The red flour beetle's large nose: An expanded odorant receptor gene family in Tribolium castaneum

Abstract

The Tribolium castaneum genome sequence reveals a large number of odorant receptor (Or) genes compared to those found in other insects whose olfactory genomes have been studied-341 Or genes and pseudogenes, encoding 259 intact odorant receptor proteins. An RT-PCR study of larvae and adults revealed that only 145 (64%) of 233 genes with successful genomic DNA amplifications were expressed. No expression of the other 87 genes was detected at any age, suggesting either that these genes are not expressed in this particular strain, or that they are induced only in certain environmental or developmental conditions. TcOR1, the ortholog of the Drosophila Or83b (DmOr83b) gene, which is required for the function of olfactory receptor proteins in Drosophila, was expressed in extracts from adult and larval heads and in extracts from adult bodies. Expression of 41 TcOr genes was detected in extracts from larval head tissue and 111 in extracts from adult head tissue (both figures exclude TcOr1). Twenty-eight TcOrs were detected only in adult bodies. Beetle pupae were injected with TcOr1 dsRNA; unlike sham-injected and control beetles, these knock-down beetles showed no significant response to the Tribolium aggregation pheromone, supporting the hypothesis that TcOr1 plays a similar decisive role in olfaction to DmOr83b. The substantial number of Ors poses the question of why Tribolium has such a large olfactory receptor repertoire, and underlines the need for more studies of the natural history of this species.

Molecular evolution of the major chemosensory gene families in insects

“…Interestingly, the clustered arrangement is also maintained in other insect genomes (Xu et al, 2003;Forêt and Maleszka 2006). Drosophila OR and GR genes, on the other hand, appear more scattered throughout the genome, having only a few clusters (Robertson et al, 2003); this distribution differs from other insects where the receptor genes are arranged in a number of clusters (Robertson and Wanner, 2006;Bohbot et al, 2007;Engsontia et al, 2008). Indeed, the chromosomal distribution of OR genes have revealed repeated inter-chromosomal translocation events across the Drosophila phylogeny; these evolutionary events seem to be more frequent in this receptor family than in the OBP family (Guo and Kim, 2007;Conceição and Aguadé, 2008).…”

“…The insect chemoreceptor superfamily comprises two distant and highly variable protein families, the ORs and GRs (Clyne et al, 1999(Clyne et al, , 2000Gao and Chess, 1999;Vosshall et al, 1999;Fox et al, 2001;Scott et al, 2001;Hill et al, 2002;Robertson and Wanner, 2006;Engsontia et al, 2008). They are seven-transmembrane domain receptor proteins of about 400 amino acids that bind environmental compounds, thereby transforming the chemical signal into the activation of neurons in the higher processing centres in the brain, which in turn mediate the appropriate behaviour.…”

“…However, a comparison of chemosensory families in distantly related insects (Drosophila, Anopheles, Tribolium and Apis) reveals much more dramatic variation in gene family size and total number of genes. Although the gene copy number tends to be conserved across the chemosensory families of Drosophila, the comparative genomic analyses among these insects have identified an unexpectedly large number of gene gains/losses and pseudogenes (Robertson and Wanner, 2006;Forêt et al, 2007;Engsontia et al, 2008); these numbers are higher for the receptor superfamily than for OBPs. Interestingly, deletions and pseudogenisation events are not randomly distributed across the phylogeny.…”

The genome of the model beetle and pest Tribolium castaneum

“…We identified and annotated 265 apparently functional odorant receptors, 42 full-length pseudogenes and 34 pseudogene fragments. Most of these T. castaneum odorant receptors are in seven species-specific subfamilies, including one containing 150 genes, and most are in tandem gene arrays, created by gene duplication within the Tribolium lineage in the last 300 million years 42 .…”

Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

“…The chemical messages carried by the OBPs and CSPs are decoded when odorant receptors (OR) or in some cases gustatory receptors (GR) selectively bind different chemicals (Vosshall and Stocker, 2007). The odorant receptor family varies in size from 54 genes in Drosophila virilis to 299 in the flour beetle Tribolium castaneum (Nozawa and Nei, 2007;Engsontia et al, 2008). The OBP and CSP gene families are smaller, OBP family containing 4-81 genes and CSP 3-22 genes in the insect species studied this far (Forêt and Maleszka, 2006;Forêt et al, 2007;Gong et al, 2007;Vieira and Rozas, 2011).…”