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Journal of Integrative Agriculture  2024, Vol. 23 Issue (12): 4120-4135    DOI: 10.1016/j.jia.2024.03.043
Special Issue: 昆虫分子生物与功能基因Insect molecular biology
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Functional characterization of sensory neuron membrane protein 1a involved in sex pheromone detection of Apolygus lucorum (Hemiptera: Miridae)

Yan Li1, 2, Xingkui An1, Shuang Shan1, 3, Xiaoqian Pang1, 4, Xiaohe Liu1, Yang Sun2, Adel Khashaveh1#, Yongjun Zhang1#

1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

2 Anhui Provincial Key Laboratory of Molecular Enzymology and Mechanism of Major Diseases, College of Life Sciences, Anhui Normal University, Wuhu 241000, China

3 State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100193, China

4 School of Resource and Environment, Henan Institute of Science and Technology, Xinxiang 453003, China

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摘要  
绿盲蝽Apollygus lucorum(半翅目:盲蝽科)是一种杂食性害虫,危害多种寄主植物。由于它的快速繁殖,目前绿盲蝽的防治仍具有挑战性,因此了解其性信息素的传播是必需的。性信息素的识别由多种化学感觉相关蛋白介导,对求偶和交配行为至关重要。其中,感觉神经元膜蛋白(SNMP),一种CD36相关蛋白,被认为在检测性信息素方面发挥着至关重要的作用。在本研究中,通过对绿盲蝽转录组和基因组数据分析以及系统发育进化进行研究,共鉴定出四个具有完整开放阅读框的假定SNMP基因(AlucSNMP1a, AlucSNMP1b, AlucSNMP2a, 和AlucSNMP2b)。表达谱分析显示,AlucSNMP转录本在多种组织中普遍存在,只有AlucSNMP1a在雄性触角中偏向性表达,这表明其在雄性化学感受中可能发挥作用。利用非洲爪蟾卵母细胞表达系统结合双电极电压钳记录进行功能分析表明,与单独表达性信息受体(PRs)和共受体(Orco)相比,AlucSNMP1a与特异性信息素受体和共受体的共表达显著增强了对性信息素的电生理反应。此外,研究结果表明,AlucSNMP1a的存在不仅影响了对性信息素的反应,还影响了诱导信号的动力学反应(激活和失活)。相反,AlucSNMP1b与AlucPR/Orco复合物的共表达对两种性信息素化合物诱导的电流反应没有影响。对20个物种的SNMP1基因的选择压力的研究表明,这些基因具有很强的正向选择压力,这意味着在各种昆虫中具有潜在的功能保守性。这些发现强调了AlucSNMP1a在性信息素反应中的关键作用。


Abstract  
The mirid bug Apolygus lucorum (Hemiptera: Miridae) is a polyphagous pest that affects a wide range of host plants.  Its control remains challenging mainly due to its rapid reproduction, necessitating an understanding of sex pheromone communication.  The recognition of sex pheromones is vital for courtship and mating behaviors, and is mediated by various chemosensory-associated proteins.  Among these, sensory neuron membrane protein (SNMP), a CD36-related protein, is suggested to play crucial roles in detecting sex pheromones.  In this study, we employed transcriptomic and genomic data from Alucorum and phylogenetic approaches, and identified four putative SNMP genes (AlucSNMP1a, AlucSNMP1b, AlucSNMP2a, and AlucSNMP2b) with full open reading frames.  Expression analysis revealed the ubiquitous presence of AlucSNMP transcripts in multiple tissues, with only AlucSNMP1a exhibiting male-biased expression in the antennae, suggesting its potential role in male chemosensation.  Functional analysis using the Xenopus oocyte expression system, coupled with two-electrode voltage clamp recording, demonstrated that the co-expression of AlucSNMP1a with specific pheromone receptors (PRs) and the Odorant receptor co-receptor (Orco) significantly enhanced electrophysiological responses to sex pheromones compared to the co-expression of PRs and Orco alone.  Moreover, the results indicated that the presence of AlucSNMP1a not only affected the responsiveness to sex pheromones but also influenced the kinetics (activation and inactivation) of the induced signals.  In contrast, the co-expression of AlucSNMP1b with AlucPR/Orco complexes had no impact on the inward currents induced by two pheromone compounds.  An examination of the selective pressures on SNMP1 genes across 20 species indicated strong purifying selection, implying potential functional conservation in various insects.  These findings highlight the crucial role of AlucSNMP1a in the response to sex pheromones.


Keywords:  mirid bug       pheromone perception        sensory neuron membrane proteins        expression profile        receptor interaction        evolution  
Received: 15 December 2023   Accepted: 17 January 2024
Fund: 
This work was supported by the National Natural Science Foundation of China (32150410366, 31972338, and 32372639), the earmarked fund for China Agriculture Research System (CARS-02-26), the National Key Research and Development Program of China (2021YFD1400700), and the Special Grant of China Postdoctoral Science Foundation (2022T150712).
About author:  Yan Li, E-mail: 1950198243@qq.com, #Correspondence Adel Khashaveh, E-mail: akhashaveh@caas.cn; Yongjun Zhang, Tel: +86-10-62815929, E-mail: yjzhang@ippcaas.cn

Cite this article: 

Yan Li, Xingkui An, Shuang Shan, Xiaoqian Pang, Xiaohe Liu, Yang Sun, Adel Khashaveh, Yongjun Zhang. 2024. Functional characterization of sensory neuron membrane protein 1a involved in sex pheromone detection of Apolygus lucorum (Hemiptera: Miridae). Journal of Integrative Agriculture, 23(12): 4120-4135.

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