Autumn–winter progression triggers distinct transcriptional programs in Arabidopsis thaliana

Background Temperate plants are adapted to survive winter chilling temperatures. However, the global regulatory landscape underlying acclimation to noisy and fluctuating natural cold conditions remains poorly investigated. Results We explore the transcriptome dynamics of Arabidopsis thaliana plants grown over weeks of a gradually decreasing temperature regime, mimicking natural cold conditions of autumn and early winter, including daily temperature fluctuations. Our results define two distinct genetic programs responding to either moderate cold ( COOLING genes) or to temperatures below 10 °C ( CHILLING genes). Transient induction of C-REPEAT/DEHYDRATION-RESPONSIVE ELEMENT BINDING FACTORS ( CBFs ) lies in the boundary between COOLING and CHILLING activation, while the core circadian clock component CIRCADIAN CLOCK-ASSOCIATED 1 ( CCA1 ) is essential for transcriptional responses both at moderate cold and chilling conditions. By profiling genome-wide chromatin accessibility, we demonstrate that the induction of cold-responsive genes is associated with an increase in promoter accessibility. In contrast, down-regulated genes do not lose promoter accessibility, allowing plants to rapidly reactivate transcription after the return to warm conditions. Conclusions Overall, our work provides a comprehensive view of the extent of transcriptome and promoter accessibility dynamics underlying plant adaptation to cooling and chilling conditions, revealing the function of key regulators at specific low temperature ranges.