Phosphorylation-dependent activation of the bHLH transcription factor ICE1/SCRM promotes polarization of the Arabidopsis zygote

In Arabidopsis thaliana, the asymmetric cell division (ACD) of the zygote gives rise to the embryo proper and an extraembryonic suspensor, respectively. This process is controlled by the ERECTA-YODA-MPK3/6 receptor kinase-MAP kinase-signaling pathway, which also orchestrates ACDs in the epidermis. In this context, the bHLH transcription factor ICE1/SCRM is negatively controlled by MPK3/6-directed phosphorylation. However, it is unknown whether this regulatory module is similarly involved in the zygotic ACD. We investigated the function of SCRM in zygote polarization by analyzing the effect of loss-of-function alleles and variants that cannot be phosphorylated by MPK3/6, protein accumulation, and target gene expression. 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 WOX8. Our work further demonstrates that SCRM activity in the early embryo is positively controlled by MPK3/6-mediated phosphorylation. Therefore, the effect of MAP kinase-directed phosphorylation 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.