Polarized cells are frequently partitioned into subdomains with unique features or functions. As plant cells are surrounded by rigid walls, polarized cell shape and protein polarity in the plasma membrane are particularly important for normal physiology and development. Here we identify and characterize WALLFLOWER (WFL), a transmembrane receptor kinase that is asymmetrically distributed to the inner face of epidermal cells. 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). While WFL localization to the inner polar domain remains constant regardless of cell identity, its localization is affected by deletion of the intracellular domains. Polar localization of truncated WFL varies depending on cell identity indicating the WFL intracellular domains are important for informing cell type-specific positional information. Additionally, we observe that polar accumulation of WFL at specific plasma membrane domains is achieved and maintained by constant de novo protein secretion via a Brefeldin A sensitive endomembrane trafficking pathway. While wfl mutants don’t have a detectable abnormal phenotype, overexpression of WFL leads to a downward shift in root hair (RH) position. However, RH position is unaffected upon deletion of WFL intracellular domains, indicating that the kinase domain is required to inform RH position. Additionally, we find that roots overexpressing WFL-GFP are also sensitive to mechanical stress and prone to cell damage. However, this phenotype can be alleviated by cell wall rigidification or maintaining stable osmotic conditions. These observations, together with the shifted RH phenotype, suggest that WFL may have a role in coordinating cell wall modification with cellular expansion during RH development. We propose WFL participates in a signaling pathway that links cues from the inner cell layers of the root with polar growth at the epidermal surface, informing RH position.

In plants, coordination of cell division and differentiation is critical for tissue patterning and organdevelopment. Directional cell signaling and cell polarity have been proposed to participate in coordination of these developmental processes. For instance, a leucine-rich repeat receptor-like kinase (LRR-RLK) named INFLORESCENCE AND ROOT APICES KINASE (IRK) functions to restrict stele area and inhibit longitudinal anticlinal divisions (LADs) in the endodermis where it is polarly localized. The LRR-RLK most closely related to IRK is PXY/TDR CORRELATED 2 (PXC2) and we find that PXC2 shows similar polarized accumulation as IRK in root cell types. To further understand how these proteins operate in directional cell-cell signaling and root development we explored PXC2 function. pxc2 roots have an increase in stele area, indicating that PXC2 also functions to restrict stele size. Additionally, compared to either single mutant, irk pxc2 roots have an enhanced phenotype with further increases in endodermal LADs and stele area indicating redundant activities of these receptors. The double mutant also exhibits abnormal root growth, suggesting broader functions of PXC2 and IRK in the root. However, PXC2 is not functionally equivalent to IRK, as endodermal misexpression of PXC2 did not fully rescue irk. We propose that PXC2 is at least partially redundant to IRK with a more predominant role for IRK in repression of endodermal LADs. Our results are consistent with the hypothesis that repression of specific endodermal cell divisions and stele area through a PXC2/IRKmediated directional signaling pathway is required for coordinated root growth and development.