Department of Biology, Lund University, Sölvegatan 37, 223 62, Lund, Sweden.
Present address: Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.
BMC Biol. 2022 Feb 7;20(1):34. doi: 10.1186/s12915-022-01235-0.
In insects, airborne chemical signals are mainly detected by two receptor families, odorant receptors (ORs) and ionotropic receptors (IRs). Functions of ORs have been intensively investigated in Diptera and Lepidoptera, while the functions and evolution of the more ancient IR family remain largely unexplored beyond Diptera.
Here, we identified a repertoire of 26 IRs from transcriptomes of female and male antennae, and ovipositors in the moth Agrotis segetum. We observed that a large clade formed by IR75p and IR75q expansions is closely related to the acid-sensing IRs identified in Diptera. We functionally assayed each of the five AsegIRs from this clade using Xenopus oocytes and found that two receptors responded to the tested ligands. AsegIR75p.1 responded to several compounds but hexanoic acid was revealed to be the primary ligand, and AsegIR75q.1 responded primarily to octanoic acid, and less so to nonanoic acid. It has been reported that the C-C medium-chain fatty acids repel various insects including many drosophilids and mosquitos. We show that the C-C medium-chain fatty acids elicited antennal responses of both sexes of A. segetum, while only octanoic acid had repellent effect to the moths in a behavioral assay. In addition, using fluorescence in situ hybridization, we demonstrated that the five IRs and their co-receptor AsegIR8a are not located in coeloconic sensilla as found in Drosophila, but in basiconic or trichoid sensilla.
Our results significantly expand the current knowledge of the insect IR family. Based on the functional data in combination with phylogenetic analysis, we propose that subfunctionalization after gene duplication plays an important role in the evolution of ligand specificities of the acid-sensing IRs in Lepidoptera.
在昆虫中，空气传播的化学信号主要由两种受体家族——气味受体 (ORs) 和离子型受体 (IRs) 来检测。ORs 的功能在双翅目和鳞翅目昆虫中得到了深入研究，而更古老的 IR 家族的功能和进化在双翅目之外的昆虫中仍在很大程度上未被探索。
本文从夜蛾 Agrotis segetum 的雌性和雄性触角以及产卵器的转录组中鉴定出了 26 个 IR 基因。我们观察到由 IR75p 和 IR75q 扩张形成的一个大分支与在双翅目昆虫中鉴定出的酸感应 IRs 密切相关。本文使用非洲爪蟾卵母细胞对该分支中的 5 个 AsegIR 进行了功能检测，发现两个受体对测试配体有反应。AsegIR75p.1 对几种化合物有反应，但己酸被证明是主要配体，AsegIR75q.1 主要对辛酸有反应，对壬酸的反应较少。已报道 C-C 中链脂肪酸可排斥包括许多双翅目昆虫和蚊子在内的多种昆虫。本文表明，C-C 中链脂肪酸引起了 A. segetum 两性触角的反应，而只有辛酸在行为测定中对飞蛾有驱避作用。此外，通过荧光原位杂交，本文证明了这 5 个 IR 和它们的共同受体 AsegIR8a 并不像在果蝇中那样位于腔锥形感器中，而是位于锥形感器或毛形感器中。
本文的研究结果显著扩展了昆虫 IR 家族的现有知识。基于功能数据和系统发育分析，本文提出了基因复制后的亚功能化在鳞翅目昆虫中酸感应 IRs 配体特异性进化中发挥了重要作用。
