Insect odor and taste receptors.

Insect odor and taste receptors are highly sensitive detectors of food, mates, and oviposition sites. Following the identification of the first insect odor and taste receptors in Drosophila melanogaster, these receptors were identified in a number of other insects, including the malaria vector mosquito Anopheles gambiae; the silk moth, Bombyx mori; and the tobacco budworm, Heliothis virescens. The chemical specificities of many of the D. melanogaster receptors, as well as a few of the A. gambiae and B. mori receptors, have now been determined either by analysis of deletion mutants or by ectopic expression in in vivo or heterologous expression systems. Here we discuss recent advances in our understanding of the molecular and cellular basis of odor and taste coding in insects.

[1]  E. Grosse-Wilde,et al.  Candidate pheromone receptors of the silkmoth Bombyx mori , 2005, The European journal of neuroscience.

[2]  A. Cork,et al.  Identification of electrophysiologically‐active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts , 1996, Medical and veterinary entomology.

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

[4]  S. Nakajima,et al.  Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a , 2001, Current Biology.

[5]  M. McKenna,et al.  Putative Drosophila pheromone-binding proteins expressed in a subregion of the olfactory system. , 1994, The Journal of biological chemistry.

[6]  W. A. Johnson,et al.  Contribution of Drosophila DEG/ENaC Genes to Salt Taste , 2003, Neuron.

[7]  J. Eberwine,et al.  Expression of mRNAs Encoding for Two Different Olfactory Receptors in a Subset of Olfactory Receptor Neurons , 2000, Journal of neurochemistry.

[8]  N. Ryba,et al.  Putative Mammalian Taste Receptors A Class of Taste-Specific GPCRs with Distinct Topographic Selectivity , 1999, Cell.

[9]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

[10]  J. Hildebrand,et al.  Recent advances in insect olfaction, specifically regarding the morphology and sensory physiology of antennal sensilla of the female sphinx moth Manduca sexta , 2001, Microscopy research and technique.

[11]  C. J. Otter,et al.  Olfactory sensitivities of mosquitoes with different host preferences (Anopheles gambiae s.s., An. arabiensis, An. quadriannulatus, An. m. atroparvus) to synthetic host odours. , 1999 .

[12]  John R. Carlson,et al.  Odorant response of individual sensilla on theDrosophila antenna , 1997, Invertebrate Neuroscience.

[13]  K. D. Roeder,et al.  Electrophysiological studies of arthropod chemoreception. I. General properties of the labellar chemoreceptors of Diptera. , 1956, Journal of cellular and comparative physiology.

[14]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[15]  J. R. Carlson,et al.  Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  E. Hallem,et al.  Olfaction: Mosquito receptor for human-sweat odorant , 2004, Nature.

[17]  R. Greenspan,et al.  Courtship in Drosophila. , 2003, Annual review of genetics.

[18]  J. Rospars,et al.  Structure and development of the insect antennodeutocerebral system , 1988 .

[19]  R. Steinbrecht,et al.  Odorant‐Binding Proteins: Expression and Function , 1998, Annals of the New York Academy of Sciences.

[20]  R. Steinbrecht,et al.  Atlas of olfactory organs of Drosophila melanogaster 2. Internal organization and cellular architecture of olfactory sensilla. , 2000, Arthropod structure & development.

[21]  H. Amrein,et al.  Taste Perception and Coding in Drosophila , 2004, Current Biology.

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

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

[24]  I. Shimada,et al.  The specific receptor site for aliphatic carboxylate anion in the labellar sugar receptor of the fleshfly , 1978 .

[25]  N. Meunier,et al.  Sex-specific non-pheromonal taste receptors in Drosophila , 2000, Current Biology.

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

[27]  J. Carlson,et al.  Targeted Mutation of a Drosophila Odor Receptor Defines Receptor Requirement in a Novel Class of Sensillum , 2003, The Journal of Neuroscience.

[28]  Reinhard F. Stocker,et al.  The organization of the chemosensory system in Drosophila melanogaster: a rewiew , 2004, Cell and Tissue Research.

[29]  S. G. Lee,et al.  A comparison of responses from olfactory receptor neurons of Heliothis subflexa and Heliothis virescens to components of their sex pheromone , 2004, Journal of Comparative Physiology A.

[30]  T. Heinbockel,et al.  VARIABILITY OF OLFACTORY RECEPTOR NEURON RESPONSES OF FEMALE SILKMOTHS (BOMBYX MORI L.) TO BENZOIC ACID AND ()-LINALOOL , 1996 .

[31]  J. Carlson,et al.  A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila , 2001, Nature Neuroscience.

[32]  J. Carlson,et al.  Drosophila Gr5a encodes a taste receptor tuned to trehalose , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[33]  B. Hovemann,et al.  An increased receptive field of olfactory receptor Or43a in the antennal lobe of Drosophila reduces benzaldehyde-driven avoidance behavior. , 2005, Chemical senses.

[34]  M. Tanouye,et al.  Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. , 2002, Genome research.

[35]  J. V. van Loon,et al.  Sensitivities of antennal olfactory neurons of the malaria mosquito, Anopheles gambiae, to carboxylic acids. , 1999, Journal of insect physiology.

[36]  I. Shimada,et al.  Taste response to 2,5-anhydro-d-hexitols; rigid stereospecificity of the furanose site in the sugar receptor of the flesh fly , 1985, Journal of Comparative Physiology.

[37]  H. Breer,et al.  A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens , 2002, The European journal of neuroscience.

[38]  C. Masson,et al.  Whole‐cell recording from honeybee olfactory receptor neurons: ionic currents, membrane excitability and odourant response in developing workerbee and drone , 2002, The European journal of neuroscience.

[39]  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.

[40]  Martin Heisenberg,et al.  Targeted expression of tetanus neurotoxin interferes with behavioral responses to sensory input in Drosophila. , 2002, Journal of neurobiology.

[41]  Kazushige Touhara,et al.  Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Michael Leon,et al.  Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb , 1998 .

[43]  Linda B Buck,et al.  Odor maps in the olfactory cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

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

[46]  T. Tanimura,et al.  Multiple receptor proteins for sweet taste inDrosophila discriminated by papain treatment , 1981, Journal of comparative physiology.

[47]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[48]  R. Stocker,et al.  Smell and Taste Perception in Drosophila melanogasterLarva: Toxin Expression Studies in Chemosensory Neurons , 1999, The Journal of Neuroscience.

[49]  Kristin Scott,et al.  Taste Representations in the Drosophila Brain , 2004, Cell.

[50]  Eleanor H. Slifer,et al.  The Structure of Arthropod Chemoreceptors , 1970 .

[51]  S. van Straten,et al.  Volatile compounds in food. , 1977 .

[52]  W. Leal,et al.  Kinetics and molecular properties of pheromone binding and release. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[53]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[54]  N. Meunier,et al.  Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. , 2004, Journal of neurobiology.

[55]  R. Steinbrecht,et al.  Three odorant-binding proteins are co-expressed in sensilla trichodea of Drosophila melanogaster , 2005 .

[56]  V. R. Shamprasad,et al.  Maxillary palp glomeruli and ipsilateral projections in the antennal lobe ofDrosophila melanogaster , 2004, Journal of Biosciences.

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

[58]  R. Falk,et al.  Labellar taste organs of Drosophila melanogaster , 1976, Journal of morphology.

[59]  S. Shanbhag,et al.  Functional implications of the projections of neurons from individual labellar sensillum of Drosophila melanogaster as revealed by neuronal-marker horseradish peroxidase , 1992, Cell and Tissue Research.

[60]  M. Koganezawa,et al.  Multiple receptor sites for nucleotide reception in the labellar taste receptor cells of the fleshfly Boettcherisca peregrina. , 1999, Journal of insect physiology.

[61]  P. Solari,et al.  Bitter taste recognition in the blowfly Electrophysiological and behavioral evidence , 2000, Physiology & Behavior.

[62]  T. Tanimura,et al.  Taste sensitivity to trehalose and its alteration by gene dosage in Drosophila melanogaster. , 1988, Genetics.

[63]  A. Chess,et al.  Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. , 1999, Genomics.

[64]  J. Boeckh,et al.  Insect olfactory receptors. , 1965, Cold Spring Harbor symposia on quantitative biology.

[65]  K. Störtkuhl,et al.  Functional analysis of an olfactory receptor in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Kazushige Touhara,et al.  Insect Sex-Pheromone Signals Mediated by Specific Combinations of Olfactory Receptors , 2005, Science.

[67]  W. Gao,et al.  Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears , 2000, Nature Neuroscience.

[68]  A. Dubin,et al.  Inactivation of olfactory sensilla of a single morphological type differentially affects the response of Drosophila to odors. , 2002, Journal of neurobiology.

[69]  Cori Bargmann,et al.  Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans , 1995, Cell.

[70]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[71]  H Maarse,et al.  Volatile compounds in food : qualitative and quantitative data , 1990 .

[72]  H. Breer,et al.  A candidate olfactory receptor subtype highly conserved across different insect orders , 2003, Journal of Comparative Physiology A.

[73]  S. Meister,et al.  Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system , 2001, Current Biology.

[74]  Linda B. Buck,et al.  Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb , 1994, Cell.

[75]  V. Rodrigues,et al.  Genetic analysis of chemosensory pathway , 1978, Proceedings / Indian Academy of Sciences.

[76]  A. Chess,et al.  Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe , 2000, Nature Neuroscience.

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

[78]  J. Hildebrand,et al.  Cephalic sensory pathways in the central nervous system of larval Manduca sexta (Lepidoptera : Sphingidae). , 1987, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[79]  P. Xu,et al.  Drosophila OBP LUSH Is Required for Activity of Pheromone-Sensitive Neurons , 2005, Neuron.

[80]  G. Pollack,et al.  Birth times of neurons in labellar taste sensilla of the blowfly Phormia regina. , 1995, Journal of neurobiology.

[81]  M. Koganezawa,et al.  A specific receptor site for glycerol, a new sweet tastant for Drosophila: structure-taste relationship of glycerol in the labellar sugar receptor cell. , 2004, Chemical senses.

[82]  I. Shimada,et al.  Separation of two receptor sites in a single labellar sugar receptor of the flesh-fly by treatment with p-chloromercuribenzoate. , 1974, Journal of insect physiology.

[83]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[84]  P. Mombaerts,et al.  A Contextual Model for Axonal Sorting into Glomeruli in the Mouse Olfactory System , 2004, Cell.

[85]  F. Marion-Poll,et al.  Differentiated Response to Sugars among Labellar Chemosensilla in Drosophila , 2002, Zoological science.

[86]  D. P. Smith,et al.  LUSH odorant-binding protein mediates chemosensory responses to alcohols in Drosophila melanogaster. , 1998, Genetics.

[87]  P. Guerin,et al.  Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. , 2000, Journal of insect physiology.

[88]  V. Rehder Sensory pathways and motoneurons of the proboscis reflex in the suboesophageal ganglion of the honey bee , 1989, The Journal of comparative neurology.

[89]  R. J. Pitts,et al.  A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[91]  L. Riddiford,et al.  Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea polyphemus. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[92]  Ichiro Shimada,et al.  Genetic dimorphism in the taste sensitivity to trehalose inDrosophila melanogaster , 1982, Journal of comparative physiology.

[93]  R. J. Pitts,et al.  Identification of a chemosensory receptor from the yellow fever mosquito, Aedes aegypti, that is highly conserved and expressed in olfactory and gustatory organs. , 2004, Chemical senses.

[94]  B. Hansson,et al.  Evolution of the olfactory code in the Drosophila melanogaster subgroup , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[95]  J. Rospars,et al.  Peripheral coding of bitter taste in Drosophila. , 2003, Journal of neurobiology.

[96]  G. Pollack,et al.  Central projections of labellar taste hairs in the blowfly, Phormia regina Meigen , 1986, Cell and Tissue Research.

[97]  R. Crnjar,et al.  Saccharin stimulates the “deterrent” cell in the blowfly: behavioral and electrophysiological evidence , 2004, Physiology & Behavior.

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

[99]  Shubha V. Nayak,et al.  Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster meigen (Diptera : Drosophilidae) , 1983 .

[100]  R. Stocker,et al.  Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. , 2003, Journal of neurobiology.

[101]  T. Baker,et al.  Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea , 2002, Journal of Comparative Physiology A.

[102]  J Y Lettvin,et al.  Chemical transmission in the nose of the frog. , 1965, The Journal of physiology.

[103]  Jean-Pierre Rospars,et al.  Why are insect olfactory receptor neurons grouped into sensilla? The teachings of a model investigating the effects of the electrical interaction between neurons on the transepithelial potential and the neuronal transmembrane potential , 2004, European Biophysics Journal.

[104]  R. Stocker,et al.  Cobalt filling of sensory projections from internal and external mouthparts in Drosophila , 2004, Cell and Tissue Research.

[105]  K. D. Roeder,et al.  Physiology of a primary chemoreceptor unit. , 1955, Science.

[106]  M. Rosbash,et al.  Members of a family of drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs , 1994, Neuron.

[107]  L. Murdock,et al.  Central projections of axons from taste hairs on the labellum and tarsi of the blowfly, Phormia regina Meigen , 1992, The Journal of comparative neurology.

[108]  O. Vostrowsky,et al.  A new pheromone of the silkworm moth Bombyx mori , 1978, The Science of Nature.

[109]  R. Friedrich,et al.  Combinatorial and Chemotopic Odorant Coding in the Zebrafish Olfactory Bulb Visualized by Optical Imaging , 1997, Neuron.

[110]  F. Hanson,et al.  TASTE PAPILLAE OF THE BLOWFLY. , 1965, Journal of cellular and comparative physiology.

[111]  Shubha V. Nayak,et al.  Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen (Diptera : Drosophilidae) , 1985 .

[112]  K. Srivastava,et al.  Free and forced convection flow in a rotating channel bounded below by a permeable bed , 1978 .

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

[114]  L. Riddiford,et al.  Pheromone binding and inactivation by moth antennae , 1981, Nature.

[115]  Gregory S.X.E. Jefferis,et al.  Glomerular Maps without Cellular Redundancy at Successive Levels of the Drosophila Larval Olfactory Circuit , 2005, Current Biology.

[116]  P. Hiesinger,et al.  Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster , 1999, The Journal of comparative neurology.

[117]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[118]  H. Amrein,et al.  A Putative Drosophila Pheromone Receptor Expressed in Male-Specific Taste Neurons Is Required for Efficient Courtship , 2003, Neuron.

[119]  Ivan Rodriguez,et al.  Axon Guidance of Mouse Olfactory Sensory Neurons by Odorant Receptors and the β2 Adrenergic Receptor , 2004, Cell.

[120]  H Breer,et al.  Genes encoding candidate pheromone receptors in a moth (Heliothis virescens). , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[121]  R. Yamaoka,et al.  Perception of noxious compounds by contact chemoreceptors of the blowfly, Phormia regina: putative role of an odorant-bindingpProtein. , 2003, Chemical senses.

[122]  R. Zacharuk Ultrastructure and function of insect chemosensilla , 1980 .

[123]  Jayaram Chandrashekar,et al.  A Novel Family of Mammalian Taste Receptors , 2000, Cell.

[124]  Peter J. Clyne,et al.  Odor Coding in a Model Olfactory Organ: TheDrosophila Maxillary Palp , 1999, The Journal of Neuroscience.

[125]  R. N. Singh,et al.  Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera : Drosophilidae) , 1984 .

[126]  K. Isono,et al.  A Single-Amino-Acid Change of the Gustatory Receptor Gene, Gr5a, Has a Major Effect on Trehalose Sensitivity in a Natural Population of Drosophila melanogaster , 2004, Genetics.

[127]  Bill S Hansson,et al.  Novel natural ligands for Drosophila olfactory receptor neurones , 2003, Journal of Experimental Biology.

[128]  Mariella Tegoni,et al.  Structural aspects of sexual attraction and chemical communication in insects. , 2004, Trends in biochemical sciences.

[129]  W. Leal,et al.  Peripheral Coding of Sex Pheromone and a Behavioral Antagonist in the Japanese Beetle, Popillia japonica , 2002, Journal of Chemical Ecology.

[130]  J. Hildebrand,et al.  Trans-sexually grafted antennae influence development of sexually dimorphic neurones in moth brain , 1982, Nature.

[131]  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.

[132]  H. Morita,et al.  Stimulation of the Labellar Sugar Receptor of the Fleshfly by Mono- and Disaccharides , 1968, The Journal of general physiology.

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

[134]  H. Wieczorek,et al.  The labellar sugar receptor ofDrosophila , 1989, Journal of Comparative Physiology A.

[135]  R. Falk,et al.  Mutation affecting taste perception in Drosophila melanogaster , 1975, Nature.

[136]  L. Vosshall,et al.  Functional conservation of an insect odorant receptor gene across 250 million years of evolution , 2005, Current Biology.

[137]  J. Carlson,et al.  Coexpression of Two Odorant-Binding Protein Homologs inDrosophila: Implications for Olfactory Coding , 1997, The Journal of Neuroscience.

[138]  G. Gisselmann,et al.  Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[139]  D. P. Smith,et al.  Putative Drosophila odor receptor OR43b localizes to dendrites of olfactory neurons. , 2001, Insect biochemistry and molecular biology.

[140]  K. Galindo,et al.  A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. , 2001, Genetics.

[141]  J. V. van Loon,et al.  Olfactory receptors on the antennae of the malaria mosquito Anopheles gambiae are sensitive to ammonia and other sweat-borne components. , 2001, Journal of insect physiology.

[142]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[143]  R. J. Pitts,et al.  A cluster of candidate odorant receptors from the malaria vector mosquito, Anopheles gambiae. , 2002, Chemical senses.

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

[145]  J. Hildebrand,et al.  Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds , 2001, Journal of Comparative Physiology A.

[146]  K. Mori,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. , 1992, Journal of neurophysiology.

[147]  R A Steinbrecht,et al.  Expression mosaic of odorant‐binding proteins in Drosophila olfactory organs , 2001, Microscopy research and technique.

[148]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

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

[150]  A. Borst,et al.  Neuronal architecture of the antennal lobe in Drosophila melanogaster , 1990, Cell and Tissue Research.