SummaryDNA methylation is antagonistically controlled by DNA methyltransferases and DNA demethylases. The level of DNA methylation controls plant gene expression on a global level. We have examined impacts of global changes in DNA methylation on the Arabidopsis immune system. A range of hypo‐methylated mutants displayed enhanced resistance to the biotrophic pathogen Hyaloperonospora arabidopsidis (Hpa), whereas two hyper‐methylated mutants were more susceptible to this pathogen. Subsequent characterization of the hypo‐methylated nrpe1 mutant, which is impaired in RNA‐directed DNA methylation, and the hyper‐methylated ros1 mutant, which is affected in DNA demethylation, revealed that their opposite resistance phenotypes are associated with changes in cell wall defence and salicylic acid (SA)‐dependent gene expression. Against infection by the necrotrophic pathogen Plectosphaerella cucumerina, nrpe1 showed enhanced susceptibility, which was associated with repressed sensitivity of jasmonic acid (JA)‐inducible gene expression. Conversely, ros1 displayed enhanced resistance to necrotrophic pathogens, which was not associated with increased responsiveness of JA‐inducible gene expression. Although nrpe1 and ros1 were unaffected in systemic acquired resistance to Hpa, they failed to develop transgenerational acquired resistance against this pathogen. Global transcriptome analysis of nrpe1 and ros1 at multiple time‐points after Hpa infection revealed that 49% of the pathogenesis‐related transcriptome is influenced by NRPE1‐ and ROS1‐controlled DNA methylation. Of the 166 defence‐related genes displaying augmented induction in nrpe1 and repressed induction in ros1, only 25 genes were associated with a nearby transposable element and NRPE1‐ and/or ROS1‐controlled DNA methylation. Accordingly, we propose that the majority of NRPE1‐ and ROS1‐dependent defence genes are regulated in trans by DNA methylation.

As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.

Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance traits to their progeny. However, the evolutionary and ecological significance of transgenerational induced resistance (t-IR) is poorly understood because a clear understanding of how parents interpret environmental cues in relation to the effectiveness, stability, and anticipated ecological costs of t-IR is lacking. Here, we have used a full factorial design to study the specificity, costs, and transgenerational stability of t-IR following exposure of Arabidopsis thaliana to increasing stress intensities by a biotrophic pathogen, a necrotrophic pathogen, and salinity. We show that t-IR in response to infection by biotrophic or necrotrophic pathogens is effective against pathogens of the same lifestyle. This pathogen-mediated t-IR is associated with ecological costs, since progeny from biotroph-infected parents were more susceptible to both necrotrophic pathogens and salt stress, whereas progeny from necrotroph-infected parents were more susceptible to biotrophic pathogens. Hence, pathogen-mediated t-IR provides benefits when parents and progeny are in matched environments but is associated with costs that become apparent in mismatched environments. By contrast, soil salinity failed to mediate t-IR against salt stress in matched environments but caused non-specific t-IR against both biotrophic and necrotrophic pathogens in mismatched environments. However, the ecological relevance of this non-specific t-IR response remains questionable as its induction was offset by major reproductive costs arising from dramatically reduced seed production and viability. Finally, we show that the costs and transgenerational stability of pathogen-mediated t-IR are proportional to disease pressure experienced by the parents, suggesting that plants use disease severity as an environmental proxy to adjust investment in t-IR.