Cold exposure memory reduces pathogen susceptibility in Arabidopsis based on a functional plastid peroxidase system

Chloroplasts serve as cold priming hubs modulating the transcriptional response of Arabidopsis thaliana to a second cold stimulus for several days by post-cold accumulation of thylakoid ascorbate peroxidases (tAPX). In an attempt to investigate cross-priming effects of cold on plant pathogen protection, we show here that such a single 24 h cold treatment at 4°C decreased the susceptibility of Arabidopsis to virulent Pseudomonas syringae pv. tomato DC3000 (Pst), but did not alter resistance against the avirulent strains Pst avrRPM1 and Pst avrRPS4 or the effector-deficient Pst hrcC- strain. The effect of cold priming against Pst was active immediately after cold exposure and memorized for at least 5 days. The priming benefit was established independent of the immune regulator EDS1 (Enhanced Disease Susceptibility 1) or activation of the immune-related genes NHL10, FRK1, ICS1 and PR1, but required thylakoid-bound as well as stromal ascorbate peroxidase activities as the effect was absent or weak in corresponding knock-out-lines. Suppression of tAPX post-cold regulation in a conditional-inducible tAPX-RNAi line lead to increased bacterial growth numbers. This highlights that the plant immune system benefits from post-cold regeneration of the protective chloroplast peroxidase system.