MUTE Directly Orchestrates Cell State Switch and the Single Symmetric Division to Create Stomata

SUMMARY Precise cell division control is critical for developmental patterning. For the differentiation of a functional stoma, a cellular valve for efficient gas exchange, the single symmetric division of an immediate precursor is absolutely essential. Yet, the mechanism governing the single division event remains unclear. Here we report the complete inventories of gene expression by the Arabidopsis bHLH protein MUTE, a potent inducer of stomatal differentiation. MUTE switches the gene expression program initiated by its sister bHLH, SPEECHLESS. MUTE directly induces a suite of cell-cycle genes, including CYCD5;1, and their transcriptional repressors, FAMA and FOUR LIPS . The architecture of the regulatory network initiated by MUTE represents an Incoherent Type 1 Feed-Forward Loop. Our mathematical modeling and experimental perturbations support a notion that MUTE orchestrates a transcriptional cascade leading to the tightly-restricted, robust pulse of cell-cycle gene expression, thereby ensuring the single cell division to create functional stomata. Highlights Complete inventories of gene expression in stomatal differentiation state are elucidated MUTE switches stomatal patterning program initiated by its sister bHLH, SPEECHLESS MUTE directly induces cell-cycle genes and their direct transcriptional repressors Incoherent feed-forward loop by MUTE ensures the single division of a stomatal precursor