Functional characterization of olfactory receptors in the Oriental fruit fly Bactrocera dorsalis that respond to plant volatiles

Abstract

The Oriental fruit fly, Bactrocera dorsalis, is a highly destructive pest of various fruits. The reproductive and host-finding behaviors of this species are affected by several plant semiochemicals that are perceived through chemosensory receptors. However, the chemosensory mechanisms by which this perception occurs have not been fully elucidated. We conducted RNA sequencing analysis of the chemosensory organs of B. dorsalis to identify the genes coding for chemosensory receptors. We identified 60 olfactory receptors (ORs), 17 gustatory receptors and 23 ionotropic receptors-including their homologs and variants-from the transcriptome of male antennae and proboscises. We functionally analyzed ten ORs co-expressed with the obligatory co-receptor ORCO in Xenopus oocytes to identify their ligands. We tested 24 compounds including attractants for several Bactrocera species and volatiles from the host fruits of B. dorsalis. We found that BdorOR13a co-expressed with ORCO responded robustly to 1-octen-3-ol. BdorOR82a co-expressed with ORCO responded significantly to geranyl acetate, but responded weakly to farnesenes (a mixture of isomers) and linalyl acetate. These four compounds were subsequently subjected to behavioral bioassays. When each of the aforementioned compound was presented in combination with a sphere model as a visual cue to adult flies, 1-octen-3-ol, geranyl acetate, and farnesenes significantly enhanced landing behavior in mated females, but not in unmated females or males. These results suggest that the ORs characterized in the present study are involved in the perception of plant volatiles that affect host-finding behavior in B. dorsalis.

The diversity and evolution of odorant receptors in beetles (Coleoptera)

“…Ligands have been described for most of the ORs in Drosophila melanogaster Meigen (Mansourian and Stensmyr, 2015), and relatively large subsets of ORs have been functionally characterized from a few other insects (Wang et al, 2010;de Fouchier et al, 2017;Liu et al, 2017;Slone et al, 2017). Otherwise, function is broadly known only for the pheromone receptors of the Lepidoptera (Zhang and Löfstedt, 2015;Yuvaraj et al, 2018) and a few ORs from other scattered insect species (eg Mitchell et al, 2012;Andersson et al, 2016;Miyazaki et al, 2018).…”

Involvement of the Antennal and Maxillary Palp Structures in Detection and Response to Methyl Eugenol by Male Bactrocera dorsalis (Diptera: Tephritidae)

“…We believe that these findings support our suggestion that the maxillary palps be an additional focal point of olfactory research in Tephritid fruit flies. This can hopefully be combined with extensive work conducted recently on the transcriptomes of the oriental fruit fly and other Tephritid species focusing on identifying genes and proteins in these species involved in chemoreception ( Zheng et al 2013 ; Wu et al 2015 ; Elfekih et al 2016 ; Liu et al 2016 ; 2017 , 2018 ; Miyazaki et al 2018 ) as part of the search for novel ways to control these highly destructive and invasive pests.…”

“…Concomitant with current rapid developments in functional genomics and associated technologies in insects ( Suh et al 2014 , Elfekih et al 2016 , Miyazaki et al 2018 ), elucidation of mechanisms of odorant reception in the antennae of insect pests has gained considerable attention that may ultimately assist in the development of novel pest management strategies ( Brito et al 2016 , Reisenman et al 2016 ). Hitherto, much work has been focused on the antennae ( Hansson 1999 , Hansson and Stensmyr 2011 ) compared with maxillary palp, although it is known that the antenna and maxillary palp form two bilateral and symmetrical pairs of olfactory organs on an insect’s head.…”

Deorphanization of an odorant receptor revealed new bioactive components for green mirid bug Apolygus lucorum (Hemiptera: Miridae)

“…[13][14][15] Insect ORs are highly divergent seven-transmembrane ligand-specific proteins which have been described as heteromeric ligand-gated ion channels and work as complexes together with a highly conserved OR called OR co-receptor (Orco). 13,16 Since the first report of ORs in Drosophila, several methods have been developed for functional studies of ORs, of which heterologous expression in Xenopus oocyte and two-electrode voltage-clamp system (TEVC) have been adopted for several years. 8,13,14,16,17 Recently, based on transcriptome and genome sequencing, a large number of insect OR repertoires have been identified.…”

“…13,16 Since the first report of ORs in Drosophila, several methods have been developed for functional studies of ORs, of which heterologous expression in Xenopus oocyte and two-electrode voltage-clamp system (TEVC) have been adopted for several years. 8,13,14,16,17 Recently, based on transcriptome and genome sequencing, a large number of insect OR repertoires have been identified. [17][18][19] A total of 109 ORs has been annotated in A. lucorum 20 .…”