Abstract
BackgroundThe chemical senses of insects mediate behaviors that are closely linked to survival and reproduction. The order Diptera contains two model organisms, the vinegar fly Drosophila melanogaster and the mosquito Anopheles gambiae, whose chemosensory genes have been extensively studied. Representing a third dipteran lineage with an interesting phylogenetic position, and being ecologically distinct by feeding on plants, the Hessian fly (Mayetiola destructor Say, Diptera: Cecidomyiidae) genome sequence has recently become available. Among plant-feeding insects, the Hessian fly is unusual in ‘reprogramming’ the plant to create a superior food and in being the target of plant resistance genes, a feature shared by plant pathogens. Chemoreception is essential for reproductive success, including detection of sex pheromone and plant-produced chemicals by males and females, respectively.ResultsWe identified genes encoding 122 odorant receptors (OR), 28 gustatory receptors (GR), 39 ionotropic receptors (IR), 32 odorant binding proteins, and 7 sensory neuron membrane proteins in the Hessian fly genome. We then mapped Illumina-sequenced transcriptome reads to the genome to explore gene expression in male and female antennae and terminal abdominal segments. Our results reveal that a large number of chemosensory genes have up-regulated expression in the antennae, and the expression is in many cases sex-specific. Sex-specific expression is particularly evident among the Or genes, consistent with the sex-divergent olfactory-mediated behaviors of the adults. In addition, the large number of Ors in the genome but the reduced set of Grs and divergent Irs suggest that the short-lived adults rely more on long-range olfaction than on short-range gustation. We also report up-regulated expression of some genes from all chemosensory gene families in the terminal segments of the abdomen, which play important roles in reproduction.ConclusionsWe show that a large number of the chemosensory genes in the Hessian fly genome have sex- and tissue-specific expression profiles. Our findings provide the first insights into the molecular basis of chemoreception in plant-feeding flies, representing an important advance toward a more complete understanding of olfaction in Diptera and its links to ecological specialization.
Highlights
The chemical senses of insects mediate behaviors that are closely linked to survival and reproduction
The proportion of reads that successfully mapped to the Hessian fly genome assembly was high in all four transcriptomes, ranging from 75% to 80%, despite strict mapping parameters that allowed for only 2 bp mismatches to account for the high sequence similarity among recently duplicated chemosensory genes
While many studies of these genes have been performed on Diptera, especially Drosophila and mosquitoes, this is the first of a fly that feeds on plants
Summary
The chemical senses of insects mediate behaviors that are closely linked to survival and reproduction. The sequencing of insect genomes and more recently of transcriptomes from chemosensory appendages, have paved the way for identification and characterization of the gene families that are important for chemoreception e.g. Receptors encoded by three large gene families are involved in chemoreception and expressed in sensory neurons, located mainly on the antennae and to a lesser extent on other sensory appendages [7]. These families encode the odorant receptors (OR), gustatory receptors (GR), and ionotropic receptors (IR) [8,9,10]. OBPs have been shown to improve the specificity of pheromone-detecting neurons [18,19], but see [20]
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