Root Cap-Specific Transcriptomics Identify the NAC Transcription Factor SOMBRERO as a Versatile Regulator of Auxin Gradients

Auxin gradients in the root cap play a crucial role in the root cap development and root tropism. In the central root cap, meristematic cells in the columella initial differentiate into gravity-sensing columella cell, and mature into border-like cells that eventually separate from the root cap. Golgi stacks exhibit distinct ultrastructural features in each cell type across the central root cap, serving as effective cell markers. This cell type-specific Golgi remodeling was inhibited in smb-3 mutant root cap. When we carried out transcriptomic analyses of isolated root cap from Col-0 and smb-3, transcript levels of numerous auxin-related genes, including those involved in auxin synthesis, transport, and signaling, were significantly altered in smb-3 mutant root caps. The auxin gradient was suppressed within the central root cap of smb-3 mutant lines and they displayed decreased sensitivity to N-1-naphthylphthalamic acid (NPA) in comparison to Col-0. Furthermore, we demonstrated that the SMB binds to the promoter regions of auxin-related genes displaying large changes in smb-3 root cap cells. Our findings suggest that SMB functions as a versatile transcription factor that regulates the expression of genes critical for local auxin distribution and responses in the root cap, thereby coordinating root cap cell differentiation and controlling root growth directions in response to external stimuli.