Abstract

Disease resistance often comes with a penalty in growth and yield. The microRNA miR156 and its target, the transcription factor gene IDEAL PLANT ARCHITECTURE 1 ( IPA1 ), regulate developmental processes such as tillering and panicle branching while enhancing disease resistance and abiotic stress tolerance in rice ( Oryza sativa ). However, how this transcription factor regulates multiple processes remains unclear. Here, we found that IPA1 physically interacts with NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (OsNPR1) in the nucleus. Under normal conditions, the OsNPR1 expression levels are low, and OsCULLIN3a (OsCUL3a), an E3 ligase responsible for OsNPR1 degradation, keeps the abundance of monomeric OsNPR1 low in the nucleus and prevents IPA1 from transcriptionally regulating defense genes. When the plant is attacked by pathogens, OsNPR1 oligomers dissociate into monomers, which translocate into the nucleus and physically interact with IPA1, facilitating its binding to promoters of downstream genes, thereby activating positive defense regulators and repressing negative defense regulators. Simultaneously, IPA1 abundance increases, and IPA1 interacts with OsNPR1 and OsCUL3a, interfering with the OsCUL3a–OsNPR1 interaction, dampening the ubiquitin-mediated degradation of OsNPR1. The stabilization of OsNPR1 by IPA1 further enhances IPA1 transcriptional activity in disease resistance. Our work demonstrates that OsNPR1 facilitates IPA1 binding to the promoters of genes related to disease resistance and that IPA1 inhibits OsCUL3a-mediated degradation of OsNPR1. The physical interaction between IPA1 and OsNPR1in the nucleus both enhances the transcriptional activity of IPA1 in rice immunity and stabilizes OsNPR1 via preventing it from OsCUL3a-mediated degradation.