Perturbation of Spermine Homoeostasis Uncouples Hypersensitive Cell Death From Systemic Plant Immunity

Polyamines are key regulators of plant stress responses, yet their contribution to coordinating local immune responses with systemic immunity remains poorly understood. Here, we investigated how spermine (Spm) homeostasis influences local and systemic defence responses in Arabidopsis thaliana following inoculation with Pseudomonas syringae pv. tomato DC3000 expressing AvrRpm1 (Pst AvrRpm1), which elicits both pattern- and effector-triggered immune responses. Pst AvrRpm1 reconfigured polyamine metabolism, notably inducing SPERMINE SYNTHASE (SPMS) and POLYAMINE OXIDASE 4 (PAO4) expression and promoting a metabolic shift toward Spm biosynthesis and oxidation. Loss of Spm biosynthesis in the spms mutant enhanced reactive oxygen species (ROS) accumulation, lipid peroxidation and hypersensitive cell death following Pst AvrRpm1 inoculation, but reduced systemic resistance and altered the resistance-inducing activity and metabolite composition of petiole exudates, including lower relative abundance of salicylic acid and pipecolic acid. Likewise, pao4 mutants showed altered systemic resistance and petiole-exudate composition, consistent with a contribution of Spm oxidation to defence-associated metabolic outputs. In addition, exogenous Spm elicited dose-dependent local cell death and enhanced systemic resistance, both partly dependent on PAO4, and triggered coordinated transcriptional reprogramming of defence-, redox- and hormone-associated pathways. Together, our findings support a model in which balanced Spm biosynthesis and PAO4-dependent oxidation contribute to a productive redox window that supports controlled local cell death, defence-gene activation, SAR-associated metabolic outputs and systemic immunity. These results highlight the importance of Spm homeostasis in plant immunity.