Bearskin2 mediates the coordinated secretion of xylogalacturonan and root cap polygalacturonase in Arabidopsis border-like cells

Border-like cells (BLCs) are sheets of cells that are continuously sloughed off and replenished at the Arabidopsis root cap surface. ROOT CAP POLYGALACTURONASE (RCPG) encodes a putative pectinase involved in BLC shedding. Xylogalacturonan (XGA) is a pectic polysaccharide whose synthesis is associated with cell detachment and secreted separately from other cell wall polysaccharides. BEARSKIN1 (BRN1) and BRN2 are Arabidopsis NAC family transcription factors, and RCPG expression is inhibited in brn1/2. To explore the link between XGA and RCPG, we examined XGA synthesis in Arabidopsis lines with altered RCPG levels. We found that RCPG was contained in XGA-carrying vesicles budding from the trans-Golgi, but XGA synthesis was not affected in the rcpg mutant. XGA was absent in BLCs of brn2, but not of brn1, indicating that BRN2 is necessary for XGA synthesis. Overexpression of functional RCPG-GFP (oeRCPG-GFP) caused upregulation of BRN2, ectopic XGA synthesis, overaccumulation of endogenous RCPG, and accelerated BLC turnover, suggesting a positive regulatory loop between RCPG and BRN2. Inactivation of BRN2 in oeRCPG-GFP suppressed RCPG-GFP expression, excess RCPG, and XGA synthesis. Our data provide evidence that XGA and RCPG are secreted together and that BRN2 controls XGA synthesis, which facilitates RCPG export and BLC separation.