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 (TIR) can be maintained over at least two stress-free generation and is proportional to the level of disease stress encountered by the parental plants (1-3).
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)methylation machinery (4,5). These analyses have shown that reduced DNA methylation in disease-exposed parent plants is transmitted to their progeny, where it primes salicylic acid-dependent and independent immune responses. While the exact hypomethylated loci that controlling TIR unknown, independent lines of evidence suggest that reduced DNA methylation at transposable elements (TEs) in the (peri)centromeric regions trans-regulates priming of defence genes across the plant’s entire genome (2,5-7).
The discovery of TIR 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 disease resistance (6). However, creating epigenetically altered crop varieties has proven difficult because crop species are typically more sensitive to genome-wide reductions in DNA methylation than Arabidopsis, causing lethality or sterility. Therefore, exploitation of TIR in crop species requires adjustable methods of DNA hypomethylation, which would prevent lethality/sterility by over-stimulation, whilst still ensuring sufficient DNA hypomethylation to induce TIR.
Current studies in our lab are focusing on the mechanisms by which selected hypomethylated DNA loci mediate long-priming of defence genes across the plant genome. In addition, we are developing chemical and molecular-genetic tools that enable introduction of adjustable levels of DNA hypomethylation. These tools will help crop breeders to exploit epigenetic variation, and select for epigenetically primed varieties that require fewer pesticides to control pests and diseases.
1. Luna et al. & Ton (2012) Plant Physiol. 158, 844-853 2. Stassen, Lopez et al. & Ton (2018) Sci Reports 8: 14761. 3. Lopez et al. & Ton (2021) Front Plant Sci DOI: 3389/fpls.2021.644999. 4. Luna E & Ton J (2012) Plant Signal Behav 7, 615-618. 5. Lopez, Stassen et al. & Ton J (2016) Plant J 88: 361-374. 6. Furci L et al. & Ton J (2019) eLife, 8: 40655. 7. Wilkinson et al. & Ton (2019) Ann Rev Phytopathol 57: 505-529.