Feng Hong-Yan, Zhao Ya-Qin, Yang Tao, Zhou Yang-Yuntao, Gong Lang-Lang, Zhang Meng-Qi, Ma Yun-Feng, Hull J Joe, Dewer Youssef, Zhang Fan, Smagghe Guy, He Ming, He Peng
State Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, P. R. China.
Pest Management and Biocontrol Research Unit, US Arid Land Agricultural Research Center, USDA Agricultural Research Services, Maricopa, AZ, USA.
Pest Manag Sci. 2025 Feb;81(2):572-584. doi: 10.1002/ps.8530. Epub 2024 Nov 7.
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.
德国小蠊是一种臭名昭著的城市卫生害虫，已对多种杀虫剂产生抗性。因此，迫切需要新型非致死性害虫控制剂。通过干扰与性信息素识别相关的基因来进行嗅觉干扰提供了一种有前景的方法。德国小蠊具有独特的求偶行为，其中成年雌性在触角被触碰时会释放接触性信息素（CSPs），随后引发独特的雄性性行为反应。由于CSPs的挥发性有限，其识别的分子机制以及被激活的特定嗅觉途径仍不清楚。尽管气味受体共受体（Orco）对大多数昆虫的嗅觉至关重要，但感觉神经元膜蛋白（SNMPs），尤其是SNMP1，在蛾类和果蝇的性信息素识别中也起着关键作用。虽然在多种昆虫物种中已鉴定出多个SNMP1同源物，但它们在蟑螂中的功能尚未完全表征。
在本研究中，RNA干扰（RNAi）介导的BgerOrco基因敲低降低了雄性的电生理反应和求偶行为，表明CSP感知是通过嗅觉途径进行的。在雄性触角中主要表达的BgerSNMP1e和BgerSNMP1d的类似RNAi敲低揭示了它们在感知德国小蠊CSP混合物主要成分中的关键作用。与BgerSNMP1e不同，还发现BgerSNMP1d在感知CSP次要成分中起作用。分子对接分析表明，BgerSNMP1d对CSP主要成分和次要成分的结合亲和力没有差异，而BgerSNMP1e的结合亲和力对主要成分表现出明显的选择性。
我们的结果表明，嗅觉途径对CSP识别至关重要，并且两个在雄性中富集的SNMP基因BgerSNMP1e和BgerSNMP1d是介导德国小蠊雄性对CSP刺激反应的关键因素。本研究为研究CSP识别机制奠定了基础，并提供了具有作为求偶行为干扰剂开发潜力的新型分子靶点。© 2024化学工业协会。
