Distinct heat shock factors and chromatin modifications mediate the organ‐autonomous transcriptional memory of heat stress

Summary Plants can be primed by a stress cue to mount a faster or stronger activation of defense mechanisms upon subsequent stress. A crucial component of such stress priming is the modified reactivation of genes upon recurring stress; however, the underlying mechanisms of this are poorly understood. Here, we report that dozens of Arabidopsis thaliana genes display transcriptional memory, i.e. stronger upregulation after a recurring heat stress, that lasts for at least 3 days. We define a set of transcription factors involved in this memory response and show that the transcriptional memory results in enhanced transcriptional activation within minutes of the onset of a heat stress cue. Further, we show that the transcriptional memory is active in all tissues. It may last for up to a week, and is associated during this time with histone H3 lysine 4 hypermethylation. This transcriptional memory is cis‐encoded, as we identify a promoter fragment that confers memory onto a heterologous gene. In summary, heat‐induced transcriptional memory is a widespread and sustained response, and our study provides a framework for future mechanistic studies of somatic stress memory in higher plants. Significance Statement Heat priming activates an organ‐autonomous transcriptional memory that is controlled by the HSFA1 and HSFA2 transcription factors, resulting in sustained chromatin modification that lasts significantly longer than previously described.