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Abstract Polarity of plasma membrane proteins is essential for cell morphogenesis and control of cell division and, thus, influences organ and whole plant development. In Arabidopsis (Arabidopsis thaliana) root endodermal cells, 2 transmembrane kinases, INFLORESCENCE AND ROOT APICES RECEPTOR KINASE (IRK) and KINASE ON THE INSIDE (KOIN), accumulate at opposite lateral domains. Their polarization is tightly linked to their activities regulating cell division and ground tissue patterning. The polarization of IRK and KOIN relies solely on the secretion of newly synthesized protein. However, the secretion machinery by which their opposite, lateral polarity is achieved remains largely unknown. Here, we show that different sets of ADP-ribosylation factor (ARF)-guanine-nucleotide exchange factors (ARF-GEFs) mediate their secretion. ARF-GEF GNOM-like-1 (GNL1) regulates KOIN secretion to the inner polar domain, thereby directing KOIN sorting early in the secretion pathway. For IRK, combined chemical and genetic analyses showed that the ARG-GEF GNL1, GNOM, and the BREFELDIN A-INHIBITED-GUANINE NUCLEOTIDE-EXCHANGE FACTORs 1 to 4 (BIG1-BIG4) collectively regulate its polar secretion. The ARF-GEF-dependent mechanisms guiding IRK or KOIN lateral polarity were active across different root cell types and functioned regardless of the protein's inner/outer polarity in those cells. Therefore, we propose that specific polar trafficking of IRK and KOIN occurs via distinct mechanisms that are not constrained by cell identity or polar axis and likely rely on individual protein recognition. 

ABSTRACT Polarized cells are frequently partitioned into subdomains with unique features or functions. As plant cells are surrounded by walls, polarized cell shape and protein polarity in the plasma membrane are particularly important for normal physiology and development. We have identified WALLFLOWER (WFL), a transmembrane receptor kinase that is asymmetrically distributed at the inner face of epidermal cells and this localization is maintained independent of cell type. In epidermal hair (H) cells in the elongation and differentiation zones, WFL exhibits a dual polar localization, accumulating at the inner domain as well as at the root hair initiation domain (RHID). Furthermore, overexpression of WFL leads to a downward shift in root hair (RH) position suggesting WFL operates in a signaling pathway that functions across H cells to inform RH position. WFL asymmetric distribution and function is affected by deletion of the intracellular domains resulting in its mislocalization to the outer polar domain of H cells and exclusion from RHIDs and bulges. Thus, our results demonstrate that in epidermal H cells the WFL intracellular domains are required to direct its dual polar localization and influence RH position. ONE SENTENCE SUMMARYA receptor kinase with dual polar localization, to the inner polar domain and root hair initiation domain, in root epidermal cells, requires its intracellular domain for localization and function. 

Abstract In plants, cell polarity plays key roles in coordinating developmental processes. Despite the characterization of several polarly localized plasma membrane proteins, the mechanisms connecting protein dynamics with cellular functions often remain unclear. Here, we introduce a polarized receptor, KOIN, that restricts cell divisions in the Arabidopsis root meristem. In the endodermis, KOIN polarity is opposite to IRK, a receptor that represses endodermal cell divisions. Their contra-polar localization facilitates dissection of polarity mechanisms and the links between polarity and function. We find that IRK and KOIN are recognized, sorted, and secreted through distinct pathways. IRK extracellular domains determine its polarity and partially rescue the mutant phenotype, whereas KOIN’s extracellular domains are insufficient for polar sorting and function. Endodermal expression of an IRK/KOIN chimera generates non-cell-autonomous misregulation of root cell divisions that impacts patterning. Altogether, we reveal two contrasting mechanisms determining these receptors’ polarity and link their polarity to cell divisions in root tissue patterning.