Stem cells in the plant meristems are kept undifferentiated by signals from surrounding cells and provide the basis for continuous organ formation. In the stem cell organizer of the Arabidopsis thaliana root, the Quiescent Center (QC), the WOX5 transcription factor functions as a central hub in regulating columella stem cell (CSC) homeostasis. However, the processes mediating WOX5 function have yet to be discovered. Here, we identify the transcription factor HAN as a central mediator of WOX5-regulated stem cell maintenance. HAN is required and sufficient to maintain CSCs undifferentiated and to induce ectopic stem cells. WOX5 and HAN repress transcription of the differentiation factor gene CDF4 in a coherent Feed Forward Loop (cFFL), one output of which is the expression of the auxin biosynthesis gene TAA1 and maintaining auxin response maxima in the organizer. Mathematical WOX5/HAN/CDF4cFFL modeling suggests a mechanism to buffer columella stem cell maintenance against input noise.