POLYGALACTURONASES REGULATED BY AUXIN facilitate root cell elongation in Arabidopsis thaliana via pectin remodeling

Root cell elongation, the main driver of root growth, is tightly associated with cell wall remodeling, particularly through pectin modifications, which facilitate cell wall loosening and strengthening while maintaining structural integrity. Root cell elongation is precisely regulated by the phytohormone auxin, which has long been known to inhibit this process. The molecular pathways through which auxin influences cell wall modifications remain poorly understood. In this study, we explore the transcriptional regulation of cell wall-related genes by auxin in Arabidopsis thaliana roots. The nuclear auxin pathway altered the expression of numerous cell-wall related genes, suggesting dynamic modification of the cell wall during root cell elongation. We identified novel root-specific polygalacturonases (PGs), enzymes involved in pectin degradation, which we termed POLYGALACTURONASES REGULATED BY AUXIN (PGRAs). PGRAs are expressed specifically in the root epidermis, beginning at the elongation zone. Our results demonstrate that induction of PGRA1 expression initially promotes root cell elongation, while long term overexpression inhibits root growth. Auxin downregulates PGRA1 in the elongation zone, and plants lacking PGRAs fail to increase root growth rate in response to reduced auxin levels. This suggests that auxin downregulates PGRA expression to prevent PGRA-mediated pectin remodeling, thereby contributing to inhibition of root cell elongation. We established a novel link between auxin signaling and pectin modifications in the control of cell growth. These findings provide new insights into the molecular mechanisms through which auxin regulates root cell elongation, highlighting the role of pectin matrix modifications in this process.