Mucilage secretion from the root cap requires the NAC family transcription factor BEARSKIN2

The root cap secretes mucilage and sheds border cells (border-like cells, BLCs) in Arabidopsis (Arabidopsis thaliana). These mucilage and root cap-derived cells form a defensive barrier against soil pathogens. BEARSKIN1 (BRN1) and BRN2 are 2 homologous NAM, ATAF1/2, and CUC2 (NAC) family transcription factors of Arabidopsis, and mucilage secretion is inhibited in the brn1/2 double mutant. BRN1 and BRN2 are also involved in the expression of a pectin-digesting enzyme, POLYGALACTURONASE (RCPG), that facilitates BLC shedding. To further explore the connection between mucilage secretion and BLC shedding, we examined mucilage production in Arabidopsis lines displaying altered BLC detachment. Inactivation of BRN2 blocked mucilage synthesis and secretion, while inactivation of BRN1 and RCPG did not. Interestingly, RCPG sorted into mucilage-carrying vesicles budding from the Golgi and inhibited mucilage secretion in brn2-delayed BLC detachment. The root cap of a germinating seedling is initially covered with a cuticle, which is replaced by mucilage from BLCs as the seedling begins to shed these cells. Ectopic expression of RCPG in germinating seedlings caused early BLC formation and accelerated the cuticle-to-mucilage transition, indicating that RCPG expression and mucilage secretion are co-regulated. Furthermore, brn2 roots exhibited slower growth and increased cell death when subjected to salt or osmotic stress. Our research suggests that BRN2-mediated mucilage secretion contributes to BLC release to build an extracellular defense zone surrounding the root cap.