Phosphorylation-Dependent Activation of the bHLH Transcription Factor ICE1/SCRM Promotes Polarization of the Arabidopsis Zygote

Asymmetric cell divisions are a key mechanism for breaking symmetry and orchestrating different cell identities in multicellular organisms. In Arabidopsis thaliana, as in most flowering plants, the first zygotic cell division is asymmetric, giving rise to the embryo proper and an extraembryonic suspensor. Zygotic polarization and differential cell identities in the daughter cells are controlled by the ERECTA-YODA pathway, a prototype receptor kinase-MAP kinase signaling pathway. This pathway also controls asymmetric cell divisions in the epidermis during stomatal development. In this context, the bHLH transcription factor ICE1/SCRM is a direct target of MPK3/6, and phosphorylation negatively controls SCRM activity by targeting the protein for proteasomal degradation. This raises the question if this regulatory module is also involved in the asymmetric division of the zygote. Our results show that SCRM has a critical function in zygote polarization and acts in parallel with the known MPK3/6 target WRKY2 in activating the homeobox transcription factor gene WOX8. Our work further demonstrates that SCRM activity in the early embryo is positively controlled by MPK3/6-mediated phosphorylation. Therefore, the mode of MAP kinase regulation of the same target protein fundamentally differs between the embryo and the epidermis, shedding light on cell type-specific, differential gene regulation by common signaling pathways.