Department of Biology, Lund University, Lund, Sweden.
Department of Chemistry and Biomedical Sciences, Faculty of Health and Life Sciences, Linnaeus University, Kalmar, Sweden.
Mol Biol Evol. 2021 Oct 27;38(11):4934-4947. doi: 10.1093/molbev/msab218.
Insects detect odors using an array of odorant receptors (ORs), which may expand through gene duplication. How and which new functions may evolve among related ORs within a species remain poorly investigated. We addressed this question by functionally characterizing ORs from the Eurasian spruce bark beetle Ips typographus, in which physiological and behavioral responses to pheromones, volatiles from host and nonhost trees, and fungal symbionts are well described. In contrast, knowledge of OR function is restricted to two receptors detecting the pheromone compounds (S)-(-)-ipsenol (ItypOR46) and (R)-(-)-ipsdienol (ItypOR49). These receptors belong to an Ips-specific OR-lineage comprising seven ItypORs. To gain insight into the functional evolution of related ORs, we characterized the five remaining ORs in this clade using Xenopus oocytes. Two receptors responded primarily to the host tree monoterpenes (+)-3-carene (ItypOR25) and p-cymene (ItypOR27). Two receptors responded to oxygenated monoterpenoids produced in larger relative amounts by the beetle-associated fungi, with ItypOR23 specific for (+)-trans-(1R, 4S)-4-thujanol, and ItypOR29 responding to (+)-isopinocamphone and similar ketones. ItypOR28 responded to the pheromone E-myrcenol from the competitor Ips duplicatus. Overall, the OR responses match well with those of previously characterized olfactory sensory neuron classes except that neurons detecting E-myrcenol have not been identified. The characterized ORs are under strong purifying selection and demonstrate a shared functional property in that they all primarily respond to monoterpenoids. The variation in functional groups among OR ligands and their diverse ecological origins suggest that neofunctionalization has occurred early in the evolution of this OR-lineage following gene duplication.
昆虫使用一系列气味受体（ORs）来检测气味，这些受体可能通过基因复制而扩大。物种内相关 OR 之间如何以及可能进化出哪些新功能仍未得到充分研究。我们通过功能表征欧洲云杉树皮甲虫 Ips typographus 的 OR 来解决这个问题，该甲虫的性信息素、寄主和非寄主树木挥发物以及真菌共生体的生理和行为反应已有很好的描述。相比之下，OR 功能的知识仅限于检测性信息素化合物（S）-（-）-ipsenol（ItypOR46）和（R）-（-）-ipsdienol（ItypOR49）的两个受体。这些受体属于包含七个 ItypOR 的 Ips 特异性 OR 谱系。为了深入了解相关 OR 的功能进化，我们使用非洲爪蟾卵母细胞对该谱系中的其余五个 OR 进行了表征。两个受体主要对寄主树木单萜（+）-3-蒈烯（ItypOR25）和对-伞花烃（ItypOR27）做出反应。两个受体对由与甲虫相关的真菌产生的相对大量含氧单萜化合物有反应，ItypOR23 特异性识别（+）-反式-（1R，4S）-4-松醇，而 ItypOR29 对（+）-异松油精和类似酮类物质有反应。ItypOR28 对来自竞争物种 Ips duplicatus 的性信息素 E-松油醇有反应。总的来说，OR 反应与以前表征的嗅觉感觉神经元类群非常吻合，只是尚未鉴定出检测 E-松油醇的神经元。所表征的 OR 受到强烈的净化选择，并且具有共同的功能特性，即它们都主要对单萜化合物做出反应。OR 配体的功能基团变化及其多样的生态起源表明，在这个 OR 谱系的基因复制后，新功能化很早就发生了。
