A nucleoporin-associated signaling cascade controls plant immunity via histone modification

Abstract

Plants undergo massive transcriptional reprogramming upon pathogen infection. The transcription factors SAR DEFICIENT1 (SARD1) and CAM-BINDING PROTEIN 60-LIKE G (CBP60g) are master regulators of this process. However, the regulation of SARD1 and CBP60g transcription remains unclear. We discover a signaling complex centered on the plant-specific nucleoporins CONSTITUTIVE EXPRESSION OF PR GENES 5 (CPR5) and GUANYLATE-BINDING PROTEIN-LIKE GTPASE 3 (GBPL3), which critically regulates SARD1 and CBP60g transcription. We establish that the RNA processing complexes NineTeen Complex (NTC) and CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR (CPSF) act downstream of CPR5 to activate immunity. A genetic screen identifies GBPL3 and key histone modification complex components as suppressors of the autoimmune phenotype in cpr5 mutants, functioning downstream of NTC/CPSF. Transcriptomic and genetic analyses demonstrate that SARD1 and CBP60g are fully responsible for autoimmune activation in cpr5. Crucially, GBPL3 and the histone modifiers physically interact, bind directly to the SARD1 and CBP60g loci, and repress their expression. Pathogen infection substantially reduces this binding. Consistently, the active histone mark H3K4me3 at SARD1 and CBP60g is modulated by the CPR5-NTC/CPSF-GBPL3/histone modifiers cascade and accumulates significantly upon pathogen infection. Our findings reveal a CPR5-NTC/CPSF-GBPL3/histone modifiers signaling cascade that controls the transcription of the SARD1 and CBP60g via histone modification, thereby modulating the transcriptional reprogramming during plant immune responses.