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Abstract MAPK signaling modules play crucial roles in regulating numerous biological processes in all eukaryotic cells. How MAPK signaling specificity and strength are tightly controlled remains a major challenging question. InArabidopsisstomatal development, the MAPKK Kinase YODA (YDA) functions at the cell periphery to inhibit stomatal production by activating MAPK 3 and 6 (MPK3/6) that directly phosphorylate stomatal fate-determining transcription factors for degradation in the nucleus. Recently, we demonstrated that BSL1, one of the four BSL protein phosphatases, localizes to the cell cortex to activate YDA, elevating MPK3/6 activity to suppress stomatal formation. Here, we showed that at the plasma membrane, all four members of BSL proteins contribute to the YDA activation. However, in the nucleus, specific BSL members (BSL2, BSL3, and BSU1) directly deactivate MPK6 to counteract the linear MAPK pathway, thereby promoting stomatal formation. Thus, the pivotal MAPK signaling in stomatal fate determination is spatially modulated by a signaling dichotomy of the BSL protein phosphatases inArabidopsis, providing a prominent example of how MAPK activities are integrated and specified by signaling compartmentalization at the subcellular level. 

Abstract Cell polarity is a fundamental feature underlying cell morphogenesis and organismal development. In theArabidopsisstomatal lineage, the polarity protein BASL controls stomatal asymmetric cell division. However, the cellular machinery by which this intrinsic polarity site is established remains unknown. Here, we identify the PRAF/RLD proteins as BASL physical partners and mutating fourPRAFmembers leads to defects in BASL polarization. Members of PRAF proteins are polarized in stomatal lineage cells in a BASL-dependent manner. Developmental defects of theprafmutants phenocopy those of thegnommutants. GNOM is an activator of the conserved Arf GTPases and plays important roles in membrane trafficking. We further find PRAF physically interacts with GNOM in vitro and in vivo. Thus, we propose that the positive feedback of BASL and PRAF at the plasma membrane and the connected function of PRAF and GNOM in endosomal trafficking establish intrinsic cell polarity in theArabidopsisstomatal lineage.