Long-lasting memory of jasmonic acid-dependent immunity requires DNA demethylation and ARGONAUTE1

Abstract

Stress exposure can have long-lasting impacts on ecologically relevant life-history traits in plants. Here, we have investigated the long-term impacts of the stress hormone jasmonic acid (JA) on the defence phenotype, transcriptome and DNA methylome of Arabidopsis thaliana. Three weeks after transient JA signalling activity in seedlings, 5-week-old plants retained induced resistance (IR) against herbivory but showed enhanced susceptibility to necrotrophic and biotrophic pathogens. Transcriptome analysis revealed that JA seedling treatment causes prolonged priming and/or up-regulation of JA-dependent defence genes but repression of ethylene- and salicylic acid-dependent genes. Long-term JA-IR against herbivory was dependent on MYC2/3/4 transcription factors and DNA (de)methylation pathways. Although DNA methylome analysis did not reveal consistent changes in DNA methylation near MYC2/3/4-controlled defence genes, plants from JA-treated seedlings showed enrichment of differentially methylated regions at ATREP2 transposable elements (TEs). Our study points to a trans-acting mechanism whereby hypomethylated TEs mediate long-lasting epigenetic memory of JA-dependent immunity.

Editorial: Induced resistance and priming against pests and pathogens

“…Catoni et al (2022) found in tomato a reduction in cytosine methylation in gene promoters and DNA transposons of tomato plants primed for pathogen resistance by treatment with b-aminobutyric acid (BABA). Similarly, Wilkinson et al (2022) reported in Arabidopsis that longlasting JA-IR against herbivore feeding was associated with reduced cytosine methylation at AtREP2 transposons. However, in both cases, the majority of priming-related changes in DNA methylation did not occur in the proximity of primed genes, suggesting that methylation may affect priming via trans-acting mechanisms.…”

“…(2022) found in tomato a reduction in cytosine methylation in gene promoters and DNA transposons of tomato plants primed for pathogen resistance by treatment with β-aminobutyric acid (BABA). Similarly, Wilkinson et al. (2022) reported in Arabidopsis that long-lasting JA-IR against herbivore feeding was associated with reduced cytosine methylation at AtREP2 transposons.…”