Insect chemoreception

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Insect chemoreception is mediated by a large and diverse superfamily of seven-transmembrane domain receptors. These receptors were first identified in Drosophila, but have since been found in other insects, including mosquitoes and moths. Expression and functional analysis of these receptors have been used to identify receptor ligands and to map receptors to functional classes of neurons. Many receptors detect general odorants or tastants, whereas some detect pheromones. The non-canonical receptor Or83b, which is highly conserved across insect orders, dimerizes with odorant and pheromone receptors and is required for efficient localization of these proteins to dendrites of sensory neurons. These studies provide a foundation for understanding the molecular and cellular basis of olfactory and gustatory coding.

Introduction

Insect chemosensory systems detect a wide range of volatile and soluble chemicals and are important for finding and assessing the quality of food sources, in addition to identifying mates and oviposition sites. Chemosensory neurons are present in specialized sensory hairs called sensilla. In many insects olfactory sensilla are present on two pairs of olfactory organs on the head, the antennae and the maxillary palps. Gustatory sensilla are present on several parts of the body including the external and internal mouthparts, the legs, the wing margins and the ovipositor in females.

In adult Drosophila, each olfactory sensillum is innervated by up to four olfactory receptor neurons (ORNs) [1]. Pores in the cuticular walls of the sensilla enable passage of odorant molecules from the environment to the dendrites of ORNs. Taste sensilla have a single pore at the tip and are innervated by one or more gustatory receptor neurons (GRNs), typically four, and a mechanosensory neuron [1]. Physiological and behavioral analysis has shown that GRNs are tuned to four classes of compounds: sugars (attractants), bitter compounds (repellents), salts and water [2].

A superfamily of 60 odorant receptor (Or) and 60 gustatory receptor (Gr) genes was identified in Drosophila using bioinformatic and molecular approaches [3, 4, 5, 6]. Subsequently, counterparts of these genes were identified in the malaria vector mosquito Anopheles gambiae and the moths Heliothis virescens and Bombyx mori [7, 8, 9, 10].

Section snippets

Organization of the olfactory system

The expression of Or genes in olfactory organs has been demonstrated by a variety of techniques including in situ hybridization and reporter gene expression. In adult Drosophila, most Or genes are expressed in subsets of ORNs in either the antenna or the maxillary palp [3, 5, 11, 12, 13••]. Expression of ∼23 Or genes has also been detected at the larval stage, including 11 genes that are not expressed in the adult [14•]. Staining with antibodies raised against Or22a/b or Or43b showed that Or

Organization of the gustatory system

In Drosophila, analysis of Gr gene expression is based primarily on reporter gene expression studies that use Gr-promoter transgenes. In general, Gr genes appear to be expressed in subsets of GRNs in the adult, in one or more gustatory tissues including the proboscis, legs, wing margins and internal mouthparts [35, 36, 37, 38••, 39•]. Similar to the Or genes, some Gr genes are expressed during the larval stage [35]. In addition, at least one is expressed in a sexually dimorphic manner [40].

Functional analysis of odorant receptors

Initial evidence that Or genes encode odorant receptors was provided by experiments in which the antennal receptor Or43a was overexpressed in a large number of antennal neurons [43]. Electrophysiological responses to benzaldehyde and some structurally related odorants were increased in these flies, suggesting that Or43a is a receptor for these odorants. At the same time, expression of Or43a in Xenopus oocytes was found to impart a response to these same odors [44].

Validation of the chemosensory

A receptor-to-neuron map

The discriminatory power of the olfactory system depends largely on the molecular diversity of the odorant receptor repertoire. Initial in situ hybridization experiments showed that 32 Or genes are expressed in the Drosophila antenna [11]. Of these, all except one were tested in the ‘empty’ ab3A neuron of Or22a/b mutant flies; each receptor was expressed and physiological recordings were then taken from the ab3A neuron to determine the odor specificity that each receptor conferred. Twenty four

Function of the non-canonical Or83b receptor

Or83b is an unusual Or gene; it is the most conserved chemoreceptor gene in insects [6, 8, 48, 49•, 50••], and unlike other Or genes that have been examined, it is expressed in most olfactory neurons, in the adult and in the larvae [22, 34••]. Or83b orthologs have been found in other flies, mosquitoes, honeybees, moths and beetles [48, 49•, 50••, 51, 52]. The function of Or83b is also conserved across insect orders: Or83b orthologs from the medfly, the mosquito and the moth can all substitute

Functional analysis of taste receptors

Evidence that the Gr genes encode taste receptors came from the analysis of the role of Gr5a in the response to the disaccharide trehalose. Electrophysiological and behavioral responses to trehalose are diminished in deletion mutants that lack the Gr5a gene [54, 55]. These defects are specific to trehalose; responses to another sugar, sucrose, are not affected. The trehalose response in Gr5a mutant flies was rescued by supplying a wild type copy of Gr5a on a transgene, but not a mutant copy of

Functional analysis of pheromone receptors

Recently, three members of the Or and Gr superfamilies have been implicated in pheromone reception. The function of Gr68a was analyzed in Drosophila by reducing its level of expression using RNAi [40]. Although its ligand has not been identified, the results suggest that Gr68a has a role in courtship behavior. Affected males initiate courtship but fail to progress through the entire behavioral sequence efficiently. Gr68a is expressed in male forelegs, consistent with the possibility that it

Conclusions

Insect odor and taste receptors belong to an ancient receptor superfamily that mediates responses to diverse chemical stimuli in both adults and larvae. In the past few years, substantial progress has been made in our understanding of the molecular basis of odor coding in peripheral olfactory organs. Odorant response profiles of most of the Drosophila odorant receptors have now been identified, and many of these receptors have been mapped to the functional classes of neurons in which they are

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors’ research is supported by grants from the National Institute of Health, DC04729, DC02174 and GM63364, and a Senior Scholar Award from the Ellison Medical Foundation to JR Carlson.

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