Mechanical cues trigger phellem differentiation during barrier transition

Abstract

A continuous and uninterrupted barrier tissue is essential for protecting internal tissues from the external environment. In many dicot roots, the endodermis fulfils this role during primary growth; however, the onset of secondary growth in the vascular tissue coincides with the rupture of the overlying endodermis and formation of a new barrier, the periderm, beneath it. Despite the importance of barrier integrity for plant survival, the mechanisms coordinating this barrier transition have remained unexplored. Here, we show that endodermal rupture in Arabidopsis thaliana roots releases mechanical constraints on the underlying properiderm. This release leads to cell expansion and triggers differentiation of the outermost properiderm cells into phellem, a ligno-suberized barrier cell type. Premature relief of mechanical constraints, through hyperosmotic stress or targeted endodermal ablation, is sufficient to trigger phellem differentiation. FERONIA, a cell wall integrity receptor kinase, is required for phellem differentiation in response to mechanical stress. Overall, our findings establish mechanical stress as an instructive cue for phellem differentiation, revealing how plants convert mechanical signals into robust, adaptive protective barriers.