After defence priming has been established, the resistance can be maintained throughout the life cycle of the plant. Since epigenetic mechanisms, such as chromatin modifications and DNA hypomethylation, can cause long-lasting adjustments in the sensitivity of defence genes, we investigated the possibility that maintenance of defence priming is under epigenetic control. We discovered that progeny from severely diseased Arabidopsis plants are primed to express defence genes (1). Isogenic Arabidopsis plants were exposed to fitness-reducing levels of bacterial speck disease by P. syringae, upon which their progenies were collected and tested for disease resistance. Compared to progeny from mock-inoculated plants, progeny from diseased plants were more resistant to (hemi-)biotrophic pathogens, such as downy mildew. This transgenerational acquired resistance (TAR) can be maintained over at least two stress-free generation and is proportional to the level of disease stress encountered by the parental plants (1,2).
To examine the mechanisms by which trans-generational priming is transmitted to following generations, we carried out further experiments with Arabidopsis mutants in DNA (de)methyation machinery (3,4). These analyses have suggested that reduced DNA methylation in disease-exposed parent plants is transmitted to their progeny, where it primes salicylic acid-dependent immune responses. While the exact TAR-regulatory sequences that become targeted for DNA de-methylation remain unknown, independent lines of evidence are suggest that reduced DNA methylation at transposable elements (TEs) in the (peri)centromeric regions trans-regulate priming of defence genes across the plant’s genome (2,4,5).
The discovery of TAR and epigenetic inheritance of defence priming not only changes the conventional view on how plant communities adapt to long-lasting biotic stress, it also provides new opportunities for novel strategies of crop crop protection and breeding. Particularly, our recent study of epigenetic recombinant inbred lines (epiRILs) of Arabidopsis has provided more evidence that reduced DNA methylation at selected loci in the (peri)centromeric regions can yield high levels of heritable quantitative resistance (5).
Current studies in our lab are focusing on the mechanisms by which selected pericentromeric regions control heritable defence gene priming across the genome, as well as the ecological and evolutionary drivers of TAR. In addition, we are developing chemical and genetic tools that enable introduction of adjustable levels of hypo-methylation at the (pericentromeric) regions of tomato. These tools will help crop breeders to exploit epigenetic variation, and select for epigenetically primed varieties that require fewer chemicals for disease control.
1. Luna E et al. & Ton J (2012) Plant Physiol. 158, 844-853 2. Stassen J et al. & Ton J. (2018) Sci Reports 8: 14761. 3. Luna E & Ton J (2012) Plant Signal Behav 7, 615-618. 4. Lopez A, Stassen J, et al. & Ton J (2016) Plant J 88: 361-374. 5.Furci L et al. & Ton J (2019) eLife, in press.