Paternal CHH methylation potentiates stress responses against Pseudomonas syringae in Arabidopsis progenies

Systemic acquired resistance (SAR) is an induced immune mechanism in plants, involving epigenetic regulation by chromatin remodeling and DNA methylation, which can be inherited to progeny following stress exposure. Intersexual epigenetic conflict sometimes leads to unequal expression of maternal and paternal alleles in offspring, resulting in parent-of-origin effects of inheritance. To better understand the parental contributions of epialleles in plant defense, isogenic Arabidopsis parental lines were mock-treated (M) and Pseudomonas syringae (Pst)-treated (P) for reciprocal crosses to produce F1 progenies (MP, PM). Together with their self-fertilized F1 descendants (MM, PP), the genome-wide inherited DNA methylation and transcriptomic changes against Pst were analyzed. F1 descendants shared widespread DNA methylation and transcriptional changes at transposable elements (TEs) and genes. The confrontation of epigenomes triggers the reprogramming of DNA methylation in reciprocal crosses, resulting in transgressive segregation that also shows the parental effect of Pst treatment. Compared to PM, the MP (Pst-primed paternal genome) was found to contributes to CHH hypermethylation, which is associated with processes in plant-pathogen interaction, including carbohydrate metabolism, glutathione metabolism and stronger translation process, which potentially contribute to improved disease resistance in MP in response to Pst challenge. Our data suggested a parent-of-origin effect of defense priming that contributes differently toward improved defense response in progenies.