The NAC transcription factor SOMBRERO controls auxin gradients for columella root cap maturation and turnover

The plant root cap consists of continuously renewed cells that collectively protect meristematic stem cells, sense environmental stimuli, and guide root growth direction. Auxin gradients within the root cap are essential for cell turnover, root responses to external cues, and root cap development. However, our understanding of how the auxin gradient is established and maintained remains limited. Here, we show that the root cap-specific NAC transcription factor SOMBRERO (SMB), previously implicated in root cap maturation, turnover, and programmed cell death, coordinates auxin homeostasis, and signaling in the columella root cap. Inactivation of SMB (smb-3) disrupted the subcellular maturation program of root cap cells and diminished the auxin response gradient in the columella root cap. Root tip-specific transcriptomic profiling of wild-type (Col-0) and smb-3 revealed that transcript levels of auxin biosynthesis, transport, and signaling were significantly altered in smb-3. EMSA and promoter reporter assays further showed that SMB binds promoter fragments of multiple auxin-related genes and modulates their transcriptional activity, supporting a transcriptional role for SMB in auxin regulation. Perturbation of auxin transport impaired Golgi remodeling, xylogalacturonan accumulation, and border-like cell turnover. Exogenous auxin partially restored Golgi morphology but failed to rescue root cap organization and border-like cell turnover, indicating that proper auxin dynamics, rather than auxin levels alone, are required for root cap development. Taken together, these results extend previous understanding of SMB function and identify SMB as a versatile transcription factor that coordinates auxin dynamics with Golgi remodeling and root cap turnover.