Deciphering plant stress memory: the exploration of how DNA methylation and the rhizosphere microbiome control stress memory in plants

Plant pests and pathogens pose a major threat to the global food supply. Pesticides are currently the primary control strategy however there is clear evidence that they can negatively impact the health of humans and the wider environment. To ensure a sustainable future for our food supply, agriculture must abandon its reliance on harmful chemical pesticides. Enhancing the plant's natural ability to resist pests such as caterpillars will help achieve this goal. In this fellowship I will decipher the mechanisms underpinning one aspect of the plants immune system which has great potential for exploitation. Following exposure to specific environmental stimuli such as mild pest damage, plants become more resistant to future attack. This phenomenon is known as acquired or induced resistance and is type of stress memory. The formation of stress memory involves changes in a plant's epigenome, the collection of chemical modifications which regulate the plants genome. In a recent publication I identified that a reduction in one specific modification, DNA methylation, at specific genomic regions is essential for long-lasting stress memory and resistance against chewing herbivores. The removal of DNA methylation, DNA demethylation, has also been shown to influence the plant root associated microbiome by controlling the production of root exudates and in turn the recruitment of beneficial microbes. These recent findings raise a major unanswered question, is stress memory in plants underpinned by the combination of DNA methylation and microbiomes? More specifically, does stress induced loss of DNA methylation regulate the recruitment of a beneficial microbiome to plant roots and does this facilitate stress memory and long-lasting resistance? In this fellowship I will investigate these timely questions and generate transformative new insights about the mechanisms of plant stress adaptation. The research programme for the fellowship will be split into four objectives addressed using the important crop species tomato (Solanum lycopersicum; Objectives 1-3) and the model plant Arabidopsis thaliana (Objective 4). Objective 1, investigate the requirement of a functional soil microbiome for plants to express long-lasting induced resistance after herbivory stress or removal of DNA methylation using an inducible DNA demethylation system. Objective 2, characterise the herbivory stress induced shift in the root transcriptome associated with stress memory and determine whether this results in a long-lasting change in root exudation and recruitment of a beneficial microbiome. Objective 3, demonstrate that herbivory stress induces a loss of DNA methylation and establish if this regulates root exudate metabolism. Objective 4, expand the research to ascertain whether the requirement of DNA methylation dependent changes in the root associated microbiome for long-lasting stress memory is plant species specific. The knowledge gained from this fellowship will inform the breeding of novel crop varieties which display enhanced resistance to pests without the requirement to be exposed to stress. It will also direct the development of new soil management strategies which promote pest-resistance inducing microbes. Together these novel pest control strategies will help ensure sustainable production of our food which will benefit farmers, consumers, and the wider environment.