Transcriptional memories mediate the plasticity of cold stress responses to enable morphological acclimation in...

Plants that successfully acclimate to stress can resume growth under stressful conditions. The grass Brachypodium distachyon can grow a cold-adaptive morphology during cold acclimation. Studies on transcriptional memory (TM) have revealed that plants can be primed for stress by adjusting their transcriptional responses, but the function of TM in stress acclimation is not well understood. We investigated the function of TM during cold acclimation in B. distachyon. Quantitative polymerase chain reaction (qPCR), RNA-seq and chromatin immunoprecipitation qPCR analyses were performed on plants exposed to repeated episodes of cold to characterize the presence and stability of TM during the stress and growth responses of cold acclimation. Transcriptional memory mainly dampened stress responses as growth resumed and as B. distachyon became habituated to cold stress. Although permanent on vernalization gene VRN1, TMs were short-term and reversible on cold-stress genes. Growing under cold conditions also coincided with the acquisition of new and targeted cold-induced transcriptional responses. Overall, TM provided plasticity to cold stress responses during cold acclimation in B. distachyon, leading to stress habituation, acquired stress responses, and resumed growth. Our study shows that chromatin-associated TMs are involved in tuning plant responses to environmental change and, as such, regulate both stress and developmental components that characterize cold-climate adaptation in B. distachyon.