A molecular framework for the epigenetic control of pathogen response and memory in plants

Context The challenge of climate change coupled with a growing global population demands that farmers do more with less; agricultural outputs must double by 2050 to mitigate growing food insecurity. Plant diseases account for almost 40% of all crop losses annually, yet we still do not fully understand how plants perceive and respond to pathogens. Plants possess a form of native immunity called Pattern Triggered Immunity (PTI). Activation of this immunity promotes survival against pathogens in the short term, but interestingly also in the long term. Furthermore, PTI can be enhanced (i.e. "primed"), through mechanisms that remain unclear. The challenge this project addresses Emerging evidence shows that plants integrate lasting adaptive responses (i.e. memory) to their environment by altering the accessibility of their DNA, in a process called chromatin remodelling. The extent to which chromatin remodelling integrates a memory of PTI is largely unknown. This proposal will fill this knowledge gap by describing a novel chromatin-based mechanism that primes PTI by allowing plants to ‘remember’ previous infections. Aims and objectives In previous work I showed that a plant chromatin remodelling complex, known as the Polycomb Repressive Complex 2 (PRC2), regulates growth and flooding stress tolerance in the model species Arabidopsis thaliana. I showed that a plant-specific subunit of this complex (called VRN2) directly senses and transduces environmental stimuli to facilitate stress adaptation and survival. In unpublished work I have now shown that the PRC2 also senses pathogens - my preliminary data has revealed that VRN2 is stabilised when PTI is activated and also influences pathogen-associated gene expression. I propose that the VRN2 sensor subunit acts as a previously unknown link between the perception of pathogens and the induction of immediate and long-term survival responses. Using a range of physiological, molecular, and omics-based workflows that I have established, I aim to define VRN2 as a novel pathogen sensor and evaluate the impact of the PRC2 on plant immunity and priming responses. I will achieve this by addressing three objectives: Objective 1: Show that diverse biotic factors influence the stability and makeup of PRC2, and assess how it contributes to defence responses. Objective 2: Use genome-wide sequencing to understand how PTI-triggered stabilisation of VRN2 influences chromatin structure and gene expression. Objective 3: Examine how PRC2 imprints a memory of biotic stress that primes future immune responses and investigate its potential as a point of crosstalk between biotic and abiotic stress responses. Potential applications and benefits This work will reveal a novel mechanism that allows plants to sustain long-term resistance to disease by remembering previous pathogen encounters. Our crops face a barrage of biotic and abiotic stresses that restrict their fitness and yield. Climate change will drive the frequency and intensity of these stresses to greater extremes. Enhancing our knowledge of plant immunity will help to alleviate this by facilitating the development of more resilient crops and providing new disease management strategies. My work is poised to answer fundamental questions about how plants sense and remember interactions with pathogens. This will have broad implications on how we think about crop species, which constantly interact with microbes in the soil and air. This knowledge will inform agricultural policy writing and breeding strategies. Ultimately, this work has the potential to provide new targets for mitigating crop losses, benefiting both society and the economy.