Specific CBF transcription factors and cold-responsive genes fine-tune the early triggering response after acquisition of cold priming and memory

Abstract

Plants need to adapt to fluctuating temperatures throughout their lifetime. Previous research showed that Arabidopsis memorizes a first cold stress (priming) and improves its primed freezing tolerance further when subjected to a second similar stress after a lag phase. This study investigates primary metabolomic and transcriptomic changes during early cold priming or triggering after 3 days at 4°C interrupted by a memory phase. DREB1 family transcription factors DREB1C/CBF2, DREB1D/CBF4, DREB1E/DDF2, and DREB1F/DDF1 were strongly significantly induced throughout the entire triggering. During triggering, genes encoding Late Embryogenesis Abundant (LEA), antifreeze proteins or detoxifiers of reactive oxygen species (ROS) were higher expressed compared with priming. Examples of early triggering responders were xyloglucan endotransglucosylase/hydrolase genes encoding proteins involved in cell wall remodeling, while late responders were identified to act in fine-tuning the stress response and developmental regulation. Induction of non-typical members of the DREB subfamily of ERF/AP2 transcription factors, the relatively small number of induced CBF regulon genes and a slower accumulation of selected cold stress associated metabolites indicate that a cold triggering stimulus might be sensed as milder stress in plants compared with priming. Further, strong induction of CBF4 throughout triggering suggests a unique function of this gene for the response to alternating temperatures.