Localized proliferation of lateral roots in NO3--rich patches is a striking example of the nutrient-induced plasticity of root development. In Arabidopsis, NO3- stimulation of lateral root elongation is apparently under the control of a NO3--signaling pathway involving the ANR1 transcription factor. ANR1 is thought to transduce the NO3- signal internally, but the upstream NO3- sensing system is unknown. Here, we show that mutants of the NRT1.1 nitrate transporter display a strongly decreased root colonization of NO3--rich patches, resulting from reduced lateral root elongation. This phenotype is not due to lower specific NO3- uptake activity in the mutants and is not suppressed when the NO3--rich patch is supplemented with an alternative N source but is associated with dramatically decreased ANRI expression. These results show that NRT1.1 promotes localized root proliferation independently of any nutritional effect and indicate a role in the ANR1- dependent N0 signaling pathway, either as a NO3- sensor or as a facilitator of NO3- influx into NO3--sensing cells. Consistent with this model, the NRT1. I and ANRI 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 NO3--rich zone impairs the efficient acquisition of N0 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 NO3--sensing system that enables the plant to detect and exploit NO3--rich soil patches. [ABSTRACT FROM AUTHOR]