Trends in Genetics
Volume 31, Issue 12, December 2015, Pages 683-695
Journal home page for Trends in Genetics

Review
Drosophila Chemoreceptors: A Molecular Interface Between the Chemical World and the Brain

https://doi.org/10.1016/j.tig.2015.09.005Get rights and content

Trends

Odorant receptors (Ors) have been found to activate an increasing number of behavioral circuits.

Gustatory receptors (Grs) are expressed in a wide diversity of organs. Emerging results reveal roles in an expanding repertoire of functions, extending beyond chemoreception.

Ionotropic receptors (IRs) are expressed not only in olfactory organs but also in taste organs. A large clade has recently been found to be expressed in all taste organs of the fly.

Ors, Grs, and IRs all have roles in the sexual behavior of the fly.

Chemoreception is essential for survival. Feeding, mating, and avoidance of predators depend on detection of sensory cues. Drosophila contains diverse families of chemoreceptors that detect odors, tastants, pheromones, and noxious stimuli, including receptors of the odor receptor (Or), gustatory receptor (Gr), ionotropic receptor (IR), Pickpocket (Ppk), and Trp families. We consider recent progress in understanding chemoreception in the fly, including the identification of new receptors, the discovery of novel biological functions for receptors, and the localization of receptors in unexpected places. We discuss major unsolved problems and suggest areas that may be particularly ripe for future discoveries, including the roles of these receptors in driving the circuits and behaviors that are essential to the survival and reproduction of the animal.

Section snippets

The Problem

Animals in their natural environments are immersed in a sea of chemical compounds. Some of these compounds signal the presence of nutrients, while others signify the danger of poisons. Some compounds indicate the proximity of a mating partner, while others warn of a predator. Animals must be able to detect and identify a wide variety of meaningful signals among the vast complexity of their chemical milieu.

In addition to chemical identity, chemical intensity can also be critical to an animal.

The Cellular Context of Chemoreception

Volatile compounds are sensed by olfactory receptor neurons (ORNs) of the olfactory system, whereas non-volatile compounds are detected by gustatory receptor neurons (GRNs) of the taste system. However, the conceptual wall dividing olfaction and taste has been increasingly assaulted by a barrage of experimental results that establish new links between the two sensory modalities.

The Largest Families of Chemoreceptors

Chemoreceptors of the fly are numerous and sundry (Figure 4). A recurrent source of excitement in the field has been the discovery of new kinds of chemoreceptors. Below we describe the largest classes of chemoreceptors. We also introduce some additional classes of chemoreceptors in Box 2. Other kinds of receptors may well lurk in the genome of the fly, awaiting discovery.

Concluding Remarks and Future Perspectives

Great progress has been made in understanding the receptors that constitute the basis of all of chemosensory perception. However, critical boxes remain black, key principles remain controversial, and major topics remain unexplored (see Outstanding Questions). It is as if a new continent has been discovered but only the coastline has been mapped.

Ors and Grs are currently represented as squiggles through cartoon membranes, with much uncertainty in the case of Grs. A 3D structure of Ors and Grs

Acknowledgments

The authors thank Karen Menuz and Zhe He for helpful comments. They apologize to those whose work has not been cited due to space constraints or amnesia. Their work is supported by an NRSA (R.M.J.) and grants (J.R.C.) from the NIH.

References (130)

  • A.A. Dobritsa

    Integrating the molecular and cellular basis of odor coding in the Drosophila antenna

    Neuron

    (2003)
  • E. Fishilevich et al.

    Genetic and functional subdivision of the Drosophila antennal lobe

    Curr. Biol.

    (2005)
  • E.A. Hallem et al.

    Coding of odors by a receptor repertoire

    Cell

    (2006)
  • M.C. Stensmyr

    A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila

    Cell

    (2012)
  • H.K. Dweck

    Olfactory preference for egg laying on citrus substrates in Drosophila

    Curr. Biol.

    (2013)
  • A. Ejima

    Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate

    Curr. Biol.

    (2007)
  • Q. Li

    Combinatorial rules of precursor specification underlying olfactory neuron diversity

    Curr. Biol.

    (2013)
  • L.B. Vosshall

    A spatial map of olfactory receptor expression in the Drosophila antenna

    Cell

    (1999)
  • E. Song

    Determinants of the Drosophila odorant receptor pattern

    Dev. Cell

    (2012)
  • S.A. Kreher

    The molecular basis of odor coding in the Drosophila larva

    Neuron

    (2005)
  • S.A. Kreher

    Translation of sensory input into behavioral output via an olfactory system

    Neuron

    (2008)
  • L. Dunipace

    Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system

    Curr. Biol.

    (2001)
  • N. Thorne

    Taste perception and coding in Drosophila

    Curr. Biol.

    (2004)
  • L.A. Weiss

    The molecular and cellular basis of bitter taste in Drosophila

    Neuron

    (2011)
  • K. Scott

    A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila

    Cell

    (2001)
  • S. Fujii

    Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing

    Curr. Biol.

    (2015)
  • A. Dahanukar

    Two Gr genes underlie sugar reception in Drosophila

    Neuron

    (2007)
  • Z. Wang

    Taste representations in the Drosophila brain

    Cell

    (2004)
  • Y.T. Jeong

    An odorant-binding protein required for suppression of sweet taste by bitter chemicals

    Neuron

    (2013)
  • Y. Jiao

    Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila

    Curr. Biol.

    (2008)
  • S.J. Moon

    A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship

    Curr. Biol.

    (2009)
  • S.J. Moon

    A taste receptor required for the caffeine response in vivo

    Curr. Biol.

    (2006)
  • P. Fan

    Genetic and neural mechanisms that inhibit Drosophila from mating with other species

    Cell

    (2013)
  • S. Bray et al.

    A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship

    Neuron

    (2003)
  • G.M. Tauxe

    Targeting a dual detector of skin and CO2 to modify mosquito host seeking

    Cell

    (2013)
  • R. Benton

    Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila

    Cell

    (2009)
  • L. Abuin

    Functional architecture of olfactory ionotropic glutamate receptors

    Neuron

    (2011)
  • T.W. Koh

    The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors

    Neuron

    (2014)
  • L.B. Vosshall et al.

    Molecular architecture of smell and taste in Drosophila

    Annu. Rev. Neurosci.

    (2007)
  • S.R. Shanbhag

    Expression mosaic of odorant-binding proteins in Drosophila olfactory organs

    Microsc. Res. Tech.

    (2001)
  • R.I. Wilson

    Early olfactory processing in Drosophila: mechanisms and principles

    Annu. Rev. Neurosci.

    (2013)
  • R.F. Stocker

    The organization of the chemosensory system in Drosophila melanogaster: a review

    Cell Tissue Res.

    (1994)
  • F. Martin

    Elements of olfactory reception in adult Drosophila melanogaster

    Anat. Rec. (Hoboken)

    (2013)
  • N. Meunier

    Peripheral coding of bitter taste in Drosophila

    J. Neurobiol.

    (2003)
  • F. Ling

    The molecular and cellular basis of taste coding in the legs of Drosophila

    J. Neurosci.

    (2014)
  • A. Yanagawa

    Hygienic grooming is induced by contact chemicals in Drosophila melanogaster

    Front. Behav. Neurosci.

    (2014)
  • M.L. Wolbarsht et al.

    Electrical activity in the chemoreceptors of the blowfly. I. Responses to chemical and mechanical stimulation

    J. Gen. Physiol.

    (1958)
  • M.J. Rice

    Blowfly ovipositor receptor neurone sensitive to monovalent cation concentration

    Nature

    (1977)
  • B.J. Taylor

    Sexually dimorphic neurons of the terminalia of Drosophila melanogaster: II. Sex-specific axonal arborizations in the central nervous system

    J. Neurogenet.

    (1989)
  • J.H. Park et al.

    Heterogeneous expression of Drosophila gustatory receptors in enteroendocrine cells

    PLoS ONE

    (2011)
  • Cited by (238)

    View all citing articles on Scopus
    View full text