Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis.

Variation in DNA methylation enables plants to inherit traits independently of changes to DNA sequence. Here, we have screened an Arabidopsis population of epigenetic recombinant inbred lines (epiRILs) for resistance against Hyaloperonospora arabidopsidis (Hpa). These lines share the same genetic background, but show variation in heritable patterns of DNA methylation. We identified four epigenetic quantitative trait loci (epiQTLs) that provide quantitative resistance without reducing plant growth or resistance to other (a)biotic stresses. Phenotypic characterisation and RNA-sequencing analysis revealed that Hpa-resistant epiRILs are primed to activate defence responses at the relatively early stages of infection. Collectively, our results show that hypomethylation at selected pericentromeric regions is sufficient to provide quantitative disease resistance, which is associated with genome-wide priming of defence-related genes. Based on comparisons of global gene expression and DNA methylation between the wild-type and resistant epiRILs, we discuss mechanisms by which the pericentromeric epiQTLs could regulate the defence-related transcriptome.

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

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.