CAREER: Dissecting the Environmentally Responsive Plant Epigenome

The Climate Crisis is not only predicted to coincide with more severe episodes of abiotic stress, but it is also predicted to shift the range of crop suitability as well as the geographic range of numerous plant pathogens. As a result, there is an urgent need for the development of more stress-resilient crop plants through breeding to safeguard our future food security. A critical component of plant stress defense pathways is the epigenome which is a critical regulatory layer of various structural features that control the interpretation of the genetic information in an environmental cue-dependent manner. The architects responsible for shaping the dynamic plant epigenome are DNA-binding proteins, commonly known as transcription factors. They act as pivotal recruitment platforms for protein complexes capable of altering the structure of the epigenome. This project will use a newly developed high-throughput epigenome profiling platform to investigate the role of the master MYC-type helix-loop-helix transcription factor MYC2 in shaping the environmentally-responsive epigenome. Since MYC2 controls a major branch of the plant defense network, it is anticipated that a better understanding of its function will provide significant new insight with the potential to advance the development of resilient crops for U.S. agriculture. The newly developed platform will be made available to other researchers in the field thereby broadly impacting plant science research. Equally important to improve breeding efforts is training the next generation of scientists and introducing them to genomics-enabled research. This opportunity will be facilitated through the Epigenome Explorer course, where students can dive into the study of dynamic plant epigenomes and uncover thrilling new information. Harnessing the regulatory capabilities of master transcription factors to engineer plants with enhanced stress resilience holds great promise mitigating the negative impact of the current climate crisis. Plant immune responses against herbivorous insects and fungi are controlled by the jasmonic acid (JA) pathway with MYC2 as its master regulator. Perception of the defense hormone JA directly controls the composition and consequently the functional output of the MYC2-centric JA-responsive epigenome which comprises MYC2, various transcriptional co-activators/repressors, and chromatin regulators. Despite its significant regulatory importance, the dynamic nature and the functional repertoire of this regulatory module remains poorly understood. The goal of this project will shed light on how MYC2 establishes the JA-responsive epigenome in the model plant Arabidopsis thaliana. By utilizing the newly developed PHILO (Plant HIgh-throughput LOw input) ChIP-seq platform, the MYC2-centric JA-responsive epigenome will be comprehensively investigated with an emphasis on JA-induced enhancer regions. CRISPR/Cas9-facilated cis-regulatory variation will also be utilized to reveal general principles of the MYC2 module during active JA signaling. Moreover, by perturbing the JA-responsive epigenome with elevated temperature, an unexplored but immensely important crosstalk between a plant immune pathway and the thermomorphogenesis pathway will be studied. Taken together, the knowledge gained on how the JA-responsive epigenome is established and how it can be manipulated will pave the way for the creation of new plant varieties to enhance plant resilience to stresses. All project outcomes will be made available to the broader research community through deposition at long-term public data and germplasm repositories. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.