Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae)

Abstract:
Background: The 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.

Results: We 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.

Conclusions: We 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.