Thermopriming prewires orchestrated regulatory programs to enhance heat stress adaptability

Abstract

- Plants can remember earlier stress exposures (priming), which improves tolerance to later, more severe stress. How this stress memory is organised in crops remains largely unresolved. - We studied five-day-old rice seedlings subjected to severe heat stress with or without thermopriming, combining phenotyping, time-resolved transcriptomic and epigenomic profiling with systems biology approaches and targeted molecular experiments. - Compared with unprimed seedlings, primed seedlings showed a restrained, lower-entropy transcriptional response spanning diverse biological processes. This response was driven by fewer transcription factors that modulate regulons for both stress response and growth, together contributing to better adaptability to severe stress. - Primed seedlings maintained global H3K27me3 levels, which declined in unprimed seedlings, linking retention rather than removal of this mark to the restrained response. - Priming led to the accumulation of memory chaperone transcripts, enabling a rapid rise in protein abundance under severe stress. This supports better post-translational regulation, alongside the coordinated transcriptional response. Overall, thermopriming establishes pre-wired programmes that enhance adaptability through regulatory order and speed, not amplitude, and repressive-mark retention, not removal, during early development. These findings have implications for (i) understanding heat stress memory in addressing climate change driven heat extremes, and (ii) engineering climate-resilient crops.