Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context

435

427

CO2 elicits a response from many insects, including mosquito vectors of diseases such as malaria and yellow fever, but the molecular basis of CO2 detection is unknown in insects or other higher eukaryotes. Here we show that Gr21a and Gr63a, members of a large family of Drosophila seven-transmembrane-domain chemoreceptor genes, are coexpressed in chemosensory neurons of both the larva and the adult. The two genes confer CO2 response when coexpressed in an in vivo expression system, the ''empty neuron system.'' The response is highly specific for CO2 and dependent on CO2 concentration. The response shows an equivalent dependence on the dose of Gr21a and Gr63a. None of 39 other chemosensory receptors confers a comparable response to CO2. The identification of these receptors may now allow the identification of agents that block or activate them. Such agents could affect the responses of insect pests to the humans they seek.chemoreceptors ͉ insect ͉ Gr genes

Section: Gr21a and Gr63asupporting

confidence: 86%

mentioning

confidence: 99%

See 1 more Smart Citation

The molecular basis of CO ₂ reception in Drosophila

Kwon

Dahanukar

Weiss

et al. 2007

435

427

“…We note that an earlier study observed a repellent effect of geranyl acetate (8); we do not know the basis of this difference, but repellency has been found to be sensitive to larval age (37) and could also be sensitive to other factors that differed between the two studies (38). Aversive responses to CO 2 are mediated by neurons of another larval organ, the terminal organ, that coexpress Gr21a and Gr63a (2,(39)(40)(41)(42), and it is possible that other unidentified neurons also mediate airborne aversive responses.…”

Section: Discussionmentioning

confidence: 86%

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

104

184

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...

“…T he ability to detect and respond to changing concentrations of environmental CO 2 is widespread among animals and plays a critical role in locating food, finding hosts and mates, and avoiding danger (1)(2)(3)(4). CO 2 exposure can also have profound physiological effects, including altered respiration, motility, fecundity, and emotional state (5-7).…”

mentioning

confidence: 99%

Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans

Hallem

Spencer

McWhirter

et al. 2010

118

173

CO 2 is both a critical regulator of animal physiology and an important sensory cue for many animals for host detection, food location, and mate finding. The free-living soil nematode Caenorhabditis elegans shows CO 2 avoidance behavior, which requires a pair of ciliated sensory neurons, the BAG neurons. Using in vivo calcium imaging, we show that CO 2 specifically activates the BAG neurons and that the CO 2 -sensing function of BAG neurons requires TAX-2/ TAX-4 cyclic nucleotide-gated ion channels and the receptor-type guanylate cyclase GCY-9. Our results delineate a molecular pathway for CO 2 sensing and suggest that activation of a receptor-type guanylate cyclase is an evolutionarily conserved mechanism by which animals detect environmental CO 2 .guanylyl cyclase | olfaction | transcriptional profiling | regulator of G protein signaling | chemosensation T he ability to detect and respond to changing concentrations of environmental CO 2 is widespread among animals and plays a critical role in locating food, finding hosts and mates, and avoiding danger (1-4). CO 2 exposure can also have profound physiological effects, including altered respiration, motility, fecundity, and emotional state (5-7). CO 2 is sensed as an aversive cue by many free-living animals, including humans (3,6,8,9). By contrast, many parasites and disease vectors are attracted to CO 2 , which serves as a sensory cue for host location (1, 10).Nematodes constitute a large and highly diverse phylum that includes both free-living and parasitic species. Many parasitic nematodes, including some of the most devastating human-and plant-parasitic nematodes, are attracted to CO 2 . By contrast, adults of the free-living species Caenorhabditis elegans are repelled by CO 2 (11-14). CO 2 avoidance by C. elegans requires a pair of head neurons called the BAG neurons (13), which also mediate responses to decreases in ambient oxygen levels (15). Whether the BAG neurons directly sense CO 2 is not known, and the signaling pathways that mediate CO 2 detection are poorly understood.We show here that environmental CO 2 specifically activates the BAG neurons and not other neurons that drive avoidance behavior, suggesting that the BAG neurons are primary sensory neurons that detect CO 2 . Prolonged CO 2 exposure causes desensitization of avoidance behavior and the BAG neurons themselves, indicating that behavioral adaptation to CO 2 occurs at the level of the BAG neurons. In addition, we show that the CO 2 -evoked activity of the BAG neurons requires a cGMP signaling pathway consisting of the receptor guanylate cyclase GCY-9 and the cGMP-gated cation channel TAX-2/TAX-4. Insects detect CO 2 using a pair of gustatory receptors (16, 17), whereas some mammals detect CO 2 using the receptor-type guanylate cyclase, guanylate cyclase D (GC-D), and soluble adenylate cyclase (18)(19)(20). Our results show that the mechanism of CO 2 detection in C. elegans more closely resembles that of mammals than insects and suggest an evolutionarily ancient role for receptor-type guanyl...