Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster

Abstract

The insect chemoreceptor superfamily in Drosophila melanogaster is predicted to consist of 62 odorant receptor (Or) and 68 gustatory receptor (Gr) proteins, encoded by families of 60 Or and 60 Gr genes through alternative splicing. We include two previously undescribed Or genes and two previously undescribed Gr genes; two previously predicted Or genes are shown to be alternative splice forms. Three polymorphic pseudogenes and one highly defective pseudogene are recognized. Phylogenetic analysis reveals deep branches connecting multiple highly divergent clades within the Gr family, and the Or family appears to be a single highly expanded lineage within the superfamily. The genes are spread throughout the Drosophila genome, with some relatively recently diverged genes still clustered in the genome. The Gr5a gene on the X chromosome, which encodes a receptor for the sugar trehalose, has transposed from one such tandem cluster of six genes at cytological location 64, as has Gr61a, and all eight of these receptors might bind sugars. Analysis of intron evolution suggests that the common ancestor consisted of a long N-terminal exon encoding transmembrane domains 1-5 followed by three exons encoding transmembrane domains 6 -7. As many as 57 additional introns have been acquired idiosyncratically during the evolution of the superfamily, whereas the ancestral introns and some of the older idiosyncratic introns have been lost at least 48 times independently. Altogether, these patterns of molecular evolution suggest that this is an ancient superfamily of chemoreceptors, probably dating back at least to the origin of the arthropods. odorant receptor ͉ gustatory receptor ͉ olfaction ͉ taste ͉ gustation

Taste and pheromone perception in the fruit fly Drosophila melanogaster

“…The fly Gr gene family was discovered by analyzing the Drosophila genome database using algorithms that identify multitransmembrane proteins or by performing reiterated Basic Local Alignment Search Tool searches with Drosophila olfactory receptor proteins as query sequences [35,36,42], and once the entire Drosophila genome sequence was determined, a total of 68 Gr genes were found (Fig. 2) [43]. The diversity of the Gr genes is remarkable, as similarity between most receptor pairs is only 20% or less (at the amino acid sequence level).…”

“…Boxes indicated branches with 75-100% bootstrap support. Modified after [43] and [15] variable combinations of other Gr genes, which implies that possibly every Gr66a-expressing neuron may respond to overlapping, albeit distinct sets of chemical ligands. Although coexpression of these genes has not been investigated in detail outside the labial palps, there is at least one gene, Gr22e, that is expressed in GRNs of the wing that do not express Gr66a [36].…”

“…The Drosophila genome encodes hundreds of GPCRs, including the 68 GRs and 60 ORs [43]. However, only 16 genes predicted to encode G-protein subunits have been identified: 11 α subunits, three β subunits, and two γ subunits [89].…”

Generation and modulation of chemosensory behaviors in C. elegans

“…Given the critical importance of chemosensation for the worm's survival, it is perhaps not surprising that nearly 10% of the C. elegans genome is devoted to encoding predicted chemosensory receptors (CRs), a current total of ∼1,500 molecules [58, [116][117][118]. In comparison, the Drosophila genome is predicted to encode ∼62 olfactory and ∼68 gustatory receptors [119][120][121][122][123], whereas the mouse genome encodes ∼1,200 olfactory and 38 gustatory GPCRs [93,94,[124][125][126][127][128]. Although the expression patterns of only a handful of CR genes have been examined [58,129], it is clear that in stark contrast to the vertebrate or Drosophila olfactory systems, each chemosensory neuron in C. elegans expresses multiple CR genes, perhaps as many as 20 per neuron type (Fig.…”

A Systematic Analysis of Drosophila Gustatory Receptor Gene Expression in Abdominal Neurons which Project to the Central Nervous System

“…68 Drosophila gustatory receptors are made from 60 gustatory receptor (Gr) genes, due to alternatively spliced forms (Clyne et al, 2000;Dunipace et al, 2001;Robertson et al, 2003;Scott et al, 2001). Many studies have focused on the expression and function of these Grs in taste organs that have access to external sensory cues including the labellum, the pharyngeal organs, and the tarsi (Isono and Morita, 2010;Thorne et al, 2004;Wang et al, 2004;Weiss et al, 2011).…”