Lu Chongchong, Jiang Yanke, Yue Yingzhe, Sui Yurong, Hao Mingxia, Kang Xiaojing, Wang Qingbin, Chen Dayin, Liu Baoyou, Yin Ziyi, Wang Lulu, Li Yang, Dong Hansong, Li Xugang, Xin Xiufang, Liu Yinggao, Ding Xinhua
State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, China.
Shandong Pengbo Biotechnology Co., Ltd, Taian, Shandong 271018, China.
J Exp Bot. 2023 Feb 5;74(3):976-990. doi: 10.1093/jxb/erac442.
Plants have evolved a two-layer immune system comprising pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) that is activated in response to pathogen invasion. Microbial patterns and pathogen effectors can be recognized by surface-localized pattern-recognition receptors (PRRs) and intracellularly localized nucleotide-binding leucine-rich repeat receptors (NLRs) to trigger PTI and ETI responses, respectively. At present, the metabolites activated by PTI and ETI and their roles and signalling pathways in plant immunity are not well understood. In this study, metabolomic analysis showed that ETI and PTI induced various flavonoids and amino acids and their derivatives in plants. Interestingly, both glutathione and neodiosmin content were specifically up-regulated by ETI and PTI, respectively, which significantly enhanced plant immunity. Further studies showed that glutathione and neodiosmin failed to induce a plant immune response in which PRRs/co-receptors were mutated. In addition, glutathione-reduced mutant gsh1 analysis showed that GSH1 is also required for PTI and ETI. Finally, we propose a model in which glutathione and neodiosmin are considered signature metabolites induced in the process of ETI and PTI activation in plants and further continuous enhancement of plant immunity in which PRRs/co-receptors are needed. This model is beneficial for an in-depth understanding of the closed-loop mode of the positive feedback regulation of PTI and ETI signals at the metabolic level.
植物进化出了一种由模式触发免疫(PTI)和效应子触发免疫(ETI)组成的两层免疫系统,该系统在病原体入侵时被激活。微生物模式和病原体效应子可分别被位于表面的模式识别受体(PRR)和位于细胞内的核苷酸结合富含亮氨酸重复序列受体(NLR)识别,从而触发PTI和ETI反应。目前,PTI和ETI激活的代谢产物及其在植物免疫中的作用和信号通路尚不清楚。在本研究中,代谢组学分析表明,ETI和PTI在植物中诱导了各种黄酮类化合物、氨基酸及其衍生物。有趣的是,谷胱甘肽和新地奥明的含量分别被ETI和PTI特异性上调,这显著增强了植物免疫力。进一步研究表明,谷胱甘肽和新地奥明在PRR/共受体发生突变的情况下无法诱导植物免疫反应。此外,谷胱甘肽还原突变体gsh1分析表明,GSH1也是PTI和ETI所必需的。最后,我们提出了一个模型,其中谷胱甘肽和新地奥明被认为是植物ETI和PTI激活过程中诱导产生的标志性代谢产物,并且在需要PRR/共受体的情况下进一步持续增强植物免疫力。该模型有助于在代谢水平上深入理解PTI和ETI信号正反馈调节的闭环模式。