Location of Repository

Hedonic Taste in Drosophila Revealed by Olfactory Receptors Expressed in Taste Neurons

By Makoto Hiroi, Teiichi Tanimura and Frédéric Marion-Poll

Abstract

Taste and olfaction are each tuned to a unique set of chemicals in the outside world, and their corresponding sensory spaces are mapped in different areas in the brain. This dichotomy matches categories of receptors detecting molecules either in the gaseous or in the liquid phase in terrestrial animals. However, in Drosophila olfactory and gustatory neurons express receptors which belong to the same family of 7-transmembrane domain proteins. Striking overlaps exist in their sequence structure and in their expression pattern, suggesting that there might be some functional commonalities between them. In this work, we tested the assumption that Drosophila olfactory receptor proteins are compatible with taste neurons by ectopically expressing an olfactory receptor (OR22a and OR83b) for which ligands are known. Using electrophysiological recordings, we show that the transformed taste neurons are excited by odor ligands as by their cognate tastants. The wiring of these neurons to the brain seems unchanged and no additional connections to the antennal lobe were detected. The odor ligands detected by the olfactory receptor acquire a new hedonic value, inducing appetitive or aversive behaviors depending on the categories of taste neurons in which they are expressed i.e. sugar- or bitter-sensing cells expressing either Gr5a or Gr66a receptors. Taste neurons expressing ectopic olfactory receptors can sense odors at close range either in the aerial phase or by contact, in a lipophilic phase. The responses of the transformed taste neurons to the odorant are similar to those obtained with tastants. The hedonic value attributed to tastants is directly linked to the taste neurons in which their receptors are expressed

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:2440521
Provided by: PubMed Central
Download PDF:
Sorry, we are unable to provide the full text but you may find it at the following location(s):
  • http://www.pubmedcentral.nih.g... (external link)
  • Suggested articles

    Preview

    Citations

    1. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila.
    2. (2007). A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging.
    3. (2001). A large family of divergent Drosophila odorantbinding proteins expressed in gustatory and olfactory sensilla.
    4. (2001). A peripheral mechanism for behavioral adaptation to specific ‘‘bitter’’ taste stimuli in an insect.
    5. (2006). A taste receptor required for the caffeine response in vivo.
    6. (2001). An artificial sweetener stimulates the sweet taste in insect: dual effects of glycyrrhizin in Phormia regina.
    7. (2007). An inhibitory sex pheromone tastes bitter for Drosophila males.
    8. (2005). An odorant-binding protein facilitates odorant transfer from air to hydrophilic surroundings in the blowfly.
    9. (2000). An olfactory sensory map in the fly brain.
    10. (2006). Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo.
    11. (2007). Carleton A
    12. (2007). Central gustatory projections and side-specificity of operant antennal muscle conditioning in the honeybee.
    13. (2005). Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila.
    14. (2003). Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways.
    15. (2003). Contact chemoreception in feeding by phytophagous insects.
    16. (2005). Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication.
    17. (2008). Drosophila egg-laying site selection as a system to study simple decision-making processes.
    18. (2003). Drosophila Gr5a encodes a taste receptor tuned to trehalose.
    19. (2008). Drosophila odorant receptors are both ligand-gated and cyclic-nucleotideactivated cation channels.
    20. (2005). Dual, multilayered somatosensory maps formed by antennal tactile and contact chemosensory afferents in an insect brain.
    21. (1995). Effects of plant epicuticular lipids on insect herbivores.
    22. (1954). Electrical response of insect chemosensory neurons to normal stimuli.
    23. (2006). Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates.
    24. (1998). Feeding behavior and survival of glucose-averse Blattella germanica (Orthoptera : Blattoidea : Blattellidae) provided glucose as a sole food source.
    25. (2002). Genome-wide analysis of the odorant-binding protein gene family
    26. (2001). Gustatory organs of Drosophila melanogaster: fine structure and expression of the putative odorantbinding protein PBPRP2.
    27. (2001). Host recognition by the tobacco hornworm is mediated by a host plant compound.
    28. (2006). Imaging taste responses in the fly brain reveals a functional map of taste category and behavior.
    29. (2006). Insect odor and taste receptors.
    30. (2008). Insect olfactory receptors are heteromeric ligand-gated ion channels.
    31. (2005). Insect sex-pheromone signals mediated by specific combinations of olfactory receptors.
    32. (2007). Mechanisms of odor receptor gene choice in Drosophila.
    33. (1997). Mechanisms of olfactory discrimination: converging evidence for common principles across phyla.
    34. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster.
    35. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis.
    36. (1975). Mutation affecting taste perception in Drosophila melanogaster.
    37. (2002). Novel odorant-binding proteins expressed in the taste tissue of the fly.
    38. (1999). Odor coding in a model olfactory organ: the Drosophila maxillary palp.
    39. (2001). Odor coding in the Drosophila antenna.
    40. (2005). Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster.
    41. (2007). Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia.
    42. (1975). Olfactory capabilities of the ‘gustatory’ chemoreceptors of the tobacco hornworm larvae.
    43. (2004). Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction.
    44. (2003). Perception of noxious compounds by contact chemoreceptors of the blowfly, Phormia regina: putative role of an odorant-binding protein.
    45. (2008). Reduced odor responses from antennal neurons of Gqa, phospholipase Cb,a n d rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction.
    46. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system.
    47. (2004). Taste perception and coding in Drosophila.
    48. (1994). Tasting green leaf volatiles by larvae and adults of Colorado potato beetle, Leptinotarsa decemlineata.
    49. (2006). The cells and logic for mammalian sour taste detection.
    50. (2003). The G-proteincoupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints.
    51. (2004). The human olfactory receptor gene family.
    52. (2007). The molecular basis of CO2 reception in Drosophila.
    53. (2004). The molecular basis of odor coding in the Drosophila antenna.
    54. (2003). The neurobiology of taste in insects.
    55. (1994). The organization of the chemosensory system in Drosophila melanogaster - a review.
    56. (2005). The receptors and coding logic for bitter taste.
    57. (2003). The receptors for mammalian sweet and umami taste.
    58. (2000). Transduction ion channels directly gated by sugars on the insect taste cell.
    59. (2006). Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor.
    60. (2001). Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a.
    61. (2004). Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila.
    62. (2006). Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons located on the antennae and the proboscis in the moth Heliothis virescens.
    63. (2007). Two Gr genes underlie sugar reception in Drosophila.
    64. (1980). Ultrastructure of invertebrate chemo-, thermo- and hygroreceptors and its functional significance.

    To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.