Cold priming memory reduces plant pathogen susceptibility based on a functional plastid peroxidase system

Chloroplasts, as recently shown, serve as cold priming hubs in modulating the transcriptional response of Arabidopsis thaliana to a second cold stimulus after a stress-free interphase of several days. Here, we studied if such a single 24 h cold stress at 4 {degrees}C also alters the susceptibility of Arabidopsis to virulent Pseudomonas syringae pv. tomato DC3000. Our data show that cold priming did not only increase resistance of Arabidopsis to a subsequent infection immediately, but also after a memory phase of 5 days, during which thylakoid ascorbate peroxidases accumulate. Contrasting to susceptibility, the prior cold exposure did not alter resistance against avirulent and effector-triggered immunity-inducing Pseudomonas syringae strains. The effect of cold priming on the plant pathogen susceptibility was independent of the central nucleo-cytoplasmic immune regulator EDS1 (Enhanced Disease Susceptibility 1) and uncoupled from classical immune gene activation. The priming benefits against pathogens required thylakoid and stromal ascorbate peroxidase activity. Combinatorial priming of Arabidopsis pathogen susceptibility by metastable regulation of stromal ascorbate peroxidase activity and post-cold expression of thylakoid ascorbate peroxidase guarantees immediate protection without latency time and prolonged protection by the memory element that regulates future cold responses. One-sentence summary24 hour cold exposure reduces plant susceptibility against virulent pathogens dependent on chloroplast ascorbate peroxidases.