A subset of group S1 bZIP transcription factors controls resource management during starvation and recovery in Arabidopsis

Plants exhibit considerable phenotypic plasticity, allowing them to adapt their metabolism to the fluctuating energy supply in a natural environment. Using dark-induced senescence (DIS) as an experimental system, a mutant study combining phenotypic, transcriptomic and chromatin immunoprecipitation sequencing approaches identified distinct members of the Arabidopsis thaliana group S1 basic leucine zipper (bZIP) transcription factors that orchestrate the starvation response. Whereas excluding bZIP2, bZIP11, and bZIP44 to play a major role in DIS, bZIP1, and bZIP53 act partially redundantly to control a coexpression network governing amino acid catabolism and transport, gluconeogenesis and energy homeostasis. Moreover, bZIP1 and bZIP53 regulate genes involved in the asparagine-glutamine balance, two amino acids critical for carbon and nitrogen homeostasis. This transcriptional reprogramming in resource management is required for survival during starvation and regaining meristematic activity during the recovery from stress. Thus, our findings provide insights into the transcriptional control of plant resource and energy management during starvation. Overall, this work sheds light on the discrepancy between in vitro DNA binding and overexpression studies versus mutant analyses and in vivo DNA binding, providing a critical view on how to define specific transcription factor functions within large families.