Odorant reception in the malaria mosquito Anopheles gambiae

Carey, Allison F.; Wang, Guirong; Su, Chih‐Ying; Zwiebel, Laurence J.; Carlson, John R.

doi:10.1038/nature08834

Cited by 520 publications

(663 citation statements)

References 41 publications

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“…The analysis provides a foundation for elucidating the circuitry that translates receptor responses into behavior. including receptors of Drosophila adults (13,17) and larvae (8), and of mosquitoes (18).…”

Section: Significancementioning

confidence: 99%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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107

184

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The ability of an animal to detect, discriminate, and respond to odors depends on the function of its olfactory receptor neurons (ORNs), which in turn depends ultimately on odorant receptors. To understand the diverse mechanisms used by an animal in olfactory coding and computation, it is essential to understand the functional diversity of its odor receptors. The larval olfactory system of Drosophila melanogaster contains 21 ORNs and a comparable number of odorant receptors whose properties have been examined in only a limited way. We systematically screened them with a panel of ∼500 odorants, yielding >10,000 receptor-odorant combinations. We identify for each of 19 receptors an odorant that excites it strongly. The responses elicited by each of these odorants are analyzed in detail. The odorants elicited little cross-activation of other receptors at the test concentration; thus, low concentrations of many of these odorants in nature may be signaled by a single ORN. The receptors differed dramatically in sensitivity to their cognate odorants. The responses showed diverse temporal dynamics, with some odorants eliciting supersustained responses. An intriguing question in the field concerns the roles of different ORNs and receptors in driving behavior. We found that the cognate odorants elicited behavioral responses that varied across a broad range. Some odorants elicited strong physiological responses but weak behavioral responses or weak physiological responses but strong behavioral responses.T he olfactory system of the Drosophila larva achieves remarkable function with minimal structure. It detects and responds to spatial and temporal gradients of odorants, transforming chemical information into navigation via an elegant repertoire of head sweeps, runs, and turns (1-3). Its sophisticated function is based on the activities of 21 olfactory receptor neurons (ORNs), which innervate the dorsal organ of the head and send axons to the antennal lobe of the brain (4). The activities of the ORNs are in turn based on the responses of odor receptors (Ors). Thus, to understand the molecular basis of larval olfactory navigation, it is necessary to understand the function of the receptors.ORNs together express 25 members of the Or family of odor receptors and the Orco coreceptor (5-8). In each ORN, an Or and Orco together form a ligand-gated ion channel (9-11). Most ORNs express a single Or, although one ORN coexpresses Or94a and Or94b and another ORN coexpresses Or33b and Or47a (7). The significance of this coexpression remains speculative, but the response profiles of some coexpressed adult Ors are additive (12).The responses of the larval Or repertoire to a limited odorant panel was previously examined in an in vivo expression system known as the empty neuron system (8, 13). With the use of this system, 21 of the larval Ors were found to be functional. However, studies of the larval Or repertoire have been limited not only in the number of odorants examined, but also in their consideration of receptor sensitivity, tempor...

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Section: Significancementioning

confidence: 99%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

107

184

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“…In mammals, the so-called 'generalists' can be found, which have a broad receptive range (see [83]), but also in insects, studies have demonstrated that most receptors are sensitive to more than one substance [87 -89]. Overall, we can say that insects as well as mammals are sensitive to a broad range of chemicals of different structures and different classes [87,90] and although the overall number of chemical substances that can be detected is unknown, rough estimates suggest that rodents can detect several thousands or even tens of thousands of odorant molecules [83].…”

Section: The Dynamic Evolution Of Chemical Communication and Receivermentioning

confidence: 99%

“…Whereas some aromatics are major components in human emanations, A. gambiae's hosts, esters are often generated by fermentation processes and may therefore be used by D. melanogaster to find its food source. Likewise, phytophagous insects, but not Drosphila, have a large variety of ORs to detect and discriminate among terpenoids-a major chemical class emitted by plants [82,90].…”

Section: The Dynamic Evolution Of Chemical Communication and Receivermentioning

confidence: 99%

The origin and dynamic evolution of chemical information transfer

2010

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Although chemical communication is the most widespread form of communication, its evolution and diversity are not well understood. By integrating studies of a wide range of terrestrial plants and animals, we show that many chemicals are emitted, which can unintentionally provide information (cues) and, therefore, act as direct precursors for the evolution of intentional communication (signals). Depending on the content, design and the original function of the cue, there are predictable ways that selection can enhance the communicative function of chemicals. We review recent progress on how efficacybased selection by receivers leads to distinct evolutionary trajectories of chemical communication.Because the original function of a cue may channel but also constrain the evolution of functional communication, we show that a broad perspective on multiple selective pressures acting upon chemicals provides important insights into the origin and dynamic evolution of chemical information transfer. Finally, we argue that integrating chemical ecology into communication theory may significantly enhance our understanding of the evolution, the design and the content of signals in general.

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“…Indeed, we identified an oviposition attractant-sensitive OR from the Southern house mosquito, Culex quinquefasciatus (16), by mining the Culex genome for putative receptors with amino acid sequences related to an OR identified from the malaria mosquito, Anopheles gambiae, which detected related semiochemicals (16,17). Likewise, AaegOR8 from the yellow fever mosquito, Aedes aegypti, showed high amino acid identity to the malaria mosquito counterpart, AgamOR8, and both receptors were highly sensitive to 1-octen-3-ol (16)(17)(18). This assumption might not hold true for species from different orders, however, as suggested by the low amino acid identity between BmorOR1 and DmelOR7a (17%).…”

Section: Bombykol Elicits Significantly Higher Responses In Flies Thamentioning

confidence: 99%

Bombykol receptors in the silkworm moth and the fruit fly

Syed¹,

Kopp

Kimbrell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Male moths are endowed with odorant receptors (ORs) to detect species-specific sex pheromones with remarkable sensitivity and selectivity. We serendipitously discovered that an endogenous OR in the fruit fly, Drosophila melanogaster, is highly sensitive to the sex pheromone of the silkworm moth, bombykol. Intriguingly, the fruit fly detectors are more sensitive than the receptors of the silkworm moth, although its ecological significance is unknown. By expression in the "empty neuron" system, we identified the fruit fly bombykol-sensitive OR as DmelOR7a (= DmOR7a). The profiles of this receptor in response to bombykol in the native sensilla (ab4) or expressed in the empty neuron system (ab3 sensilla) are indistinguishable. Both WT and transgenic flies responded with high sensitivity, in a dose-dependent manner, and with rapid signal termination. In contrast, the same empty neuron expressing the moth bombykol receptor, BmorOR1, demonstrated low sensitivity and slow signal inactivation. When expressed in the trichoid sensilla T1 of the fruit fly, the neuron housing BmorOR1 responded with sensitivity comparable to that of the native trichoid sensilla in the silkworm moth. By challenging the native bombykol receptor in the fruit fly with high doses of another odorant to which the receptor responds with the highest sensitivity, we demonstrate that slow signal termination is induced by overdose of a stimulus. As opposed to the empty neuron system in the basiconic sensilla, the structural, biochemical, and/or biophysical features of the sensilla make the T1 trichoid system of the fly a better surrogate for the moth receptor.S ince the identification of bombykol (IUPAC name (10E,12Z)-hexadeca-10,12-dien-1-ol) as a sex pheromone for the silkworm moth, Bombyx mori (1), hundreds of sex pheromones have been identified from lepidopteran species (2). In general, femaleproduced sex pheromones in moths are complex mixtures of straight-chain acetates, aldehydes, and alcohols, with 10-12 carbon atoms and up to three unsaturations (3). This fatty acid-derived semiochemistry (4, 5) is unique to chemical communication in moths, although (7Z)-dodec-7-en-1-yl acetate also has been identified as a sex pheromone for the Asian elephant, Elephas maximus (6). Male moths detect these sex pheromones with such high selectivity and sensitivity that minimal structural modifications render them inactive (7), whereas a single molecule of bombykol is estimated to be sufficient to activate olfactory receptor neurons (ORNs) in male antennae of the silkworm moth (8). These species-specific communication channels seem to have evolved under a strong evolutionary pressure into a sophisticated signal receptor system. In contrast, we have serendipitously identified an ORN housed in the ab4 basiconic sensilla in the antennae of the fruit fly, Drosophila melanogaster, which responds to bombykol with high sensitivity (9), although the ecological significance of this bombykol detector in the fruit fly remains enigmatic. The OR housed in the ab4a neuron was pr...

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Odorant reception in the malaria mosquito Anopheles gambiae

Cited by 520 publications

References 41 publications

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Functional diversity among sensory receptors in a Drosophila olfactory circuit

The origin and dynamic evolution of chemical information transfer

Bombykol receptors in the silkworm moth and the fruit fly

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