Light-induced phyB-NPR1 interaction activates systemic acquired resistance

Light perception by phytochromes controls different aspects of plant-environment interactions including plant immunity; however, the underpinning molecular mechanisms are less well-understood. Upon localized attack on leaves by avirulent pathogens, the systemic accumulation of salicylic acid (SA) is required for the establishment of systemic acquired resistance (SAR) throughout the plant to curtail pathogen spread. We demonstrate that light-mediated Small Ubiquitin-like Modifier 1 (SUMO) conjugation to phytochrome B (phyB) is critical for increasing cellular SA levels to orchestrate SAR upon avirulent bacterial infection. SA promotes SUMOylation of phyB, which enables it to interact with the SA receptor, Nonexpressor of Pathogenesis-Related 1 (NPR1) via its SUMO1-interacting motif. SUMOylation of phyB is enhanced by the accumulation of SUMO-Conjugating Enzyme (E2) (SCE1) and the degradation of SUMO protease Overly Tolerant to Salt 1 (OTS1) in SAR-induced systemic tissues. Using confocal imaging, we show that SUMOylated phyB undergoes liquid-liquid phase separation together with NPR1 in nuclear bodies. We further validated through immunoprecipitation, ChIP and RNA-seq analysis that SUMOylated phyB associates with NPR1 and TGA transcription factors in nuclear photobodies to induce the expression of PR1 gene. We reveal a post-translational modification mechanism in which light-induced SUMOylation of photoreceptors promotes SAR by regulating NPR1 function.