Female contact sex pheromone recognition in the German cockroach (Blattella germanica) is mediated by two male antennae-enriched sensory neuron membrane proteins.

Abstract

The German cockroach Blattella germanica is a notorious urban health pest that has developed resistance to multiple pesticides. Thus, novel non-lethal pest control agents are urgently needed. Olfaction interference via disruption of sex pheromone recognition-related genes offers a promising approach. The German cockroach has a unique courtship behavior in which female adults emit contact sex pheromones (CSPs) in response to antennal touching, which subsequently triggers distinctive male sex behavioral responses. Due to the limited volatility of CSPs, the molecular mechanisms underlying their recognition and the specific olfactory pathways activated remain poorly defined. Although the odorant receptor coreceptor (Orco) is critical for most insect olfaction, sensory neuron membrane proteins (SNMPs), in particular SNMP1, also play crucial roles in sex pheromone recognition in moths and flies. While multiple SNMP1 homologs have been identified in multiple insect species, they have yet to be fully functionally characterized in cockroaches. In this study, RNA-interference (RNAi)-mediated knockdown of BgerOrco reduced both the electrophysiology responses and courtship behaviors of males, indicating CSP perception proceeds via an olfaction pathway. Similar RNAi knockdown of BgerSNMP1e and BgerSNMP1d, which are predominantly expressed in male antennae, revealed critical roles in perceiving the major component of the Blattella germanica CSP blend. Unlike BgerSNMP1e, BgerSNMP1d was also found to function in the perception of the minor CSP component. Molecular docking analyses revealed no differences in the binding affinities of BgerSNMP1d for the major and minor CSP components, whereas the binding affinities of BgerSNMP1e displayed clear selectivity for the major component. Our results show that the olfactory pathway is critical for CSP recognition and that two male-enriched SNMP genes, BgerSNMP1e and BgerSNMP1d, are crucial factors mediating the male response to CSP stimulation in German cockroaches. This study lays a foundation for studying the mechanisms of CSP recognition and provides novel molecular targets with potential to be exploited as disruptors of courtship behavior. © 2024 Society of Chemical Industry.