From recall to reset: the role of DNA (de)methylation in modulating plant immune memory
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Epigenetic reprogramming is increasingly recognised as a driver of plant immune memory, yet its molecular basis remains poorly understood. Using a chemically inducible transgene in Arabidopsis, we transiently activated the DNA demethylase REPRESSOR OF SILENCING 1 (ROS1), inducing immune memory against (hemi-)biotrophic pathogens that persisted for one to two weeks. This immune memory was characterised by reduced DNA methylation and small RNAs (sRNAs) in gene-rich chromosome arms, revealing previously uncharacterised ROS1 targets that regulate salicylic acid-dependent immunity and DNA damage responses. In contrast, (peri)centromeres had an unexpected increase in non-CG DNA methylation and sRNA abundance, indicating rapid compensatory RNA-directed DNA (re)methylation in these regions. Pharmacological inhibition of this (re)methylation response with 5-Azacytidine enhanced both the strength and durability of ROS1-induced resistance. Together, our findings reveal a novel interplay between active DNA demethylation in the chromosome arms and compensatory (re)methylation of (peri)centromeres that shapes the strength and persistence of plant immune memory.
