Adaptation inception: implanting epigenetic memories of cold stress in cereals

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Changes in the frequency, intensity and duration of weather extremes are consequences of climate change and impose challenges to agroenvironments. Sadly, the limited understanding of plants' adaptive mechanisms to changing environments restrains our ability to prepare for these consequences. Temperate plants persist by adjusting their phenology to low temperatures and are useful systems for adaptation studies. The undomesticated Brachypodium distachyon is a powerful cereal model to study cold adaptation because it naturally grows in environments where freezing spells are frequent, displays a range of vernalization requirements and as our lab first demonstrated, can increase its freezing tolerance capacity upon cold acclimation. Our long-term goal is to understand and manipulate chromatin-based regulatory mechanisms involved in cereal responses to environmental stresses to mitigate their impact on productive development. Recent work implicates chromatin-based mechanisms not only in transcriptional regulation but also in recording specific memories of stresses that can trigger stronger, more rapid cellular responses in previously challenged plants. We thus hypothesize that dynamic tuning of epigenomes is a key regulatory mechanism that primes plant responses to changing environments and supports adaptation. Aims 1 and 2 will characterize chromatin states of cold-acclimated B. distachyon by respectively identifying changes in histone modifications and DNA methylation. These aims will allow a genome-wide appreciation of chromatin marks associated with low temperature fluctuations. Aim 2 will also query the input of B. distachyon's de novo DNA methylation pathway in cold responses. This aim will link the de novo methylation pathway, which is implicated in epigenetic memory formation at stress-induced loci, to the plant's capacity to record and respond to low temperature events. With aim 3, we hope to engineer cereals with enhanced cold tolerance by implanting artificial memories of cold exposure. Here, we propose to engineer the primed chromatin memory states observed in aims 1 and 2 by deploying CRISPR-based tools in B. distachyon. This novel approach will allow plants to be primed for stress without first being exposed to growth-limiting triggers. Importantly, aim 3 will test the feasibility of epigenome editing in crops to enhance stress resilience. Together, the work proposed will provide novel insights on plant chromatin dynamics in response to environmental cues. The use of CRISPR tools to reshape chromatin will galvanize cereal crop improvement and further inform the debate on the use of non-traditional breeding approaches. Our work will thus translate to robust crop production systems, sustainable food security and lower prices. Finally, it will provide HQP capable of creating, assessing and regulating agricultural products derived from epigenetic and editing technologies.