Heat shock factor HSFA2 fine-tunes resetting of thermomemory via plastidic metalloprotease FtsH6

Plants ´memorize´ stressful events and protect themselves from future, often more severe, stresses. To maximize growth after stress, plants ´reset´, or ´forget´, memories of stressful situations which requires an intricate balance between stress memory formation and the degree of forgetfulness. HEAT SHOCK PROTEIN 21 (HSP21) encodes a small HSP in plastids of Arabidopsis thaliana. Previous research found that HSP21 functions as a key component of thermomemory, which requires a sustained elevated level of HSP21 during the recovery from heat stress (HS). A heat-induced metalloprotease, filamentation temperature sensitive H6 (FtsH6), degrades HSP21 to establish pre-stress level, thereby resetting memory during the recovery phase. The transcription factor heat shock factor A2 (HSFA2) activates downstream genes essential for mounting thermomemory thereby acting as a positive regulator in the process. Here, by employing a yeast one-hybrid screen we additionally identify HSFA2 as an upstream transactivator of the resetting element FtsH6. Constitutive and inducible overexpression of HSFA2 increases expression of FtsH6 while it is drastically reduced in the hsfa2 knockout mutant. Chromatin immunoprecipitation reveals in planta binding of HSFA2 to the FtsH6 promoter. Importantly, overexpression of HSFA2 improves thermomemory more profoundly in ftsh6 than wild-type plants. Thus, by activating both memory-supporting and -resetting genes HSFA2 acts as a cellular homeostasis factor during thermomemory