Modulation of RNA Polymerase II Phosphorylation Downstream of Pathogen Perception Orchestrates Plant Immunity

Perception of microbe-associated molecular patterns (MAMPs) elicits host transcriptional reprogramming as part of the immune response. Although pathogen perception is well studied, the signaling networks orchestrating immune gene expression remain less clear. In a genetic screen for components involved in the early immune gene transcription reprogramming, we identified Arabidopsis RNA polymerase II C-terminal domain (CTD) phosphatase-like 3 (CPL3) as a negative regulator of immune gene expression. MAMP perception induced rapid and transient cyclin-dependent kinase C (CDKC)-mediated phosphorylation of Arabidopsis CTD. The CDKCs, which are in turn phosphorylated and activated by a canonical MAP kinase (MAPK) cascade, represent a point of signaling convergence downstream of multiple immune receptors. CPL3 directly dephosphorylated CTD to counteract MAPK-mediated CDKC regulation. Thus, modulation of the phosphorylation dynamics of eukaryotic RNA polymerase II transcription machinery by MAPKs, CTD kinases, and phosphatases constitutes an essential mechanism for rapid orchestration of host immune gene expression and defense upon pathogen attacks. [Display omitted] •RNA polymerase II CTD phosphatase (CPL3) mutants show enhanced immune gene activation•MAMPs induce cyclin-dependent kinases CDKCs and RNA pol II CTD phosphorylation•Direct CDKC phosphorylation by MAP kinase (MAPK) activates immune gene expression•CPL3 counteracts MAPK-CDKC regulation via RNA pol II CTD dephosphorylation Mechanisms underlying the transcriptional reprogramming of immune genes upon pathogen perception are unclear. Li et al. find that MAP kinases downstream of multiple immune sensors in plants directly phosphorylate RNA polymerase II C-terminal domain (CTD) kinases to activate gene expression. This is counterregulated by CPL3 phosphatase to fine-tune immune gene expression.