One of the strategies that plants utilize to adapt to fluctuating soil nutrient levels is rapid reprogramming of transcriptional regulation via cell signaling mechanisms. Higher plants exposed to ammonium undergo modulation of a broad spectrum of gene expression. However, regulation of the transcriptional mechanisms underlying ammonium-mediated gene expression is poorly understood. We identified a transcriptional regulator, indeterminate domain 10 (IDD10), whose mutants exhibited an ammonium-hypersensitive root growth defect. To elucidate the molecular relationship between IDD10 and ammonium-mediated gene expression, ammonium-responsive genes were examined in mutants and overexpressors of IDD10. Among the key ammonium uptake and assimilation genes, AMT1;2 (ammonium transporter 1;2) and GDH2 (glutamate dehydrogenase 2) significantly depend on IDD10 expression levels for ammonium-mediated induction. Extensive molecular analysis revealed that IDD10 directly binds to the promoter of AMT1;2 and the fifth intron of GDH2 genes via the core sequence TTTGTC(C)/(G). Transcriptome analysis with root tissues identified many ammonium-inducible genes whose expression was increased by IDD10. Half of them contained potential IDD10-binding motifs in their promoters. This study determined that IDD10 is a transcriptional activator involved in nitrogen regulatory circuits that control a broad spectrum of gene expression, which might influence root growth in rice.