Regulation of the high-affinity NO3- uptake system by NRT1.1-mediated NO3- demand signaling in Arabidopsis

The NRT2.1 gene of Arabidopsis thaliana encodes a major component of the root high-affinity NO3- transport system ( HATS) that plays a crucial role in NO3- uptake by the plant. Although NRT2.1 was known to be induced by NO3- and feedback repressed by reduced nitrogen (N) metabolites, NRT2.1 is surprisingly up-regulated when NO3- concentration decreases to a low level (< 0.5 mM) in media containing a high concentration of NH4+ or Gln (>= 1 mM). The NRT3.1 gene, encoding another key component of the HATS, displays the same response pattern. This revealed that both NRT2.1 and NRT3.1 are coordinately down-regulated by high external NO3- availability through a mechanism independent from that involving N metabolites. We show here that repression of both genes by high NO3- is specifically mediated by the NRT1.1 NO3- transporter. This mechanism warrants that either NRT1.1 or NRT2.1 is active in taking up NO3- in the presence of a reduced N source. Under low NO3-/high NH4+ provision, NRT1.1-mediated repression of NRT2.1/NRT3.1 is relieved, which allows reactivation of the HATS. Analysis of atnrt2.1 mutants showed that this constitutes a crucial adaptive response against NH4+ toxicity because NO3- taken up by the HATS in this situation prevents the detrimental effects of pure NH4+ nutrition. It is thus hypothesized that NRT1.1-mediated regulation of NRT2.1/NRT3.1 is a mechanism aiming to satisfy a specific NO3- demand of the plant in relation to the various specific roles that NO3- plays, in addition to being a N source. A new model is proposed for regulation of the HATS, involving both feedback repression by N metabolites and NRT1.1-mediated repression by high NO3-.