Chemical Senses Advance Access originally published online on February 22, 2006
Chemical Senses 2006 31(4):325-334; doi:10.1093/chemse/bjj036
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Discrimination between Enantiomers of Linalool by Olfactory Receptor Neurons in the Cabbage Moth Mamestra brassicae (L.)
1 Neuroscience Unit, Department of Biology, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway and 2 Ecological Chemistry Group, Department of Chemistry, Royal Institute of Technology, SE-100 44 Stockholm, Sweden
Correspondence to be sent to: Stig Ulland, Neuroscience Unit, Department of Biology, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway. e-mail: stig.ulland{at}nt.ntnu.no
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
Plants emit complex blends of volatiles, including chiral compounds that might be detected by vertebrates and invertebrates. Insects are ideal model organisms for studying the underlying receptor neuron mechanisms involved in olfactory discrimination of enantiomers. In the present study, we have employed two-column gas chromatography linked to recordings from single olfactory receptor neurons of Mamestra brassicae, in which separation of volatiles in a polar and a chiral column was performed. We here present the response properties of olfactory receptor neurons tuned to linalool. The narrow tuning of these receptor neurons was demonstrated by their strong responses to (R)-(–)-linalool, the weaker responses to the (+)-enantiomer as well as a few structurally related compounds, and no responses to the other numerous plant released volatiles. The enantioselectivity was verified by parallel dose-response curves, that of (R)-(–)-linalool shifted 1 log unit to the left of the (S)-(+)-linalool curve. A complete overlap of the temporal response pattern was found when comparing the responses of the same strength. Analysis of the spike amplitude and waveform indicated that the responses to the two enantiomers originated from the same neuron.
Key words: enantiomeric discrimination, GC–SCR, Mamestra brassicae, olfactory receptor neurons, (R)-(–)-linalool
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
Chiral recognition by receptors and enzymes is well demonstrated in biochemical, pharmaceutical, and chemosensory research. Many chiral odorants are perceived by humans as different qualities and/or having different intensities (Friedman and Miller, 1971
; Leitereg et al., 1971; Pike et al., 1988; Ohloff, 1994; Brenna et al., 2003), like (R)-(–)-linalool which smells slightly different from (S)-(+)-linalool, and has a much stronger intensity (Christoph and Drawert, 1985). In contrast, the odor of other enantiomers may not be distinguished by humans (Ohloff, 1994). The importance of enantiomers in olfaction is well demonstrated in insects where optical configurations of pheromone components may be critical and contribute to population differences within species as well as to isolation between species (Tumlinson et al., 1977; Birch et al., 1980; Lanier et al., 1980; Hagaman and Cardè, 1984; Wallner et al., 1984). The presence of different olfactory receptor neurons (RNs) for these enantiomers have been demonstrated by extracellular recordings in several insect species (Mustaparta et al., 1980; Hansen et al., 1983; Wojtasek et al., 1998; Plettner et al., 2000; Nikonov and Leal, 2002).
Studies of herbivorous insects have also provided interesting data on RN detection of chiral compounds emitted by plants. Most interesting are the results obtained by the use of gas chromatography (GC), employing chiral columns linked to electrophysiological recordings from single olfactory RNs [gas chromatography–single cell recording (GC–SCR)] (Stranden et al., 2002, 2003a,b; Bichão et al., 2005b). This is because chiral GC is a means of providing optically pure compounds, which is a challenge when testing the effects of enantiomers. In three related heliothine moths, the sesquiterpene germacrene D, consisting of two enantiomers, activates a major group of RNs (Røstelien et al., 2000a; Stranden et al., 2003a). Stimulation with compounds eluting from a chiral column have shown that all the RNs responding to this compound in heliothine moths were tuned to (–)-germacrene D that has a 10-fold stronger effect than the (+)-enantiomer. A few other compounds of related structures had a weak effect. In the strawberry blossom weevil Anthonomus rubi, RNs tuned to germacrene D were found to have a similar enantioselectivity but differed in respect to other secondary odorants (Bichão et al., 2005a). RNs tuned to linalool have been found or indicated in several insect species, where linalool may act as a host plant attractant or repellent (Hori, 1998) or as a pheromone, or synergist to the pheromone (Ochieng et al., 2002; Borg-Karlson et al., 2003). In addition, other RN types tuned to plant odorants with a chiral center have been reported in various insect species. However, these RNs have not been tested with 100% pure enantiomers separated via chiral GC columns. We here present results obtained using GC–SCR with two different columns installed in parallel to stimulate enantioselective RNs tuned to linalool in the herbivorous moth species, Mamestra brassicae.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
Insects
Mamestra brassicae pupae were supplied by The Norwegian Crop Research Institute, Ås, Norway. The sexed pupae were stored in separate containers placed in climate chambers (22°C, 14:10h light:dark photoperiod, onset of dark cycle at 10:00 AM.). After eclosion, the adult insects were kept in cylindrical containers with access to water containing sucrose (5%). The age of adult insects used in the experiments ranged from 2 to 14 days. Both sexes were used in the experiments.
Chemicals and headspace samples
Volatiles were collected from several plant species by using a headspace technique (Byrne et al., 1975; Pham-Delegue et al., 1989; Wibe and Mustaparta, 1996; Røstelien et al., 2000b). The plants were placed in a closed oven bag through which purified air was sucked and led into glass tubes containing the adsorbents (Tenax TA and Porapak Q, 1:1). The air was purified by a filter of activated charcoal before the intake to the bag, and the collection was carried out for 24 or 48 h. The trapped volatiles were eluted with hexane and ethyl acetate (1:1) and stored in vials kept in a freezer. The plant materials used for collecting volatiles were Brassica oleracea, Brassica napus, and four ecotypes of Arabidopsis thaliana. Table 1 gives an overview of the headspace samples, essential oils, standard mixtures, and single compounds used to stimulate the RNs via the GC.
|
Direct stimulation via cartridges
Direct stimulation via glass cartridges was used for screening of RN sensitivity to the various samples of headspace and other mixtures. Five microliters of each test sample was applied to a filter paper placed inside the cartridge letting the solvent evaporate before use. The RN was exposed for the test sample by puffing air (8 ml/s) through the cartridge and over the antenna. Direct stimulation via glass cartridges was also used for determining dose-response curves. In these tests, 100 µl of each dilution of linalool enantiomers (decadic steps) was applied to a filter paper, and the solvent was evaporated by N2 flow before inserting the filter paper into the glass cartridge. This resulted in test tubes containing the following amounts of linalool: 0.01 ng, 0.1 ng, 1 ng, 0.01 µg, 0.1 µg, and 1 µg. In dose-response experiments, using direct stimulation, the tests started with concentrations below the detection limit of the RN and continued toward higher concentrations. Between the stimulations, the antenna was exposed to a continuous flow (500 ml/min) of purified air. The interstimulus interval varied from 30 s at low concentrations to 3 min at high concentrations.
GC linked to single-cell recordings, GC–SCR
The insects were mounted in a Plexiglas holder, and the head and antennae were stabilized with tape and wax as described by Røstelien et al. (2000b). Electrophysiological recordings from single RNs were made by the use of electrolytically sharpened tungsten microelectrodes; the recording electrode placed into the base of a sensillum and the reference electrode into the base of the antenna. The neurons were initially screened for responses to mixtures of plant odors and single compounds via cartridges. When responding, 0.5–1 µl of the solution was injected into the column of the GC. The column was equipped with a splitter at the end, leading half of the effluent to the flame ionization detector (FID) and the other half into a constant airflow (500 ml/min) blowing over the insect antenna (Røstelien et al., 2000b). This made it possible, together with the simultaneous single-cell recording, to determine which compounds in the mixture elicited the responses. The spike rate and the gas chromatogram were recorded using EAD software (Syntech, Netherlands), while the spikes were recorded and stored using Spike2 software (Cambridge Electronic Design Limited, Cambridge, Great Britain). The GC was equipped with two columns of different separation properties, installed in parallel (Stranden et al., 2002). In the present experiments, we used a DBwax [25 m, inner diameter (i.d.) 0.25 mm, film thickness 0.25 µm, J&W Scientific, Agilent Technologies, Palo Alto, CA] and a chiral column [25 m, i.d. 0.25 mm, octakis (6-O-methyl-2,3-di-O-pentyl)-
-cyclodextrin (80% in OV 1701), König et al., 1990]. Separation in the polar column was performed with two different programs, the first and most frequently used program starting at 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. The second program was used to achieve better separation of the compounds in some of the headspace samples: performed from the initial temperature 50°C isothermal for 2 min followed by a 3°C/min increase to 180°C and a final increase of 15°C/min to 220°C. In the chiral column, enantiomeric separation of linalool, dihydrolinalool, and tetrahydrolinalool was optimal at the isothermal temperature 80°C. The FID temperature was set to 230°C for all programs. The GC was equipped with a cold on–column injector.
Spike analysis and cell classification
The spikes from RNs were analyzed using the Spike2 software. Separation of the cell types in one recording was based on differences in spike amplitudes and waveforms. The RNs were classified according to which odorant elicited the strongest response (primary odorant) as well as those having weaker effects (secondary odorants).
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
General response characteristics
Excitation and temporal response pattern
Out of 43 olfactory RNs recorded in M. brassicae females and males, 12 neurons responded best to the plant volatile linalool. The 12 RNs were obtained in six females and six males. Altogether, the RNs were tested 89 times via the GC (GC = 89), out of which 49 tests were performed on the same neuron (Table 1, RN no. I). In 30 out of the 49 tests, this neuron responded strongly to linalool present in the various headspace samples of host and nonhost plants as well as to synthetic linalool. In addition, the other RNs tested repeatedly with samples containing linalool demonstrated reproducibility of the responses, which appeared as increased firing rate upon stimulation with linalool (Figure 1A). Three other compounds elicited weaker responses in the most sensitive neurons. No inhibition was observed. When stimulating via the GC, the firing rate of the RNs followed the concentration profile of the active GC peak, regaining the spontaneous activity within half a minute or a few minutes. Responses to high concentrations elicited responses that far outlasted the GC peak. Most of the 12 RNs showed responses also to the solvents hexane and ethyl acetate. Stimulation directly with linalool via cartridges, giving a fast onset and more constant concentration profile, showed a phasic-tonic response pattern. After stimulation with high concentrations of linalool, the RNs showed adaptation which might last for several minutes. Most recordings presented from the GC–SCR indicated activity of two or three RNs responding to different compounds. The responses of the RNs were distinguished based on spike analysis in the Spike2 software. Similar amplitudes and waveforms of the spikes were ascribed to the same RN.
|
Concentration dependency
Ten out of the twelve RNs responded to linalool at low concentrations. The threshold concentration for the most sensitive neurons was approximately 0.5 ng of racemic linalool when tested via the polar GC column. Dose-dependent excitation was shown by stimulation with decadic increase of concentrations over 5 log units. As shown in Figure 1B, the most sensitive linalool RN displayed an approximately linear increase of the firing frequency over the three highest concentrations (5 ng–0.5 µg), reaching a maximum firing rate of more than 200 spikes/s. The temporal response pattern of the same RN when stimulated with the three highest concentrations is shown in Figure 1C. The firing rate of the neuron increased from the onset of the stimulus, that is, when the GC peak appeared, reaching a maximum after 300–400 ms at the peak of the concentration profile. During the high firing frequency of the strongest response, the spike amplitude decreased below the noise level making spike counting difficult. This was the cause of the apparently rapid drop in spike frequency in Figure 1C. Nevertheless, recovery of spike amplitude showed that the actual spike frequency recovered fairly quickly toward baseline levels, that is, to about 50% of maximum within 5 s.
The molecular receptive range and enantioselectivity
Stimulation with compounds eluting from the polar column
The molecular receptive range was described by stimulating the neurons with headspace samples, essential oils, and synthetic compounds via the polar GC column. Figure 2A shows the gas chromatogram of the headspace sample of the host plant B. oleracea var. italica and the simultaneously recorded activity of a single RN. The response appeared at the retention time of linalool (11.29 min), present in trace amount below the detection limit of the FID. In addition, weak responses to two other compounds appeared at the retention times 12.47 and 14.07 min. The trace amount did not allow identification of these two compounds by GC–mass spectrometry. Responses during the elution of the large amounts of the solvents (hexane and ethyl acetate) were also obtained in this type of neuron of high sensitivity. When stimulating with the headspace sample of A. thaliana, the most sensitive neurons responded during the elution of the two solvents and at the retention time (11.29 min) of linalool (Figure 2B). Also in this sample, the amount of linalool was below the detection limit of the FID. Altogether, six headspace samples of Brassica spp. and A. thaliana and two essential oils were tested on this neuron, all eliciting responses at the retention time of linalool. Racemic linalool injected in the polar column elicited one strong response to the linalool peak. Also, a weaker response to dihydrolinalool appeared before the elution of linalool. In addition, weak responses were obtained to two structurally related compounds, tetrahydrolinalool and 1-octen-3-ol (Figure 2C). The selectivity for linalool was further demonstrated by no responses to the numerous other compounds present in the standards and headspace samples tested.
|
Stimulation with compounds eluting from the chiral column
Eight of the twelve RNs (RN no. I, II, V, VIII–XII) were tested with compounds eluted from the chiral column. All of them showed enantioselectivity by responding stronger to (R)-(–)-linalool than to (S)-(+)-linalool. Approximately a 10-fold stronger effect of the (–)-enantiomer than of (S)-(+)-linalool was found for all eight neurons. This is illustrated for RN no. I in Figure 3A where the concentrations 0.05 µg of (R)-(–)-linalool and 0.5 µg of (S)-(+)-linalool elicited the same firing frequencies. Analysis of the spikes of the two responses showed similar amplitudes and waveforms, indicating that they originated from the same neuron. The 10-fold difference in stimulatory effect was also shown by the dose-response curves obtained by direct stimulation, the (R)-(–)-linalool curve shifted 1 log unit to the left of the (S)-(+)-linalool curve (Figure 3B). Enantioselectivity was also found for the responses to dihydrolinalool and tetrahydrolinalool by two RNs (RN no. I and XII) stimulated with the compounds eluted from the chiral GC column (Figure 3C). However, the elution sequence of these enantiomers in the chiral column is not known. Comparison of the responses to 0.05 µg (R)-(–)-linalool and to 0.5 µg (S)-(+)-linalool showed complete overlap of the temporal response pattern (Figure 3D).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
Discrimination between odors is based on the presence of a large number of olfactory receptor protein types, each expressed in subsets of sensory neurons, as shown in various vertebrates and insects (Buck and Axel, 1991
; Clyne et al., 1999; Krieger and Breer, 1999; Mombaerts, 1999; Vosshall, 2001). The convergence of axons belonging to one subtype in one or two specific glomeruli in the primary olfactory center, the olfactory bulb in vertebrates, and antennal lobe in insects further elucidate the principle called "the molecular logic of smell" (Axel, 1995). Depending on the tuning of the receptors, the information about one compound may be mediated by one or several types of RNs resulting in activation of one or more glomeruli. Among the olfactory RN types recorded in M. brassicae, the neurons tuned to linalool constituted the largest group. They all showed similar functional characteristics, indicating that M. brassicae detect linalool by one type of RNs that has a narrow tuning to (R)-(–)-linalool. This RN type is 10 times more sensitive to (R)-(–)-linalool than to (S)-(+)-linalool and show the same temporal response pattern to the two enantiomers. It suggests that M. brassicae perceive the odors of these enantiomers as similar quality but with different intensity. Although RNs tuned to (S)-(+)-linalool have not been found in this species, we can not exclude the possibility that they might be present among the large number of olfactory RNs responding to plant odors, for example, indicated by the numerous ordinary glomeruli (67 ± 1) in the antennal lobe of this species (Rospars, 1983). It is also possible that the two enantiomers of linalool have differential effects on RNs tuned to other compounds, resulting in different across-glomerular stimulation patterns and behavioral discrimination. In another insect species, the strawberry blossom weevil A. rubi, two types of linalool RNs have been described, one tuned to the (S)-(+)-linalool and the other to the (R)-(–)-linalool, both showing considerably lower sensitivity to the opposite enantiomer (Bichão et al., 2005b). So far, the results obtained in these two species indicate that the strawberry blossom weevil may easily discriminate between the two enantiomers, whereas M. brassicae may perceive these odors as being of the same or similar quality. How the information about the two enantiomers is represented by specific glomerular activation is not known in these species. However, in another species of moths Manduca sexta, two specific glomeruli have been identified that receive enantioselective information about linalool (Reisenman et al., 2004). According to these results, M. sexta certainly possesses at least two populations of RNs that discriminate linalool enantiomers. In fact, another study of linalool responding RNs of M. sexta showed individual variations of the molecular receptive ranges when directly stimulated with numerous selected compounds (Shields and Hildebrand, 2001). It would be interesting to test these neurons by GC-SCR and with the same protocol as in M. brassicae, for comparison of specificity and enantioselectivity.
Linalool is a typical floral constituent produced in a wide range of plants. It is synthesized via a condensation of dimethyl allyl pyrophosphate and isopenthyl pyrophosphate to geranyl diphosphate (GPP) and converted to linalool in a reaction catalyzed by linalool synthase, which is enantioselective (Dudareva et al., 1996; Cseke et al., 1998). Both enantiomers of linalool are present in many plant species, but in a few species only one of them is present (Borg-Karlson et al., 1996; Casabianca et al., 1998). Each inflorescence can produce its own specific composition of the enantiomers (A.-K. Borg-Karlson, unpublished data). It is not known whether M. brassicae moths uses a narrow or a broad range of flowering plants for nectar feeding, but their larvae are particularly associated with plants of the genus Brassica (Skou, 1991). The enantiomeric ratio of linalool released by these host plants has previously not been reported and was not investigated in the present study by separating headspace samples in the chiral column. However, in A. thaliana (Columbia ecotype) of the same family, Brassicaceae, a larger amount of (R)-(–)-linalool than (S)-(+)-linalool is emitted (ratio 2:1) (Chen et al., 2003). Furthermore, a gene coding for a protein involved in catalyzing GPP to pure (S)-(+)-linalool has been identified, which implies that there is also a particular gene coding for the (–)-enantiomer. Emission of linalool in A. thaliana (Columbia ecotype) is shown exclusively from the flowering parts, and the release is continuous with no indications of induction by stress (J. Gershenzon, personal communication). If Brassicaceae plants have a similar distribution of linalool enantiomers, we may assume that M. brassicae uses (R)-(–)-linalool as a cue in the nectar feeding and not in the oviposition. In fact, in wind tunnel experiments, mated M. brassicae females did not show upwind flight to stimulation with linalool (Rojas, 1999).
Important in demonstrating enantioselectivity of RNs is to obtain an optimal separation in the chiral GC column. This is in order to make the sensory neurone able to recover enough from adaptation to the first eluted enantiomer before stimulated with the second one, which was the case in the present study. The RN responded to (S)-(+)-linalool although it eluted after the stronger response to (R)-(–)-linalool. The 10-fold difference of the stimulatory effect of the (–)- and (+)-enantiomers also demonstrated by direct stimulation corresponds to what is found in other enantioselective plant odor RNs in insects when stimulated via the chiral GC column (Stranden et al., 2002, 2003a; Bichão et al., 2005a). The molecular properties of enantiomers are interesting in considering odor-receptor interactions. The present results show that the chiral center at carbon 3 in the linalool molecule is important in the interaction with the receptor of M. brassicae. The molecule with hydroxyl group in R configuration at carbon 3 in combination with the allylic double bond elicits the highest response, followed by the S configuration. A similar ratio of the stimulatory effect can be assumed for the corresponding configurations of the weaker stimulants dihydrolinalool and tetrahydrolinalool, for which the sequence of elution is not known. When stimulating with the smaller molecule, 1-octen-3-ol, lacking both of the methyl groups at carbon 3 and 7, the response is even more reduced. Speculations about the binding between the receptor protein and the linalool enantiomers are difficult without knowing the amino acid sequence of the binding area of the receptor protein.
Because the linalool enantiomers are common in many plant species, it would be interesting to know the enantioselectivity of the receptors in insects of different genera and families as well as in vertebrates. Based on this, it might be possible to figure out why the receptors for detecting these enantiomers have evolved similar or different specificities across species and why some species have one and others have two types of enantioselective linalool receptors.
|
Acknowledgements |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
The project was financed by the Norwegian Research Council project No. 143250/I10 (Project coordinator Prof. Atle Bones, Department of Biology, Norwegian University of Science and Technology). We also acknowledge the Royal Institute of Technology and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) for financial support to Anna-Karin Borg-Karlson. Stein Winæs and Dr Richard Meadow at The Norwegian Crop Research Institute, Ås have kindly supplied the insect material and Atle Bones the Arabidopsis ecotypes.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAcknowledgementsReferences |
|---|
Axel, R. (1995) The molecular logic of smell. Sci. Am., 273, 154–159.[Web of Science][Medline]
Bichão, H., Borg-Karlson, A.-K., Araújo, J. and Mustaparta, H. (2005a) Five types of olfactory receptor neurons in the strawberry blossom weevil Anthonomus rubi: selective responses to inducible host-plant volatiles. Chem. Senses, 30, 153–170.
Bichão, H., Borg-Karlson, A.-K., Wibe, A., Araújo, J. and Mustaparta, H. (2005b) Molecular receptive ranges of olfactory receptor neurones responding selectively to terpenoids, aliphatic green leaf volatiles and aromatic compounds, in the strawberry blossom weevil Anthonomus rubi. Chemoecology, 15, 211–226.[CrossRef]
Birch, M.C., Light, D.M., Wood, D.L., Browne, L.E., Silverstein, R.M., Bergot, B.J., Ohloff, G., West, J.R. and Young, J.C. (1980) Pheromonal attraction and allomonal interruption of Ips pini in California by the two enantiomers of ipsdienol. J. Chem. Ecol., 6, 703–717.[CrossRef][Web of Science]
Borg-Karlson, A.-K., Tengö, J., Valterová, I., Unelius, C.R., Taghizadeh, T., Tolasch, T. and Francke, W. (2003) (S)-(+)-Linalool, a mate attractant pheromone component in the bee Colletes cunicularius. J. Chem. Ecol., 29, 1–14.[CrossRef][Web of Science][Medline]
Borg-Karlson, A.-K., Unelius, C.R., Valterova, I. and Nilsson, L.A. (1996) Floral fragrance chemistry in the early flowering shrub Daphne mezereum. Phytochemistry, 41, 1477–1483.[CrossRef]
Brenna, E., Fuganti, C. and Serra, S. (2003) Enantioselective perception of chiral odorants. Tetrahedron: Assymetr., 14, 1–42.
Buck, L. and Axel, R. (1991) A novel multigene family may encode odorant receptors: a molecular basis for odour recognition. Cell, 65, 175–187.[CrossRef][Web of Science][Medline]
Byrne, K.J., Gore, W.E., Pearce, G.T. and Silverstein, R.M. (1975) Porapak-Q collection of airborne organic compounds serving as models for insect pheromones. J. Chem. Ecol., 1, 1–7.
Casabianca, H., Graff, J.B., Faugier, V., Fleig, F. and Grenier, C. (1998) Enantiomeric distribution studies of linalool and linalyl acetate. J. High Resolut. Chromatogr., 21, 107–112.
Chen, F., Tholl, D., D'Auria, J.C., Farooq, A., Pichersky, E. and Gershenzon, J. (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell, 15, 1–14.
Christoph, N. and Drawert, F. (1985) Olfactory thresholds of odour stimuli determined by gas chromatographic sniffing technique; structure-activity relationships. In Berger, R.G., Nitz, S., Schreier, P., Eichhorn, H. and Marzling-Hangenham (eds), Proceedings of the International Conference on Topics in Flavor Research. Freising-Weihenstephan.
Clyne, P.J., Warr, C.G., Freeman, M.R., Lessing, D., Kim, J. and Carlson, J.R. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron, 22, 327–338.[CrossRef][Web of Science][Medline]
Cseke, L., Dudareva, N. and Pichersky, E. (1998) Structure and evolution of linalool synthase. Mol. Biol. Evol., 15, 1491–1498.
Dudareva, N., Cseke, L., Blanc, V.M. and Pichersky, E. (1996) Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell, 8, 1137–1148.[Abstract]
Friedman, L. and Miller, J.G. (1971) Odour incongruity and chirality. Science, 172, 1044–1046.
Hagaman, T.E. and Cardè, R.T. (1984) Effect of pheromone concentrations on organization of preflight behaviours of the male gypsy moth, Lymantria dispar (L.). J. Chem. Ecol., 10, 17–23.
Hansen, K., Schneider, D. and Boppré, M. (1983) Chiral pheromone and reproductive isolation between the gypsy- and nun moth. Naturwissenschaften, 70, 466–467.[CrossRef]
Hori, M. (1998) Repellency of rosemary oil against Myzus persicae in a laboratory and in a screenhouse. J. Chem. Ecol., 24, 1425–1432.[CrossRef]
König, W.A., Icheln, D., Runge, T., Pforr, I. and Krebs, A. (1990) Cyclodextrins as chiral stationary phases in capillary gas chromatography, part VII: cyclodextrins with an inverse substitution pattern—synthesis and enantioselectivity. J. High Resolut. Chromatogr., 13, 702–707.[CrossRef]
Krieger, J. and Breer, H. (1999) Olfactory reception in invertebrates. Science, 286, 720–723.
Lanier, G.N., Classon, A., Stewart, T., Piston, J.J. and Silverstein, R.M. (1980) Ips pini: the basis for interpopulational differences in pheromone biology. J. Chem. Ecol., 6, 677–687.[CrossRef][Web of Science]
Leitereg, T.J., Guadagni, D.G., Harris, J., Mon, T.R. and Teranishi, R. (1971) Chemical and sensory data supporting the difference between the odours of the enantiomeric carvones. J. Agric. Food Chem., 19, 785.[CrossRef]
Mombaerts, P. (1999) Molecular biology of odorant receptors in vertebrates. Annu. Rev. Neurosci., 22, 487–509.[CrossRef][Web of Science][Medline]
Mustaparta, H., Angst, M.E. and Lanier, G.N. (1980) Receptor discrimination of enantiomers of the aggregation pheromone ipsdienol, in two species of Ips. J. Chem. Ecol., 6, 689–701.[CrossRef]
Nikonov, A.A. and Leal, W.S. (2002) Peripheral coding of sex pheromone and a behavioural antagonist in the Japanese beetle, Popillia japonica. J. Chem. Ecol., 28, 1075–1089.[CrossRef][Web of Science][Medline]
Ochieng, S.A., Park, K.C. and Baker, T.C. (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurones in male Helicoverpa zea. J. Comp. Physiol. A, 188, 325–333.
Ohloff, G. (1994) Scent and fragrances. The fascination of odours and their chemical perspectives. Springer Verlag, Heidelberg, Berlin.
Pham-Delegue, M.H., Etievant, P., Guichard, E. and Masson, C. (1989) Sunflower volatiles involved in honeybee discrimination among genotypes and flowering stages. J. Chem. Ecol., 15, 329–343.
Pike, L.M., Enns, M.P. and Hornung, D.E. (1988) Quality and intensity of carvone enantiomers when tested separately and in mixtures. Chem. Senses, 13, 307–309.
Plettner, E., Lazar, J., Prestwich, E.G. and Prestwich, G.D. (2000) Discrimination of pheromone enantiomers by two pheromone binding proteins from the gypsy moth Lymantria dispar. Biochemistry, 39, 8953–8962.[CrossRef][Medline]
Reisenman, C.E., Christensen, T.A., Francke, W. and Hildebrand, J.G. (2004) Enantioselectivity of projection neurons innervating identified olfactory glomeruli. J. Neurosci., 24, 2602–2611.
Rojas, J.C. (1999) Electrophysiological and behavioural responses of the cabbage moth to plant volatiles. J. Chem. Ecol., 25, 1867–1883.[CrossRef]
Rospars, J.P. (1983) Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae and a butterfly Pieris brassicae. J. Comp. Neurol., 220, 80–96.[CrossRef][Web of Science][Medline]
Røstelien, T., Borg-Karlson, A.-K., Fäldt, J., Jacobsson, U. and Mustaparta, H. (2000a) The plant sesquiterpene germacrene D specifically activates a major type of antennal receptor neuron of the tobacco budworm moth Heliothis virescens. Chem. Senses, 25, 141–148.
Røstelien, T., Borg-Karlson, A.-K. and Mustaparta, H. (2000b) Selective receptor neurone responses to E-ß-ocimene, ß-myrcene, E,E-
-farnesene and homo-farnesene in the moth Heliothis virescens, identified by gas chromatography linked to electrophysiology. J. Comp. Physiol. A, 186, 833–847.[CrossRef][Medline]
Shields, V.D.C. and Hildebrand, J.G. (2001) Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds. J. Comp. Physiol. A, 186, 1135–1151.[CrossRef]
Skou, P. (1991) Nordens Ugler. Håndbog over de i Danmark, Norge, Sverige, Finland og Island forekommende arter af Herminiidae og Noctuidae (Lepidoptera). Apollo Books, Stenstrup.
Stranden, M., Borg-Karlson, A.-K. and Mustaparta, H. (2002) Receptor neuron discrimination of the germacrene D enantiomers in the moth Helicoverpa armigera. Chem. Senses, 27, 143–152.
Stranden, M., Liblikas, I., König, W.A., Almaas, T.J., Borg-Karlson, A.-K. and Mustaparta, H. (2003a) (–)-Germacrene D receptor neurones in three species of heliothine moths: structure-activity relationships. J. Comp. Physiol. A, 189, 563–577.[CrossRef]
Stranden, M., Røstelien, T., Liblikas, I., Almaas, T.J., Borg-Karlson, A.-K. and Mustaparta, H. (2003b) Receptor neurones in three heliothine moths responding to floral and inducible plant volatiles. Chemoecology, 13, 143–154.[CrossRef]
Tumlinson, J.H., Glein, M.G., Doolittle, R.E., Ladd, T.L. and Proveaux, A.T. (1977) Identification of the female Japanese beetle sex pheromone: inhibition of male response by an enantiomer. Science, 197, 789–792.
Vosshall, L.B. (2001) The molecular logic of olfaction in Drosophila. Chem. Senses, 26, 207–213.
Wallner, W.E., Cardé, R.T., Xu-Chonghua, Weselhof, R.M., Xilin, S., Jingjun, Y. and Schaefer, P.W. (1984) Gypsy moth (Lymantria dispar L.) attraction to disparlure enantiomers and the olefin precursor in the people's republic of China. J. Chem. Ecol., 10, 753–757.[CrossRef]
Wibe, A. and Mustaparta, H. (1996) Encoding of plant odours by receptor neurons in the pine weevil (Hylobius abietis) studied by linked gas chromatography-electrophysiology. J. Comp. Physiol. A, 179, 331–344.
Wojtasek, H., Hansson, B.S. and Leal, W.S. (1998) Attracted or repelled?—a matter of two neurons, one pheromone binding protein and a chiral center. Biochem. Biophys. Res. Commun., 250, 217–222.[CrossRef][Web of Science][Medline]
Accepted January 20, 2006
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  S. Ulland, E. Ian, M. Stranden, A.-K. Borg-Karlson, and H. Mustaparta Plant Volatiles Activating Specific Olfactory Receptor Neurons of the Cabbage Moth Mamestra brassicae L. (Lepidoptera, Noctuidae) Chem Senses, July 1, 2008; 33(6): 509 - 522. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Thakeow, S. Angeli, B. Weissbecker, and S. Schutz Antennal and Behavioral Responses of Cis boleti to Fungal Odor of Trametes gibbosa Chem Senses, April 1, 2008; 33(4): 379 - 387. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Ulland, E. Ian, R. Mozuraitis, A.-K. Borg-Karlson, R. Meadow, and H. Mustaparta Methyl Salicylate, Identified as Primary Odorant of a Specific Receptor Neuron Type, Inhibits Oviposition by the Moth Mamestra Brassicae L. (Lepidoptera, Noctuidae) Chem Senses, January 1, 2008; 33(1): 35 - 46. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||