Ren Yipeng, Dong Wenhao, Chen Juhong, Bu Wenjun, Xue Huaijun
Institute of Entomology, College of Life Sciences, Nankai University, Tianjin, 300071, PR China.
Tianjin Key Laboratory of Food and Biotechnology, School of Biotechnology and Food Science, Tianjin University of Commerce, Tianjin, 300134, PR China.
Dev Comp Immunol. 2025 Jan;162:105294. doi: 10.1016/j.dci.2024.105294. Epub 2024 Nov 28.
The Toll pathway was first identified in Drosophila and plays an essential role in defense against infection by various pathogens. To date, various noncoding RNAs (ncRNAs) have been demonstrated to maintain immune homeostasis by regulating several target genes in the insect Toll pathway. However, the characterization and function of Toll pathway genes involved in the response to environmental changes at the posttranscriptional level associated with gut bacterial changes in Riptortus pedestris, which is a significant pest of soybeans, remain unclear. In this study, we identified and classified six Toll genes into three subtypes with typical Toll domain arrangements, including a Toll/interleukin receptor (TIR) domain, a transmembrane domain, and multiple leucine-rich repeat (LRR) domains; in addition, only one positive selection site was found in hemipteran sPP-Tolls, and a total of five downstream members in the Toll signaling pathway were selected and characterized. The expression patterns revealed that all these genes were widely expressed at all developmental stages of R. pedestris, and they presented variable expression levels among the different feeding treatments in the R. pedestris gut. Our comprehensive prediction analysis revealed that there are sixty miRNA‒mRNA interaction pairs, including fifty-six miRNA and six Toll pathway genes (P‒Toll1, sP‒Toll, Myd88, Pelle, Tube, and Cactus), and a ceRNA network comprising two lncRNA‒miRNA‒Toll pairs was constructed in response to environmental changes. Finally, the expression of some above genes and ncRNAs from the ceRNA network exhibited positive or negative association with the most changes in gut bacterial genera via Pearson correlation analysis. These findings provide valuable insights into how the Toll pathway of R. pedestris is involved in environmental adaptation at the posttranscriptional level and identifies new avenues for developing more effective methods for pest control through integration with gut bacteria.
Toll通路最初是在果蝇中发现的，在抵御各种病原体感染中发挥着重要作用。迄今为止，各种非编码RNA（ncRNA）已被证明可通过调节昆虫Toll通路中的几个靶基因来维持免疫稳态。然而，在豆长蝽（一种大豆的重要害虫）中，与肠道细菌变化相关的转录后水平上参与环境变化响应的Toll通路基因的特征和功能仍不清楚。在本研究中，我们鉴定并将六个Toll基因分为具有典型Toll结构域排列的三个亚型，包括一个Toll/白细胞介素受体（TIR）结构域、一个跨膜结构域和多个富含亮氨酸重复序列（LRR）结构域；此外，在半翅目特异性的Toll基因中仅发现一个正选择位点，并选择并鉴定了Toll信号通路中的总共五个下游成员。表达模式表明，所有这些基因在豆长蝽的所有发育阶段都广泛表达，并且它们在豆长蝽肠道的不同取食处理中呈现出不同的表达水平。我们的综合预测分析表明，有60个miRNA-mRNA相互作用对，包括56个miRNA和6个Toll通路基因（P-Toll1、sP-Toll、Myd88、Pelle、Tube和Cactus），并构建了一个包含两个lncRNA-miRNA-Toll对的ceRNA网络以响应环境变化。最后，通过Pearson相关性分析，ceRNA网络中一些上述基因和ncRNA的表达与肠道细菌属的大多数变化呈现正相关或负相关。这些发现为豆长蝽的Toll通路如何在转录后水平参与环境适应提供了有价值的见解，并为通过与肠道细菌整合开发更有效的害虫控制方法指明了新途径。
