Abstract
The Hessian fly, Mayetiola destructor Say (Diptera, Cecidomyiidae), is a pest of wheat and belongs to a group of gall-inducing herbivores. This species has a unique life history and several ecological features that differentiate it from other Diptera such as Drosophila melanogaster and blood-feeding mosquitoes. These features include a short, non-feeding adult life stage (1–2 days) and the use of a long-range sex pheromone produced and released by adult females. Sex pheromones are detected by members of the odorant receptor (OR) family within the Lepidoptera, but no receptors for similar long-range sex pheromones have been characterized from the Diptera. Previously, 122 OR genes have been annotated from the Hessian fly genome, with many of them showing sex-biased expression in the antennae. Here we have expressed, in HEK293 cells, five MdesORs that display male-biased expression in antennae, and we have identified MdesOR115 as a Hessian fly sex pheromone receptor. MdesOR115 responds primarily to the sex pheromone component (2S,8E,10E)-8,10-tridecadien-2-yl acetate, and secondarily to the corresponding Z,E-isomer. Certain sensory neuron membrane proteins (i.e., SNMP1) are important for responses of pheromone receptors in flies and moths. The Hessian fly genome is unusual in that it encodes six SNMP1 paralogs, of which five are expressed in antennae. We co-expressed each of the five antennal SNMP1 paralogs together with each of the five candidate sex pheromone receptors from the Hessian fly and found that they do not influence the response of MdesOR115, nor do they confer responsiveness in any of the non-responsive ORs to any of the sex pheromone components identified to date in the Hessian fly. Using Western blots, we detected protein expression of MdesOrco, all MdesSNMPs, and all MdesORs except for MdesOR113, potentially explaining the lack of response from this OR. In conclusion, we report the first functional characterization of an OR from the Cecidomyiidae, extending the role of ORs as long-range sex pheromone detectors from the Lepidoptera into the Diptera.
Highlights
Insects are often dependent on communication via sex pheromones to reproduce
Both of these pheromone components are present in minute amounts in female gland extracts, but they elicit powerful responses in male antennae, and both are required for optimal male attraction (Andersson et al, 2009)
It is likely that part of the response by MdesOR115 to the Z,E-isomer was due to the presence of 2S-8E,10E-13:OAc in the stimulus, and this receptor might be more specific for the E,E-isomer than it appears
Summary
Insects are often dependent on communication via sex pheromones to reproduce. In many species of several insect orders, the sex pheromone is produced by the female, and detected by the male via specialized odorant receptors (ORs) that are located in the dendritic membrane of olfactory sensory neurons (OSNs) in the antennae (Wyatt, 2014). A Sex Pheromone Receptor in the Hessian Fly divergent family of 7-transmembrane proteins that are unrelated to the ORs of vertebrates (Kaupp, 2010) These ORs form ligandgated ion channels of unknown stoichiometry together with a conserved co-receptor (Orco), metabotropic signaling seems to contribute to OR responses (reviewed in Carraher et al, 2015). Rapid advances in next-generation sequencing techniques have resulted in an accelerating number of insect species for which sequences of ORs and other proteins involved in chemoreception have been identified (Montagné et al, 2015) Phylogenetic analyses of these receptors have revealed that most species possess one or several species-specific lineage expansions, while other lineages have been reduced or are no longer present in different insect groups (Nei et al, 2008; Ramdya and Benton, 2010; Hansson and Stensmyr, 2011; Benton, 2015). To better understand the functional evolution of ORs and their role in different ecological contexts, deorphanization of ORs must extend beyond the traditional model species
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