responses to both enantiomers follows the
decrease of germacrene D concentrations. For all dilutions, the strongest
response was elicited by (-)-germacrene D. This applied to all six neurons.
The different stimulatory effect of the two enantiomers were further
demonstrated by testing on the same neuron two reference samples of (+)- and
(-)-germacrene D, each containing 10% of the opposite enantiomer
(Figure 1D). In the
(-)-germacrene D sample, 10% of the (+)-enantiomer did not elicit a detectable
response. However, in the other sample 10% of (-)-germacrene D was enough to
elicit about the same response as the nine times larger amount of the
(+)-configuration. Thus, the stimulation via the gas chromatograph showed an
10 times better effect of (-)-germacrene D than of the (+)-enantiomer.
This was confirmed by the dose—response curves obtained with direct
stimulations of two neurons with the same reference samples of (+)- and
(-)-germacrene D. Figure 2A
shows duplicated dose—response curves for one neuron, where the
(+)-germacrene D curve is shifted 1 logarithmic unit to the right for the
curve of the (-)-configuration. As shown in
Figure 2B the structures of the
two enantiomers differ in the direction of the isopropyl group in relation to
the 10-carbon ring.
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The various plant materials, selected due to the germacrene D content, were
found to contain different enantiomeric ratios of the compound. Thus, the
neurons showed consistent excitatory responses to both (+)- and (-)-germacrene
D when tested for the cubebe oil fraction, the extract of ginger and the
different extracts of Canadian goldenrod (Figures
1A and
3). Interestingly, the
different samples of Canadian goldenrod showed different enantiomeric ratios,
90% of the (-)-enantiomer in extract 1 and 70% of the
(+)-configuration in extract 2. The ginger extract seemed to contain at least
85% of (+)-germacrene D, whereas the small amount of the (-)-enantiomer was
masked by an overlapping GC-peak of another compound. Only one response to
(-)-germacrene D was obtained when testing the neurons for the extracts of
sunflower and yarrow and for a headspace sample of wild briar. The absence of
response at the retention time for the (+)-enantiomer indicates that these
samples do not contain detectable amounts of (+)-germacrene D.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In this study we have employed (i) a chiral GC-SCR column, and (ii) stimulation directly from cartridges to study the enantioselectivity of the germacrene D receptor neurons in H. armigera. The results were consistent for all the recorded germacrene D neurons, indicating that they belonged to one functional type. In addition to the strong responses to germacrene D and weak responses to three other structurally related sesquiterpenes (Stranden et al., unpublished data), the present results have demonstrated that all of the neurons possessed the same enantioselectivity. The well separated germacrene D enantiomers in the chiral GC-column consistently elicited a stronger response during the elution of the (-)- than of the (+)-enantiomer. The dose—response relationships demonstrated
10 times better stimulatory effect of (-)-germacrene D,
both in the experiments with GC-SCR and/or by direct stimulation of the seven
neurons. The similarity of spike amplitudes and waveforms of responses to both
enantiomers indicated that they originated from the same neuron. During the
selected period (beginning) of the responses, the spikes of the two responses
showed overlapping waveforms of one population of spike amplitudes, i.e.
having a normal distribution around the same amplitude value. Thus, the
present results have demonstrated enantioselectivity of one germacrene D
receptor neuron type, which responds to both enantiomers, but with a 10 times
higher affinity for the (-)-configuration. The presence of only one neuron
type for receiving the information about germacrene D indicates that the two
enantiomers mediate the same kind of message to the moth, i.e. the effect of
the (-)-enantiomer can be simulated by a 10 times higher concentration of the
(+)-configuration. It is in contrast to pheromone enantiomers that activate
two different receptor neuron types, having synergistic or antagonistic
effects on the behaviour. The behavioural response of H. armigera
females to the germacrene D enantiomers is presently under investigation. Our
hypothesis is that female H. armigera will show the same behavioural
responses to both enantiomers of germacrene D. If a moth species need to
distinguish between the two enantiomers for finding suitable host plants, at
least two different types of receptor neurons should be needed, e.g. one tuned
to (+)-germacrene D and the other to (-)-germacrene D.
It is obvious that the enantiomers of chiral odorants may be critical in
the interaction with the olfactory receptor proteins, like in other
interactions between chemicals and receptors. However, the question is to what
extent in each case the chiral centre takes part in the interaction. As both
enantiomers of germacrene D activate the same receptor neuron, it can be
assumed that they are transported by the same odour binding protein and
interact with the same membrane receptor protein but with different affinity.
The difference between (+)- and (-)-germacrene D is the direction of the
isopropyl group. Thus, it is likely that this group is an active part of the
ligand in the interaction with the receptor, and that its different
orientation causes the lower effect of the (+)-enantiomer than of the
(-)-enantiomer. In previous studies of enantioselectivity of olfactory
receptor neurons, it has been difficult to assess the difference of the
stimulatory effect of enantiomers because of impurities. For instance, the
(-)-ipsdienol receptor neuron has been stimulated with (+)-ipsdienol samples
containing different impurities of the (-)-enantiomer
(Mustaparta et al.,
1980) (H. Mustaparta, unpublished data). The dose—response
curves obtained for the (+)-samples were shifted to the right according to the
lower content of (-)-ipsdienol. Stimulation with highly pure enantiomers has
shown that some receptor neurons tuned to one enantiomer may not respond to
the opposite configuration. In the study of the ipsenol enantiomers, one
sample with pure (+)-ipsenol (provided by Dr K. Mori, University of Tokyo,
Japan) showed no stimulatory effect on the (-)-ipsenol receptor neurons (H.
Mustaparta, unpublished data). In another study of three scarab beetle species
(the Japanese beetle Popilia japonica, the Osaka beetle Anomala
osakana and the scarab beetle Anomala cuprea), using highly pure
enantiomers (japonilure, buibuilactone, >99% ee), the receptor
neurons showed either no response to the opposite enantiomer or a weak
response at high concentrations (Wojtasek
et al., 1998; Larsson
et al., 1999). For biologically relevant plant odours,
enantio-selectivity has been demonstrated for two receptor neuron types in the
pine weevil (Hylobius abietis), one tuned to (+)-
-pinene and
the other one to (-)-limonene, for which the opposite configuration elicited a
weaker response (Wibe et al.,
1998). However, the stimulation was only performed via non-chiral
GC-columns, making it difficult to determine the contributions of the opposite
enantiomers. Studies of olfactory receptor neurons in mammals by the use of
the patch clamp technique have revealed neurons selective for one enantiomer
as well as neurons responding to both configurations of carvone
(Ma and Shepherd, 2000).
The importance of germacrene D as a cue for H. armigera and other
heliothine moths in the interaction with plants is indicated by the large
number of selective receptor neurons tuned to this constituent, shown in the
present and previous studies
(Røstelien et al.,
2000b) (Stranden et al., unpublished data). Germacrene D
seems to be widely distributed among higher plants, both in hosts and
non-hosts of heliothine moths. The receptor selectivity for (-)-germacrene D
might have evolved as an adaptation to the most common configuration. However,
the significance of germacrene D for the behaviour of H. armigera is
not clear, e.g. whether (-)-germacrene D is involved in location of favourable
hosts (for nutrition or oviposition) or in avoidance of unsuitable hosts. In
other insect species, different behavioural responses to (-)-germacrene D have
been demonstrated. As a host volatile produced by healthy pines (Pinus
densiflora) it is reported to act as an allomone, masking the attraction
of the cerambycid beetle (Monochamus alternatus) to the oxygenated
terpenes of the pines (Yamasaki et
al., 1997). (-)-Germacrene D is also known as a mimic of the
sex pheromones of the female American cockroach (Periplaneta
americana), eliciting the sexual attraction of the males
(Tahara et al., 1975;
Kitamura et al.,
1976). These examples indicate a wide distribution and function of
(-)-germacrene D in insect—plant interactions.
The present study also allowed determining with a very sensitive method the
enantiomeric ratio of germacrene D in the various plant species. Our findings
of the (-)-configuration in all six plant species, and exclusively in three of
them, appear to be in accordance with the hypothesis that (-)-germacrene D is
the abundant enantiomer in higher plants, whereas (+)-germacrene D is rare and
more likely to occur in lower plants
(Beechan et al., 1978;
Lorimer and Weavers, 1987;
König et
al., 1996;
Bülow,
1998;
Bülow and
König, 2000). However, we also found
a significant amount of the (+)-enantiomer in the extracts of Canadian
goldenrod, cubebe pepper and ginger, and in two cases it was the major
enantiomer. The presence of both enantiomers has also been documented in
Torilis japonica (Itokawa et
al., 1983), Araucaria bidwilli
(Pietsch and
König, 2000) and 11 different
Solidago species (Niwa et
al., 1980;
Bülow,
1998;
Bülow and
König, 2000). Altogether it seems
that the (+)-enantiomer is more widely distributed than has earlier been
thought. Variation of the enantiomeric ratio in Solidago individuals
presented here is in accordance with previous results
(Bülow,
1998). In fact, Bülow found
variations over the whole spectrum of enantiomeric ratios in Solidago
individuals depending on their geographical locations, and within an
individual the ratio was constant over a 3-year period. It was hypothesized
that the enantiomeric ratios of germacrene D in plants of Solidago
are genetically determined.
In conclusion, the use of gas chromatograph with a chiral column linked to recordings from single receptor neurons, have demonstrated that all germacrene D neurons belong to one functional type. They responded to both enantiomers, but had a 10 times higher affinity for the (-)-configuration. The slopes of the dose—response curves shifted 1 logarithmic unit, were parallel indicating that (+)- and (-)-germacrene D may interact with the same membrane receptor. The responses by this enantioselective neuron type showed the presence of one or both enantiomers in six plant species tested.
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Acknowledgments |
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The Norwegian Research Council (project no. 133958/420) provided the principal financial support for the project. We also acknowledge the support from The Nordic Academy of Advanced Studies via the visiting professorship for Dr Anna-Karin Borg-Karlson (project no. 010434) and a mobility stipend (project no 99.30.110-O) and the support from the Swedish Institute (Visby Program). Professor Wilfried A. König, University of Hamburg, Germany, is gratefully acknowledged for providing the chiral column and the enantiomeric reference samples, Dr Ezra Dunkelblum, The Volcani Centre, Bet Dagan, Israel for the insect material, Martha Isabel Ramirez, The Royal Institute of Technology, Stockholm, Sweden, for plant extracts, and Robert Biegler for comments on the manuscript.
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Accepted October 29, 2001
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