Yang Zhiming, Deng Mengqing, Wang Wenxiu, Xiao Tianxiang, Huang Xiaodan, Zhao Xinyu, Xu Xiyue, Li Jun, Sun Zhongxiang, Lu Kai
Key Laboratory of Agri-products Quality and Biosafety (Ministry of Education), Anhui Province Key Laboratory of Crop Integrated Pest Management, Anhui Province Engineering Laboratory for Green Pesticide Development and Application, School of Plant Protection, Anhui Agricultural University, Hefei, 230036, China.
State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, School of Plant Protection, Yunnan Agricultural University, Kunming, 650201, China.
Insect Biochem Mol Biol. 2025 Feb;177:104259. doi: 10.1016/j.ibmb.2025.104259. Epub 2025 Jan 17.
During the long-term interaction between plants and phytophagous insects, plants generate diverse plant secondary metabolites (PSMs) to defend against insects, whereas insects persistently cause harm to plants by detoxifying PSMs. Xanthotoxin is an insect-resistant PSM that is widely found in plants. However, the understanding of detoxification mechanism of xanthotoxin in insects is still limited at present. In this study, RNA-seq analysis showed that uridine diphosphate (UDP)-glycosyltransferases (UGTs) and cap 'n' collar isoform C (CncC) signaling pathway were specifically retrieved from the midgut and fat body of xanthotoxin-administrated Spodoptera litura larvae. The larvae were sensitive to xanthotoxin when the transcriptional expression and enzyme activity of UGTs were inhibited. Bacteria co-expressing UGT had a high survival rate after exposure to xanthotoxin and displayed high metabolic activity to xanthotoxin, which indicated that UGTs were involved in xanthotoxin detoxification. As the pivotal transcription factors, RNA interference against CncC and its partner, muscle aponeurosis fibromatosis isoform K (MafK), reduced larval tolerance to xanthotoxin as well as UGT expressional levels. Dual-luciferase reporter assay demonstrated that UGT promoter activity was activated by CncC and MafK, and was suppressed once CncC/MafK binding site was mutated. This study revealed that CncC signaling pathway regulated UGT transcriptional expression to mediate xanthotoxin detoxification in S. litura, which will facilitate a better understanding of the adaptive mechanism of phytophagous insects to host plants and provide more valuable insecticide targets for pest control.
在植物与植食性昆虫的长期相互作用过程中，植物会产生多种植物次生代谢产物（PSMs）来抵御昆虫，而昆虫则通过对PSMs进行解毒来持续危害植物。黄嘌呤毒素是一种广泛存在于植物中的抗虫PSM。然而，目前对昆虫体内黄嘌呤毒素解毒机制的了解仍然有限。在本研究中，RNA测序分析表明，从经黄嘌呤毒素处理的斜纹夜蛾幼虫的中肠和脂肪体中特异性检索到尿苷二磷酸（UDP）-糖基转移酶（UGTs）和cap 'n' collar异构体C（CncC）信号通路。当UGTs的转录表达和酶活性受到抑制时，幼虫对黄嘌呤毒素敏感。共表达UGT的细菌在接触黄嘌呤毒素后具有较高的存活率，并对黄嘌呤毒素表现出较高的代谢活性，这表明UGTs参与了黄嘌呤毒素的解毒过程。作为关键转录因子，对CncC及其伴侣肌肉腱膜纤维瘤异构体K（MafK）进行RNA干扰，降低了幼虫对黄嘌呤毒素的耐受性以及UGT的表达水平。双荧光素酶报告基因检测表明，UGT启动子活性被CncC和MafK激活，而一旦CncC/MafK结合位点发生突变，其活性就会受到抑制。本研究揭示了CncC信号通路通过调节UGT转录表达来介导斜纹夜蛾对黄嘌呤毒素的解毒作用，这将有助于更好地理解植食性昆虫对寄主植物的适应性机制，并为害虫防治提供更有价值的杀虫剂靶标。
