College of Animal Sciences, Zhejiang University, Hangzhou, China.
Laboratory of Insect Genetics and Bioscience, Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan.
Mol Ecol. 2019 Dec;28(24):5282-5298. doi: 10.1111/mec.15291. Epub 2019 Nov 25.
Gene duplication provides a major source of new genes for evolutionary novelty and ecological adaptation. However, the maintenance of duplicated genes and their relevance to adaptive evolution has long been debated. Insect trehalase (Treh) plays key roles in energy metabolism, growth, and stress recovery. Here, we show that the duplication of Treh in Lepidoptera (butterflies and moths) is linked with their adaptation to various environmental stresses. Generally, two Treh genes are present in insects: Treh1 and Treh2. We report three distinct forms of Treh in lepidopteran insects, where Treh1 was duplicated into two gene clusters (Treh1a and Treh1b). These gene clusters differ in gene expression patterns, enzymatic properties, and subcellular localizations, suggesting that the enzymes probably underwent sub- and/or neofunctionalization in the lepidopteran insects. Interestingly, selective pressure analysis provided significant evidence of positive selection on duplicate Treh1b gene in lepidopteran insect lineages. Most positively selected sites were located in the alpha-helical region, and several sites were close to the trehalose binding and catalytic sites. Subcellular adaptation of duplicate Treh1b driven by positive selection appears to have occurred as a result of selected changes in specific sequences, allowing for rapid reprogramming of duplicated Treh during evolution. Our results suggest that gene duplication of Treh and subsequent functional diversification could increase the survival rate of lepidopteran insects through various regulations of intracellular trehalose levels, facilitating their adaptation to diverse habitats. This study provides evidence regarding the mechanism by which gene family expansion can contribute to species adaptation through gene duplication and subsequent functional diversification.
基因复制为进化新奇和生态适应提供了新基因的主要来源。然而，复制基因的维持及其与适应性进化的相关性一直存在争议。昆虫海藻糖酶（Treh）在能量代谢、生长和应激恢复中发挥着关键作用。在这里，我们表明 Lepidoptera（蝴蝶和飞蛾）中 Treh 的复制与它们对各种环境压力的适应有关。通常，昆虫中有两种 Treh 基因：Treh1 和 Treh2。我们报告了 Lepidoptera 昆虫中存在三种不同形式的 Treh，其中 Treh1 被复制成两个基因簇（Treh1a 和 Treh1b）。这些基因簇在基因表达模式、酶特性和亚细胞定位上存在差异，表明这些酶可能在 Lepidoptera 昆虫中经历了亚功能化和/或新功能化。有趣的是，选择压力分析为 Lepidoptera 昆虫谱系中重复 Treh1b 基因的正选择提供了重要证据。大多数正选择位点位于α-螺旋区，几个位点靠近海藻糖结合和催化位点。正选择驱动的重复 Treh1b 的亚细胞适应似乎是由于特定序列的选择变化而发生的，这允许在进化过程中快速重新编程重复 Treh。我们的研究结果表明，Treh 的基因复制和随后的功能多样化可能通过各种调节细胞内海藻糖水平来提高鳞翅目昆虫的存活率，从而促进它们对不同栖息地的适应。这项研究提供了证据，证明了基因家族扩张如何通过基因复制和随后的功能多样化为物种适应做出贡献。
