College of Agronomy, Qingdao Agricultural University, Qingdao 266109, China.
Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao 266101, China.
Plant Physiol. 2022 Oct 27;190(3):1941-1959. doi: 10.1093/plphys/kiac300.
Perception of pathogen-associated molecular patterns (PAMPs) triggers mitogen-activated protein (MAP) kinase 4 (MPK4)-mediated phosphorylation and induces downstream transcriptional reprogramming, but the mechanisms of the MPK4 defense pathway are poorly understood. Here, we showed that phosphorylation-mediated inactivation of the CCCH protein C3H14 by MPK4 positively regulates the immune response in Arabidopsis (Arabidopsis thaliana). Compared with wild-type plants, loss-of-function mutations in C3H14 and its paralog C3H15 resulted in enhanced defense against Pst DC3000 in infected leaves and the development of systemic acquired resistance (SAR), whereas C3H14 or C3H15 overexpression enhanced susceptibility to this pathogen and failed to induce SAR. The functions of C3H14 in PAMP-triggered immunity (PTI) and SAR were dependent on MPK4-mediated phosphorylation. Challenge with Pst DC3000 or the flagellin peptide flg22 enhanced the phosphorylation of C3H14 by MPK4 in the cytoplasm, relieving C3H14-inhibited expression of PTI-related genes and attenuating C3H14-activated expression of its targets NIM1-INTERACTING1 (NIMIN1) and NIMIN2, two negative regulators of SAR. Salicylic acid (SA) affected the MPK4-C3H14-NIMIN1/2 cascades in immunity, but SA signaling mediated by the C3H14-NIMIN1/2 cascades was independent of MPK4 phosphorylation. Our study suggests that C3H14 might be a negative component of the MPK4 defense signaling pathway.
病原体相关分子模式（PAMPs）的感知会触发丝裂原激活蛋白（MAP）激酶 4（MPK4）介导的磷酸化，并诱导下游转录重编程，但 MPK4 防御途径的机制尚不清楚。在这里，我们表明，MPK4 通过磷酸化介导 CCCH 蛋白 C3H14 的失活，可正向调控拟南芥（Arabidopsis thaliana）中的免疫反应。与野生型植物相比，C3H14 及其同源物 C3H15 的功能丧失突变导致受感染叶片中对 Pst DC3000 的防御增强和系统获得性抗性（SAR）的发展，而 C3H14 或 C3H15 的过表达则增强了对该病原体的敏感性，并且未能诱导 SAR。C3H14 在 PAMP 触发的免疫（PTI）和 SAR 中的功能依赖于 MPK4 介导的磷酸化。用 Pst DC3000 或鞭毛蛋白 flg22 处理会增强 MPK4 在细胞质中对 C3H14 的磷酸化，从而减轻 C3H14 对 PTI 相关基因表达的抑制作用，并减弱 C3H14 对其靶标 NIM1-INTERACTING1（NIMIN1）和 NIMIN2 的激活表达，NIMIN1 和 NIMIN2 是 SAR 的负调控因子。水杨酸（SA）会影响免疫中 MPK4-C3H14-NIMIN1/2 级联反应，但 C3H14-NIMIN1/2 级联反应介导的 SA 信号转导不依赖于 MPK4 磷酸化。我们的研究表明，C3H14 可能是 MPK4 防御信号通路的负调控因子。
