Abstract
Uneven nutrient availability in the soil is a common problem plants have to solve to optimise their mineral nutrition and growth. One important adaptive response to this constraint involves preferential root colonization of nutrient-rich patches. In the case of nitrogen, the Arabidopsis NRT1.1 nitrate transporter was shown to be crucial for this process since it is required for local stimulation of lateral root elongation by high nitrate concentration. NRT1.1 has been suggested to act as a nitrate sensor, located upstream of the ANR1 transcription factor in the nitrate -signalling pathway triggering the root colonization response. However, both the sensing mechanism and the downstream regulatory events involved in this root architectural response, remain largely unknown. We show that NRT1.1 transports not only nitrate but also the phytohormone auxin. Nitrate inhibits NRT1.1-mediated auxin influx, suggesting that the nitrate signal transduced by NRT1.1 is a modification of auxin transport. Auxin promotes lateral root development, and mutation of NRT1.1 enhances both auxin accumulation in lateral roots and growth of these roots at low, but not a high nitrate concentration. Thus, on homogenous nitrate medium, the role of the NRT1.1 nitrate sensor is to repress lateral root development at low nitrate availability by preventing auxin accumulation in these roots. Using a split-root system, we show that auxin-mediated nitrate sensing by NRT1.1 accounts for most of the adaptive response of the root system architecture to heterogeneous nitrate distribution. Indeed, in this system, NRT1.1 lowers auxin accumulation in lateral root tips grown under low nitrate but not in those on the high nitrate side. However, NRT1.1 controls cell division but not cell elongation. This explains the residual lateral root growth response recorded in NRT1.1 mutants and indicates the occurrence of NRT1.1-independent processes in the nitrate regulation of lateral root elongation. Finally, up-regulation of NRT1.1 expression by acidification of the external medium leads to an amplified lateral root growth response to nitrate. This suggests that the transcriptional regulation of NRT1.1 allows the plant to modulate the nitrate-dependency of root branching. Altogether, our data suggest that the role of NRT1.1 is to repress lateral root growth in nitrate-poor patches by preventing auxin-dependent activation of lateral root meristems.