AP1 is a pioneer transcription factor that programmes cell fate through MADS-domain protein tetramerisation

In animals, pioneer transcription factors (TFs) have long been known to be crucial molecular players in programming cell fate. However, in plants much less is known about this functional class of TFs and how they mechanistically alter local chromatin architecture in order to reprogramme gene regulation to orchestrate cell fate changes. Here, we provide evidence that APETALA1 (AP1) functions as a pioneer TF in Arabidopsis thaliana, facilitated by tetramerisation. Using an integrated combination of multi-omics and high-resolution imaging approaches on both wild-type and AP1 mutant transgenic plants, we show that tetramerisation assists AP1 in providing access to, and enhancing the binding of AP1 to, closed chromatin in vivo. This, in turn, allows for a switching of the chromatin state from closed to open to ensure access to target DNA sequences needed for organ specification. These novel insights provide a mechanistic basis for how AP1 functions as a pioneer factor to reprogramme stem cells towards a “floral ground state”, increasing our understanding of how MADS-domain TFs function as combinatorial units during early Arabidopsis thaliana reproductive development.