The molecular basis of CO2 reception in Drosophila

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.

[1]  G. Vale Field studies of the responses of tsetse flies (Glossinidae) and other Diptera to carbon dioxide, acetone and other chemicals , 1980 .

[2]  J. Hildebrand,et al.  Floral CO2 emission may indicate food abundance to nectar-feeding moths , 2004, Naturwissenschaften.

[3]  S. Snyder,et al.  Carbon monoxide: a putative neural messenger. , 1993, Science.

[4]  Cornelia I. Bargmann,et al.  Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue , 2004, Nature.

[5]  Hugh M Robertson,et al.  G Protein-Coupled Receptors in Anopheles gambiae , 2002, Science.

[6]  Andrey Rzhetsky,et al.  A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna , 1999, Cell.

[7]  J. Hildebrand,et al.  Floral CO2 Reveals Flower Profitability to Moths , 2004, Journal of Chemical Ecology.

[8]  M. Geier,et al.  Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours , 2005, Journal of Experimental Biology.

[9]  Leslie B. Vosshall,et al.  Or83b Encodes a Broadly Expressed Odorant Receptor Essential for Drosophila Olfaction , 2004, Neuron.

[10]  J. Carlson,et al.  Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[11]  S. Kustu,et al.  Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  John R. Carlson,et al.  Coexpression of Two Functional Odor Receptors in One Neuron , 2005, Neuron.

[13]  G. Stange Carbon Dioxide Is a Close-Range Oviposition Attractant in the Queensland Fruit Fly Bactrocera tryoni , 1999, Naturwissenschaften.

[14]  John R Carlson,et al.  Chemosensory Coding by Neurons in the Coeloconic Sensilla of the Drosophila Antenna , 2005, The Journal of Neuroscience.

[15]  Leslie B. Vosshall,et al.  Genetic and Functional Subdivision of the Drosophila Antennal Lobe , 2005, Current Biology.

[16]  John R. Carlson,et al.  Odor Coding in the Drosophila Antenna , 2001, Neuron.

[17]  Leslie B. Vosshall,et al.  Two chemosensory receptors together mediate carbon dioxide detection in Drosophila , 2007, Nature.

[18]  W. Takken,et al.  Odor-mediated behavior of Afrotropical malaria mosquitoes. , 1999, Annual review of entomology.

[19]  John R. Carlson,et al.  A Novel Family of Divergent Seven-Transmembrane Proteins Candidate Odorant Receptors in Drosophila , 1999, Neuron.

[20]  R. Stocker,et al.  Adult‐like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons , 2002, The Journal of comparative neurology.

[21]  John R. Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Larva , 2005, Neuron.

[22]  G. Gisselmann,et al.  Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster , 2005, Nature Neuroscience.

[23]  Andrey Rzhetsky,et al.  A Chemosensory Gene Family Encoding Candidate Gustatory and Olfactory Receptors in Drosophila , 2001, Cell.

[24]  Silke Sachse,et al.  Atypical Membrane Topology and Heteromeric Function of Drosophila Odorant Receptors In Vivo , 2006, PLoS biology.

[25]  Richard A. Cerione,et al.  The Cool-2/α-Pix Protein Mediates a Cdc42-Rac Signaling Cascade , 2005, Current Biology.

[26]  P. O’Farrell,et al.  Nitric Oxide Contributes to Behavioral, Cellular, and Developmental Responses to Low Oxygen in Drosophila , 1999, Cell.

[27]  G. Stange,et al.  Carbon‐dioxide sensing structures in terrestrial arthropods , 1999, Microscopy research and technique.

[28]  H. Krause,et al.  The Drosophila Nuclear Receptor E75 Contains Heme and Is Gas Responsive , 2005, Cell.

[29]  R. Steinbrecht,et al.  Atlas of olfactory organs of Drosophila melanogaster , 1999 .

[30]  K. Niyogi,et al.  Rhesus expression in a green alga is regulated by CO2 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  John R. Carlson,et al.  Integrating the Molecular and Cellular Basis of Odor Coding in the Drosophila Antenna , 2003, Neuron.

[32]  David J. Anderson,et al.  A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila , 2004, Nature.

[33]  R. Putnam,et al.  Cellular mechanisms involved in CO(2) and acid signaling in chemosensitive neurons. , 2004, American journal of physiology. Cell physiology.

[34]  W. Inwood,et al.  Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels. , 2006, Transfusion clinique et biologique : journal de la Societe francaise de transfusion sanguine.

[35]  Hugh M Robertson,et al.  The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. , 2006, Genome research.

[36]  Manfred Forstreuter,et al.  Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context , 2006, Journal of Experimental Biology.

[37]  Anupama Dahanukar,et al.  Insect odor and taste receptors. , 2006, Annual review of entomology.

[38]  J. Carlson,et al.  Candidate taste receptors in Drosophila. , 2000, Science.