College of Pharmacy and Research Institute of Pharmaceutical Science, PMBBRC, Gyeongsang National University, Jinju, 660-701, Republic of Korea.
National Institute of Agricultural Sciences, Rural Development Administration, Jeonju, Republic of Korea.
Plant Physiol Biochem. 2020 Nov;156:105-114. doi: 10.1016/j.plaphy.2020.09.002. Epub 2020 Sep 5.
Many stresses induce the accumulation of unfolded and misfolded proteins in the endoplasmic reticulum, a phenomenon known as ER stress. In response to ER stress, cells initiate a protective response, known as unfolded protein response (UPR), to maintain cellular homeostasis. The UPR sensor, inositol-requiring enzyme 1 (IRE1), catalyzes the cytoplasmic splicing of bZIP transcription factor-encoding mRNAs to activate the UPR signaling pathway. Recently, we reported that pretreatment of Arabidopsis thaliana plants with tunicamycin, an ER stress inducer, increased their susceptibility to bacterial pathogens; on the other hand, IRE1 deficient mutants were susceptible to Pseudomonas syringae pv. maculicola (Psm) and failed to induce salicylic acid (SA)-mediated systemic acquired resistance. However, the functional relationship of IRE1 with the pathogen and TM treatment remains unknown. In the present study, we showed that bacterial pathogen-associated molecular patterns (PAMPs) induced IRE1 expression; however, PAMP-triggered immunity (PTI) response such as callose deposition, PR1 protein accumulation, or Pst DC3000 hrcC growth was not altered in ire1 mutants. We observed that IRE1 enhanced plant immunity against the bacterial pathogen P. syringae pv. tomato DC3000 (Pst DC3000) under ER stress. Moreover, TM-pretreated ire1 mutants were more susceptible to the avirulent strain Pst DC3000 (AvrRpt2) and showed greater cell death than wild-type plants during effector-triggered immunity (ETI). Additionally, Pst DC3000 (AvrRpt2)-mediated RIN4 degradation was reduced in ire1 mutants under TM-induced ER stress. Collectively, our results reveal that IRE1 plays a pivotal role in the immune signaling pathway to activate plant immunity against virulent and avirulent bacterial strains under ER stress.
许多应激都会导致内质网中未折叠和错误折叠蛋白的积累，这种现象称为内质网应激。为了应对内质网应激，细胞会启动一种保护反应，称为未折叠蛋白反应（UPR），以维持细胞内环境稳定。UPR 传感器肌醇需求酶 1（IRE1）可催化 bZIP 转录因子编码 mRNA 的细胞质剪接，从而激活 UPR 信号通路。最近，我们报道称，用内质网应激诱导剂衣霉素预处理拟南芥会增加其对细菌病原体的易感性；另一方面，IRE1 缺陷突变体易感染丁香假单胞菌 pv. maculicola（Psm），并且无法诱导水杨酸（SA）介导的系统获得性抗性。然而，IRE1 与病原体和 TM 处理之间的功能关系仍不清楚。在本研究中，我们发现细菌病原体相关分子模式（PAMPs）诱导了 IRE1 的表达；然而，在 ire1 突变体中，PAMP 触发的免疫（PTI）反应，如胼胝质沉积、PR1 蛋白积累或 Pst DC3000 hrcC 生长，并未改变。我们观察到 IRE1 在 ER 应激下增强了植物对细菌病原体丁香假单胞菌 pv. tomato DC3000（Pst DC3000）的免疫力。此外，在 ER 应激下，用 TM 预处理的 ire1 突变体对无毒菌株 Pst DC3000（AvrRpt2）更敏感，并且在效应子触发免疫（ETI）期间比野生型植物表现出更高的细胞死亡。此外，在 TM 诱导的 ER 应激下，ire1 突变体中 Pst DC3000（AvrRpt2）介导的 RIN4 降解减少。总之，我们的研究结果揭示了 IRE1 在免疫信号通路中起着关键作用，可激活植物对 ER 应激下毒力和无毒细菌株的免疫力。
