Polar auxin transport regulates initial auxin patterning and polar nuclear migration during lateral root initiation

Abstract

In Arabidopsis thaliana, local auxin accumulation in xylem-pole pericycle (XPP) cells specifies lateral root founder cells, which establish de novo cell polarity manifested by polar nuclear migration and subsequent asymmetric division. Here, we developed a fast-maturing, XPP/early lateral root primordium (LRP)-specific R2D2 auxin reporter (fx-R2D2) to visualize auxin dynamics with high spatiotemporal resolution during LRP initiation. We demonstrate that auxin increases broadly on the convex side of XPP during root bending. Within this region, cells showing particularly strong auxin responses emerged, and subsequently underwent polar nuclear migration and asymmetric division, initiating an LRP. When two LRPs initiated in close proximity, auxin levels in one rapidly decreased after the cell division, followed by cessation of further division. These findings provide a clear picture of auxin dynamics during LRP initiation. Under uniform auxin treatment, de novo LRP formation events occur. Auxin treatment initially induced a uniform auxin response at a high level, followed by localized auxin depletion in regions where LRPs did not subsequently form, demonstrating that auxin depletion as well as accumulation shapes the auxin patterns during LRP initiation. Furthermore, we reveal that local PIN-mediated polar auxin transport regulates both de novo auxin patterning and polar nuclear migration during LRP initiation.