The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis

Abstract

Progeny of heavily diseased plants develop transgenerational acquired resistance (TAR). In Arabidopsis, TAR can be transmitted over one stress-free generation. Although DNA methylation has been implicated in the regulation of TAR, the relationship between TAR and global DNA methylation remains unknown. Here, we characterised the methylome of TAR-expressing Arabidopsis at different generations after disease exposure. Global clustering of cytosine methylation revealed TAR-related patterns in the F3 generation, but not in the F1 generation. The majority of differentially methylated positions (DMPs) occurred at CG context in gene bodies. TAR in F3 progeny after one initial generation of disease, followed by two stress-free generations, was lower than TAR in F3 progeny after three successive generations of disease. This difference in TAR effectiveness was proportional to the intensity of differential methylation at a sub-set of cytosine positions. Comparison of TAR-related DMPs with previously characterised cytosine methylation in mutation accumulation lines revealed that ancestral disease stress preferentially acts on methylation-labile cytosine positions, but also extends to methylation-stable positions. Thus, the TAR-related impact of ancestral disease extends beyond stochastic variation in DNA methylation. Our study has shown that the Arabidopsis epigenome responds globally to disease in previous generations and we discuss its contribution to TAR.

Surviving in a Hostile World: Plant Strategies to Resist Pests and Diseases

“…Since then, various studies have confirmed that DNA methylation is inversely correlated with basal resistance to biotrophic pathogens and responsiveness/expression of SA-dependent genes (81,84,155). Furthermore, independent groups have reported that infection of Arabidopsis with Pseudomonas syringae alters genome-wide DNA methylation (44,106,128).…”

“…Hence, DNA demethylation is essential for the elicitation, transmission, and/or expression of TAR. Another recent study revealed that TAR in Arabidopsis is associated with global shifts in DNA methylation at CG contexts in gene bodies, which were more pronounced after three generations than one generation of disease stress (128). However, the genes carrying these differentially methylated cytosines (DMCs) were not enriched for defense-related functions and there was little overlap in DMCs between independent experiments.…”

“…However, the genes carrying these differentially methylated cytosines (DMCs) were not enriched for defense-related functions and there was little overlap in DMCs between independent experiments. Because the role of gene body methylation in gene expression remains unclear (13), it was concluded that the observed changes in DNA methylation mark TAR but do not necessarily cause TAR (128). Although the exact mechanisms underpinning TAR require further study, there is little doubt about the epigenetic nature of the phenomenon (see the sidebar titled Epigenetics: What's in a Name?).…”

“…Plants can also acquire resistance after the perception of specific environmental stimuli (110). This acquired resistance (AR) is typically long-lasting and can even be transmitted to following generations through changes in DNA methylation and associated chromatin density (81,84,128). As is discussed below, there is increasing evidence that these epigenetic processes can influence genetic mutations and the rate by which new defense genes evolve.…”

Ecological divergence of DNA methylation patterns at distinct spatial scales

“…2007; Jiang et al . 2014; Stassen et al . 2018), climate-CG methylation associations most likely represent solid adaptive signals.…”