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

Authors: FENG, HONG-YAN - Guizhou University; ZHAO, YA-QIN - Guizhou University; ZHOU, YANG-YUNTAO - Guizhou University; GONG, LANG-LANG - Guizhou University; ZHANG, MENG-QI - Guizhou University; MA, YUN-FENG - Guizhou University; Hull, Joe; DEWER, YOUSSEF - Agricultural Research Center Of Egypt; ZHANG, FAN - Guizhou University; HE, MING - Guizhou University; HE, PENG - Guizhou University

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/15/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: Female cockroaches signal their interest in mating to males via contact sex pheromones that trigger distinctive male sex behaviors. Since contact sex pheromones have lower degrees of gas diffusion than typical sex pheromones, their detection requires physical contact. It is unclear if this detection process proceeds via the stereotypical olfactory pathway. To address this question, key components of insect olfactory pathways previously reported to be involved in volatile sex pheromone detection were identified in cockroach sequence datasets and their functional role in contact sex pheromone detection examined. RNAi-mediated knockdown of transcripts encoding Orco and SNMP1 severely disrupted the behavioral responses of male cockroaches to female contact sex pheromones, indicating that both gene sets are critical to their detection. These findings suggest that strategies specifically targeting genes involved in contact sex pheromone detection/perception may be useful for suppressing future cockroach populations.

Technical Abstract: BACKGROUND: The German cockroach Blatella germanica is a notorious urban health pest. It has a unique courtship behavior in which female adults emit contact sex pheromones (CSPs) in response to antennae touching that subsequently triggers distinctive male sex behaviors. Due to limited CSP volatility, the molecular mechanisms underlying their recognition remain poorly defined with questions regarding the specific olfactory pathway utilized. Although the odorant receptor coreceptor (Orco) is critical for most insect olfaction, sensory neuron membrane proteins (SNMPs), in particular SNMP1, have been found to play a crucial role in sex pheromone recognition in multiple moths and flies. While multiple SNMP1 homologs have been identified in other insect species, they have yet to be fully functionally characterized. RESULTS: In this study, male cockroach courtship behavior was reduced following RNAi-mediated knockdown of Orco, indicating CSP perception is an olfactory process. In addition, male antennae-enrichment of two SNMP1 genes, BgerSNMP1e and BgerSNMP1d, was validated by qPCR and the functional role the two genes have in mediating male responses to CSPs were assessed via RNAi knockdown. Both SNMPs were found to be involved in CSP perception but mediated different behaviors. BgerSNMP1e knockdown had no effect on male wing-raising, but severely reduced courtship index values, whereas knock down of either BgerSNMP1d or BgerSNMP1e/1d reduced male wing-raising but had no effect on the courtship index. Consistent with specific roles in CSP perception molecular docking analyses revealed binding affinities of the two BgerSNMPs for CSP components were higher than for a plant volatile. CONCLUSION: Our results show that the olfactory pathway is critical for CSP recognition and that two male-enriched SNMP genes, BgerSNMP1e and 1d, are crucial factors mediating the male response to CSP stimulation in German cockroaches. This study lays a foundation for further understanding the molecular mechanisms underlying CSP recognition and provides evidence for novel CSP-associated SNMP function.