Localized proliferation of lateral roots in NO(3)(-)-rich patches is a striking example of the nutrient-induced plasticity of root development. In Arabidopsis, NO(3)(-) stimulation of lateral root elongation is apparently under the control of a NO(3)(-)-signaling pathway involving the ANR1 transcription factor. ANR1 is thought to transduce the NO(3)(-) signal internally, but the upstream NO(3)(-) sensing system is unknown. Here, we show that mutants of the NRT1.1 nitrate transporter display a strongly decreased root colonization of NO(3)(-)-rich patches, resulting from reduced lateral root elongation. This phenotype is not due to lower specific NO(3)(-) uptake activity in the mutants and is not suppressed when the NO(3)(-)-rich patch is supplemented with an alternative N source but is associated with dramatically decreased ANR1 expression. These results show that NRT1.1 promotes localized root proliferation independently of any nutritional effect and indicate a role in the ANR1-dependent NO(3)(-) signaling pathway, either as a NO(3)(-) sensor or as a facilitator of NO(3)(-) influx into NO(3)(-)-sensing cells. Consistent with this model, the NRT1.1 and ANR1 promoters both directed reporter gene expression in root primordia and root tips. The inability of NRT1.1-deficient mutants to promote increased lateral root proliferation in the NO(3)(-)-rich zone impairs the efficient acquisition of NO(3)(-) and leads to slower plant growth. We conclude that NRT1.1, which is localized at the forefront of soil exploration by the roots, is a key component of the NO(3)(-)-sensing system that enables the plant to detect and exploit NO(3)(-)-rich soil patches.