Behavioral Evidence and Olfactory Reception of a Single Alarm Pheromone Component in Halyomorpha halys

Abstract

Halyomorpha halys is a major herbivore insect in the fruit orchards of China that has become a devastating invasive pest in North America and Europe since its accidental introductions in the 1990s and 2000s, respectively. Like other hemipteran insects, H. halys releases defensive chemicals against natural enemies, including (E)-2-decenal, which is an aldehyde associated with alarm pheromones. In this study, a series of electrophysiological and behavioral tests were conducted to characterize the alarm functions of (E)-2-decenal among H. halys adults and nymphs. An antennal transcriptome was obtained from a Chinese H. halys population, and 44 odorant-binding protein (OBP) genes were annotated. Among them, five putative alarm pheromone-binding proteins were screened and were extremely consistent with their homologs from US populations. These five OBPs were later expressed in a heterologous expression system, harvested, and then challenged with (E)-2-decenal in a binding assay. All five OBPs showed high binding activities to (E)-2-decenal, which demonstrated its behavioral significance as a defensive component in H. halys, as well as being the first report of its olfactory reception. These findings will help develop behavioral-mediating tools as part of integrated pest management approaches to control this invasive pest.

Identification of Candidate Olfactory Genes in the Antennal Transcriptome of the Stink Bug Halyomorpha halys

“…However, these assumptions remain to be tested. Our findings, together with those of Paula et al (2016) and Zhong et al (2017Zhong et al ( , 2018, would provide a basis to understand the physiological functions of HhalOBPs and may facilitate to develop approaches for behavioral interference of the pest.…”

“…We found that HhalOBP8, 16, 25, and 30 were highly expressed in H. halys antennae. Coincidently, these four HhalOBPs had higher binding activities to the major component of the alarm pheromone, ( E )-2-decenal, of H. halys ( Zhong et al, 2018 ). The epoxides (3 S ,6 S ,7 R ,10 S )-10,11-epoxy-1-bisabolen-3-ol and (3 R ,6 S ,7 R ,10 S )-10,11-epoxy-1-bisabolen-3-ol were identified as the main components of the aggregation pheromone of H. halys ( Khrimian et al, 2014 ; Weber et al, 2014 ).…”

Tyramine receptor drives olfactory response to (E)-2-decenal in the stink bugHalyomorpha halys

“…Upon HhTAR1 silencing, H. halys 2 nd instar nymphs were tested in their olfactive performances by an innovative behavioral assay. This assay measured the repellent effect of (E)-2-decenal, one of the main alarm compounds released by H. halys under threats, on 2 nd instar nymphs (Zhong et al, 2017;Zhong et al , 2018;Nixon et al, 2018). The HhTAR1-dsRNA treatment caused a reduced sensitivity to (E)-2-decenal in comparison to the LacZ-dsRNA control nymphs.…”

“…The negative control acetone or the positive repellent control (E)-2-decenal were applied to a filter paper (1 cm x 1 cm) that was placed under the green bean. The positive control (E)-2-decenal, dissolved in acetone, was tested at a fixed quantity of 10 µg, a value ensuring the maximum repellence activity against the H. halys nymphs (Zhong et al, 2018). The number of H.…”

Olfactory Reception of Host Alarm Pheromone Component by the Odorant-Binding Proteins in the Samurai Wasp, Trissolcus japonicus (Hymenoptera: Scelionidae)

“…N-Phenyl-1-naphtylamine (1-NPN) was used as the fluorescent probe, and the binding constants of OBP with 1-NPN were determined according to the Scatchard equation. Then, the binding abilities of T. japonicus OBPs and (E)-2-decenal were investigated following the protocol as described by Zhong et al (2018). Each OBP was tested three times and means were used for the analysis.…”