Postdoctoral Research Associate University of Sheffield Sheffield, England, United Kingdom
Environmental stimuli such as non-lethal pathogen infection and specific plant-derived metabolites, can induce an enhanced defence capacity against future biotic stress. This induced resistance (IR) is typically based on a form of stress memory that primes the plant’s immune system. Stress memory can be maintained throughout a plant’s life and, in some cases, be transmitted to following generations. We have explored the role of DNA methylation as the internal ‘hard drive’ of plant stress memory. To investigate the mechanisms driving within-generation maintenance of IR, we treated Arabidopsis seedlings with the hormone jasmonate (JA) and investigated their IR phenotypes three weeks later. While plants from JA-treated seedlings showed increased susceptibility to pathogens, they maintained high levels of IR against herbivory. Using mRNA-seq and mutant analyses, we identified a cluster of JA-inducible defence genes displaying prolonged upregulation and/or a priming to respond faster and stronger to secondary stress. Based on JA-IR phenotypes of mutants in DNA methylation homeostasis, genome-wide methylome analysis of long-term JA-IR, and publicly available sRNA-seq data, we propose a model for stress memory. Transient JA stress in seedlings induces long-lasting DNA hypomethylation of one transposon family, AtREP2, which controls long-term JA-IR and the associated priming/up-regulation of JA-dependent defence genes via small RNAs and the protein ARGONAUTE1. DNA hypomethylation has also been linked to the maintenance of IR across generations. However, progress on deciphering the molecular-genetic mechanisms underpinning this epigenetic plant response is confounded by the relatively high variability of heritable IR. To overcome this obstacle, we have developed an estradiol-inducible transformation vector that allows for dose- and tissue-dependent induction of the DNA demethylase gene ROS1. Importantly, this tool has applications beyond research. Epigenetic variation can be introduced into the germline of crops and beneficial epigenetic traits can be selected, including stress memory and increased resistance to biotic stress.