Histone retention preserves epigenetic marks during heat stress‐induced transcriptional memory in plants

Abstract

Plants often experience recurrent stressful events, for example, during heat waves. They can be primed by heat stress (HS) to improve the survival of more severe heat stress conditions. At certain genes, sustained expression is induced for several days beyond the initial heat stress. This transcriptional memory is associated with hyper‐methylation of histone H3 lysine 4 (H3K4me3), but it is unclear how this is maintained for extended periods. Here, we determined histone turnover by measuring the chromatin association of HS‐induced histone H3.3. Genome‐wide histone turnover was not homogenous; in particular, H3.3 was retained longer at heat stress memory genes compared to HS‐induced non‐memory genes during the memory phase. While low nucleosome turnover retained H3K4 methylation, methylation loss did not affect turnover, suggesting that low nucleosome turnover sustains H3K4 methylation, but not vice versa. Together, our results unveil the modulation of histone turnover as a mechanism to retain environmentally mediated epigenetic modifications. image Heat stress memory in plants is associated with transcriptional memory and histone H3 lysine 4 hyper‐methylation. Here, reduced histone turnover at these genes is found to contribute to maintaining epigenetic memory. Histone turnover at individual loci was determined by measuring incorporation and retention of an inducible tagged H3.3. Heat stress memory genes show lower histone turnover compared to early HS genes. Histone retention/recycling promotes environmentally mediated epigenetic memory.