Anosmic flies: what Orco silencing does to olive fruit flies

Kostas D. Mathiopoulos,Alexandros Belavilas-Trovas,Maria-Eleni Gregoriou,Konstantina T. Tsoumani

doi:10.1186/s12863-020-00937-0

Abstract

BackgroundThe olive fruit fly (Bactrocera oleae) is the most destructive pest of the olive cultivation worldwide causing significant production losses and olive fruit impoverishment, as its larvae feed exclusively on the olive fruit. Reproductive and sexual behavior, as well as host-plant recognition of the fly, are highly dependent on its chemosensory system. Therefore, exploring the role of genes that play a critical role in olfaction, could reveal potential molecular targets that determine species-specific features on chemical communication and could be used to impair sexual behavior.ResultsIn this study we identified the gene that encodes the conserved olfactory co-receptor Orco (Odorant receptor co-receptor), which interacts with all divergent insect odorant receptors, and investigated how disruption of its expression affects chemoreception. We initially searched the expression profile of Bo-Orco in both sexes during sexual maturation, as well as pre- and post-mating communication by relative quantitative real time PCR (qRT-PCR) analysis suggesting that Bo-Orco was abundantly expressed in sexually mature adults.We further investigated the functional role of Bo-Orco in mating and oviposition behavior via transient gene silencing that was performed through in vivo dsRNA hemolymph injections in sexually mature flies 7 days after eclosion. Orco-knockdown phenotypes in both sexes showed reduced copulation rates in mating competitiveness tests, possibly through impaired olfactory-mediated detection of sex pheromone. In addition, oviposition was significantly inhibited in dsRNA-Orco injected females in a post-mating behavior test.ConclusionsOur results demonstrate that Orco plays a crucial role in the reproductive behavior of the olive fruit fly, since pre- and post-mating processes were affected. This is the first report in the olive fruit fly that links the chemosensory pathway with the mating behavior and the reproductive potential at a molecular basis, rendering this gene a potential target for the improvement of the olive fruit fly population control techniques.

Highlights

The olive fruit fly (Bactrocera oleae) is the most destructive pest of the olive cultivation worldwide causing significant production losses and olive fruit impoverishment, as its larvae feed exclusively on the olive fruit
XM_014236978.1) has been identified by homology Blastp searches against the NCBI non-redundant protein database of Bactrocera oleae using the Drosophila melanogaster orthologue as a query
Bactrocera oleae (Bo)-olfactory receptor co-receptor (Orco) spans a 14,416 bp genomic locus and consists of seven exons that encode a protein of 473 amino acid residues (XP_014092453.1) (Fig. 1a)

Summary

Introduction

The olive fruit fly (Bactrocera oleae) is the most destructive pest of the olive cultivation worldwide causing significant production losses and olive fruit impoverishment, as its larvae feed exclusively on the olive fruit. The caused damage results mainly from the oviposition stings onto the olive fruits by the female insects while laying their eggs, as well as from the pulp destruction by its developing monophagous larvae [1, 2]. These detrimental consequences are associated with reproductive success (mating and oviposition) and effective host-seeking. Insects should be reproductive mature in order to respond to sexual signals under the appropriate environmental conditions necessary for their life history traits.

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Results

Conclusion