Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds

Shields, Vonnie D. C.; Hildebrand, John G.

doi:10.1007/s003590000165

Cited by 135 publications

(104 citation statements)

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“…1) were as follows: ocimene (3,7-dimethyl-1,3,6-octatriene; catalog #74730; ϳ95% pure; mixture of isomers) from Fluka (Buchs, Switzerland); benzyl alcohol (catalog #30519-7; 99.8% pure), cis-3-hexenyl butyrate (catalog #W340200; Ͼ98%), geraniol (trans-3,7-dimethyl-2,6-octadien-1-ol; catalog #G-5135; 98%), hexan-1-ol (catalog #47142; 99%; hereinafter referred to as hexanol), (Ϯ)linalool [(Ϯ)3,7-dimethyl-1,6-octadien-3-ol; catalog #L2602; 97% pure], methyl salicylate (methyl 2-hydroxybenzoate; catalog #240826; Ͼ99%), nerol (cis-3,7-dimethyl-2,6-octadien-1-ol; catalog #26890-9; 97%), nonanal (catalog #76310; Ͼ95%), phenylacetaldehyde (catalog #P0145; 95% pure), trans-2-hexenal (catalog #132659; 98% pure) from Sigma-Aldrich (St. Louis, MO); and cis-3-hexenyl acetate (c3HA) (catalog #H2137; Ͼ97%), cis-3-hexenyl propionate (catalog #P858; Ͼ97%), and cis-3-hexenyl benzoate (catalog #B1039; Ͼ98%) from Tokyo Chemical Industries (Tokyo, Japan). These compounds are found among the volatiles emitted by host plants of Manduca (Loughrin et al, 1990;Fraser et al, 2003;Raguso et al, 2003) and have been shown to evoke responses from the antenna (Fraser et al, 2003) (C. E. Reisenman, unpublished observations) and/or from olfactory receptor cells (ORCs) in trichoid type-A antennal sensilla in females (Shields and Hildebrand, 2001).…”

Section: Methodsmentioning

confidence: 99%

Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus

Reisenman¹,

Christensen²,

Hildebrand³

2005

J. Neurosci.

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The antennal lobe (AL) of insects, like the olfactory bulb of vertebrates, is characterized by discrete modules of synaptic neuropil called glomeruli. In some insects (e.g., moths and cockroaches), a few glomeruli are sexually dimorphic and function in labeled lines for processing of sensory information about sex pheromones. Controversy still exists, however, about whether projection (output) neurons (PNs) of glomeruli in the main AL are also narrowly tuned. We examined this critical issue in the AL of the moth Manduca sexta. We used intracellular recording and staining techniques to investigate the chemosensory tuning of PNs innervating an identifiable, sexually isomorphic glomerulus, G35, in the main AL. We found that the morphological features and chemosensory tuning of G35-PNs were nearly identical in females and males. G35-PNs responded to low concentrations of the plant-derived volatile compound cis-3-hexenyl acetate (c3HA), but the sensitivity threshold of female PNs was lower than that of male PNs. The propionate and butyrate homologs of c3HA could evoke excitatory responses but only at moderate-to-high concentrations. Other plant volatiles did not evoke responses from G35-PNs. Moreover, PNs innervating glomeruli near G35 (in females) showed little or no response to c3HA. Female G35-PNs were hyperpolarized by (Ϯ)linalool, a compound that excites PNs in an adjacent glomerulus, thus providing evidence for lateral-inhibitory interactions between glomeruli. Our results show that PNs arborizing in an identified glomerulus in the main olfactory pathway are morphologically and physiologically equivalent in both sexes and have characteristic, limited molecular receptive ranges that are highly conserved across individuals.

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Section: Methodsmentioning

confidence: 99%

Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus

Reisenman¹,

Christensen²,

Hildebrand³

2005

J. Neurosci.

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“…Mixture A was identical to the five-component mixture but without linalool (table 1). To further test the effectiveness of (þ)-linalool as an attractant for oviposition, we prepared a synthetic mixture (mixture B, The same concentration of either (2) responses in M. sexta olfactory receptor cells (Shields & Hildebrand 2000). The components of mixture B were pseudo-randomly selected from among those of the D. wrightii floral scent to be different from, but to represent the chemical classes of, the FVs in mixture A (i.e.…”

Section: (B) Feeding Experimentsmentioning

confidence: 99%

Antagonistic effects of floral scent in an insect–plant interaction

et al. 2010

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In southwestern USA, the jimsonweed Datura wrightii and the nocturnal moth Manduca sexta form a pollinator-plant and herbivore-plant association. Because the floral scent is probably important in mediating this interaction, we investigated the floral volatiles that might attract M. sexta for feeding and oviposition. We found that flower volatiles increase oviposition and include small amounts of both enantiomers of linalool, a common component of the scent of hawkmoth-pollinated flowers. Because (þ)-linalool is processed in a female-specific glomerulus in the primary olfactory centre of M. sexta, we hypothesized that the enantiomers of linalool differentially modulate feeding and oviposition. Using a synthetic mixture that mimics the D. wrightii floral scent, we found that the presence of linalool was not necessary to evoke feeding and that mixtures containing (þ)-and/or (2)-linalool were equally effective in mediating this behaviour. By contrast, females oviposited more on plants emitting (þ)-linalool (alone or in mixtures) over control plants, while plants emitting (2)-linalool (alone or in mixtures) were less preferred than control plants. Together with our previous investigations, these results show that linalool has differential effects in feeding and oviposition through two neural pathways: one that is sexually isomorphic and non-enantioselective, and another that is female-specific and enantioselective.

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“…Specific olfactory receptor cells of M. sexta females have been shown to respond to benzyl alcohol, benzyl benzoate, methyl benzoate and methyl salicylate but no receptor cells were found for eugenol and isoeugenol (Shields and Hildebrand 2001). EAG-recordings from the nocturnal hawk moth Sphinx perelegans (Raguso and Light 1998) yielded preferentially strong responses to the same three compounds, but benzaldehyde elicited a stronger response from the S. perelegans antennae than benzyl alcohol and methyl benzoate, the opposite of what was found here for M. sexta.…”

Section: P Axillaris Flower Emission Is Nocturnal and Controlled By mentioning

confidence: 99%

“…Work on the neurobiology of M. sexta olfaction dates back 30 years, comprising studies on interneurons in the brain (Itagaki and Hildebrand 1990), detection of sex pheromone components by olfactory receptor neurons (Kalinova´et al 2001), antennal olfactory receptor cells responses (Shields and Hildebrand 2001), glomerular organization of antennal lobes (Hildebrand 1996) and their importance for odour-modulated flight (Willis et al 1995). Some information also exists on the learning capability of this hawk moth species (Daly and Smith 2000;Daly et al 2001).…”

Section: Introductionmentioning

confidence: 99%

The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta

Hoballah

Stuurman

Turlings

et al. 2005

Planta

162

154

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The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta Abstract In the genus Petunia, distinct pollination syndromes may have evolved in association with bee-visitation (P. integrifolia spp.) or hawk moth-visitation (P. axillaris spp). We investigated the extent of congruence between floral fragrance and olfactory perception of the hawk moth Manduca sexta. Hawk moth pollinated P. axillaris releases high levels of several compounds compared to the bee-pollinated P. integrifolia that releases benzaldehyde almost exclusively. The three dominating compounds in P. axillaris were benzaldehyde, benzyl alcohol and methyl benzoate. In P. axillaris, benzenoids showed a circadian rhythm with an emission peak at night, which was absent from P. integrifolia. These characters were highly conserved among different P. axillaris subspecies and P. axillaris accessions, with some differences in fragrance composition. Electroantennogram (EAG) recordings using flower-blends of different wild Petunia species on female M. sexta antennae showed that P. axillaris odours elicited stronger responses than P. integrifolia odours. EAG responses were highest to the three dominating compounds in the P. axillaris flower odours. Further, EAG responses to odour-samples collected from P. axillaris flowers confirmed that odours collected at night evoked stronger responses from M. sexta than odours collected during the day. These results show that timing of odour emissions by P. axillaris is in tune with nocturnal hawk moth activity and that flower-volatile composition is adapted to the antennal perception of these pollinators.

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Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds

Cited by 135 publications

References 0 publications

Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus

Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus

Antagonistic effects of floral scent in an insect–plant interaction

The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta

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