Silencing the odorant coreceptor (Orco) disrupts sex pheromonal communication and feeding responses in Blattella germanica: toward an alternative target for controlling insect‐transmitted human diseases

Abstract

BACKGROUND The German cockroach, Blattella germanica, is one of the most severe pests of urban and rural areas. High‐throughput genetic screening approaches indicate that the olfactory system of this pest is extremely powerful because it has an extensive array of olfactory receptor genes compared with many other insect species. Several of these genes have been identified previously, but their functions have not yet been characterized. RESULTS This study describes the sequence of five transcriptomes of B. germanica adult male antennae, female antennae, maxillary palps, legs, and fifth‐instar nymph antennae to investigate expression patterns of odorant receptors (ORs). Approximately 90% of ORs were found to be the most highly expressed genes in adult or nymph antennae. Additionally, every OR requires an odorant co‐receptor (Orco) to become fully functional, and this was selected and successfully inhibited by injection of the corresponding double‐stranded (ds)RNA targeting the Orco. A strong RNA interference (RNAi) effect was observed in which > 75% of Orco messenger RNA (mRNA) was clearly suppressed after 72 h of treatment. Olfactory behavioral assays showed that Orco‐impaired B. germanica respond more slowly and show less attraction to one volatile sex pheromone and food resources compared with a control group. CONCLUSION The results show that Orco plays a pivotal role in both sex pheromone and food‐seeking olfactory processes, and provide an alternative genetic technique for controlling this urban pest species by olfactory disruption. © 2020 Society of Chemical Industry

Silencing the odorant receptor co-receptor impairs olfactory reception in a sensillum-specific manner in the cockroach

“…We characterized ORco from the genome of P. americana . Among species in the order Blattodea, whole alignment of ORco has been conducted with sequences from the German cockroach B. germanica and two species of termites Reticulitermes chinensis and Odontotermes formosanus ( Robertson et al., 2018 ; Gao et al., 2020 ; He et al., 2020 ). Consistent with the result of a recent nuclear phylogenomic study of the order Blattodea ( Evangelista et al., 2019 ), PameORco exhibits higher homology with ORco of termites than that of B. germanica ( Figure S1 ; Robertson et al., 2018 ).…”

“…Therefore, ORco-impaired insects exhibit anosmia to a given set of odors. In both holometabolous and hemimetabolous insect species including closely related cockroach Blattella germanica , the mutagenesis or silencing of ORco disrupts odor-guided behaviors, such as orientations to various odorants and pheromone detection ( Larsson et al., 2004 ; DeGennaro et al., 2013 ; Li et al., 2016 ; Fandino et al., 2019 ; Gao et al., 2020 ; He et al., 2020 ; Sun et al., 2020 ). In addition, volatile agonists of ORco elicit behavioral responses in many species of insects ( Batra et al., 2019 ).…”

The Odorant Binding Protein, SiOBP5, Mediates Alarm Pheromone Olfactory Recognition in the Red Imported Fire Ant, Solenopsis invicta

“…Our results indicate that the RNAi Orco dsRNA-injection resulted in a significant reduction in the transcript level and electrophysiological recording of the response to EDP, TMP, and ylang ylang oil. Insect Orcos are highly conserved, not only in S. invicta , and the RNAi silencing the olfactory Orco also reduced the response to pheromones in other insects, including the red palm weevil ( Rhynchophours ferrugineus ) [ 27 ], Grapholita molesta [ 28 ], Protaetia brevitarsis Lewis [ 29 ] Blattella germanica [ 30 ], aphids [ 31 ], subterranean termite [ 32 ], gypsy moth [ 33 ], Rhodnius prolixus [ 34 ], Bactrocera dorsalis [ 35 ], and Apolygus lucorum [ 36 ]. Orco silencing may provide a novel approach for managing various pest insects, including pest ants.…”

Identification of candidate chemosensory genes by antennal transcriptome analysis in an ectoparasitoid wasp

“…Furthermore, the ligands were recognized through hydrophobic interactions within the binding pocket located in each subunit, suggesting the structure may be related to the chemical sensitivity of Orco (del Mármol et al., 2021). For example, the results of behavioural assays indicated a decreased response to sex pheromone and food volatiles in Blattella germanica by silencing Orco gene (He et al., 2021).…”