Nuclear condensates of BZU2/ZmMUTE modulate transcription to realize structural heterogeneity of the maize stomatal complex

During development, cell fate determination hinges on the dynamic activities of multiple transcription factors (TFs), but how the activities of individual TFs contribute to developmental diversity remains incompletely understood. Here, we report that BZU2/ZmMUTE is responsible for the functional and spatial heterogeneity of the four-celled stomatal complexes in maize (Zea mays), in part through its liquid-liquid phase separation (LLPS) property. Genotypic and single-cell RNA-seq analyses confirmed previous findings that ZmMUTE is associated with lineage-specific gene expression during stomatal development, while providing additional resolution of cell-type-specific transcriptional programs. The intrinsically disordered region 4 (IDR4) promotes the formation of ZmMUTE condensates, which can recruit the ZmMUTE partner ZmSCRM and associate with transcriptionally active sites. These condensates are associated with enhanced DNA binding and target gene activation, potentially influencing the development of guard cells and subsidiary cells. IDR4 is also sufficient for conferring cell-to-cell mobility to AtMUTE, highlighting its conserved role in facilitating intercellular movement. Taken together, the dynamic behavior of ZmMUTE, owing to its condensational properties, appears to orchestrate cell-type-specific regulation, thereby enabling the emergence of the unique four-celled stomatal morphology.