The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches

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 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 NO3- signaling pathway, either as a NO3- sensor or as a facilitator of NO3- influx into NO3--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 NO3--rich zone impairs the efficient acquisition of NO3- 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.