Phosphorylation-mediated inactivation of C3H14 by MPK4 enhances bacterial-triggered immunity in Arabidopsis.

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.