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

Abstract

Stress can alter important plant life-history traits. Here, we report the long-term effects of the stress hormone jasmonic acid (JA) on the defence phenotype, transcriptome and DNAmethylome of Arabidopsis. Three weeks after transient JA signalling activity, 5-week-old plants retained induced resistance (IR) against herbivory but showed enhanced susceptibility to necrotrophic and biotrophic pathogens. Transcriptome analysis of these plants revealed priming and/or up-regulation of JA-dependent defence genes but repression of ethyleneand salicylic acid-dependent genes. Long-term JA-IR against herbivory was associated with shifts in glucosinolate composition and required MYC2/3/4 transcription factors, DNA (de)methylation pathways and the small RNA (sRNA)-binding protein ARGONOUTE1 (AGO1). Although methylome analysis did not reveal consistent changes in DNA methylation near MYC2/3/4-controlled genes, JA-treated plants were specifically enriched with hypomethylated ATREP2 transposable elements (TEs), while ATREP2-derived sRNAs showed increased association with AGO1. Our results indicate that AGO1-associated sRNAs from hypomethylated ATREP2 TEs trans-regulate long-lasting memory of JAdependent immunity.

Basic helix-loop-helix (bHLH) gene family in rye (Secale cereale L.): genome-wide identification, phylogeny, evolutionary expansion and expression analyses

“…ScbHLH5 , member of subfamily 7, displayed remarkable responses at the roots in multiple abiotic stresses. Within the subfamily 8, ZBF1 ( At1g32640 ) encodes an MYC-bHLH-related transcriptional activator that plays a vital role in drought stress and ABA response [ 77 , 78 ]. Similarly, the expression of ScbHLH11 was significantly upregulated in almost all abiotic stresses, which may enhance the adaptability of rye to the environment in a similar manner.…”

Role of Epigenetic Factors in Response to Stress and Establishment of Somatic Memory of Stress Exposure in Plants

“…RdDM components were implicated in the regulation of long-lasting memory of the immunity to herbivory; Arabidopsis plants exposed to JA were more resistant to insect grazing and were more sensitive to pathogens [143]. This effect required MYC2/3/4 transcription factors and RdDM activity, as well as the DNA demethylase ROS1 and the small RNA (sRNA)-binding protein AGO1.…”

“…RdDM and ROS1 activated the ATREP2 transposable element, producing 21 nt sRNAs that are associated with AGO1. The authors hypothesized that since ATREP2 TEs are enriched with sequences from induced resistancerelated defence genes, sRNAs derived from these transposons establish or maintain JAinduced herbivore immunity [143].…”

Heritable induced resistance in Arabidopsis thaliana: Tips and tools to improve effect size and reproducibility

“…Only decades later, researchers began to examine the long‐term maintenance of IR. In Arabidopsis thaliana , Luna et al ( 2014 ) showed that priming of SA‐inducible defense genes and IR against biotrophic pathogens persists for 4 weeks after seedling treatment with BABA (Luna et al, 2014 ), while Wilkinson et al ( 2023 ) reported that priming of jasmonic acid (JA)‐dependent defense genes and IR against herbivory is still present 3 weeks after transient JA stress (Wilkinson et al, 2023 ). Both studies also revealed regulatory functions of histone modifications and DNA methylation, supporting a growing body of evidence for epigenetic regulation of IR (Hannan Parker et al, 2022 ).…”