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 postcold 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 but did not alter resistance against the avirulent P. syringae pv. tomato avRPM1 and P. syringae pv. tomato avrRPS4 strains or the effector-deficient P. syringae pv. tomato strain hrcC. The effect of cold priming against P. syringae pv. tomato was active immediately after cold exposure and memorized for at least 5 days. The priming benefit was established independent of the immune regulator Enhanced Disease Susceptibility 1 (EDS1) or activation of the immune-related genes NHL10, FRK1, ICS1 and PR1 but required thylakoid-bound as well as stromal ascorbate peroxidase activities because the effect was absent or weak in corresponding knock-out-lines. Suppression of tAPX postcold regulation in a conditional-inducible tAPX-RNAi line led to increased bacterial growth numbers. This highlights that the plant immune system benefits from postcold regeneration of the protective chloroplast peroxidase system.[Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.