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 [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} transport system (HATS) that plays a crucial role in [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} uptake by the plant. Although NRT2.1 was known to be induced by [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} and feedback repressed by reduced nitrogen (N) metabolites, NRT2.1 is surprisingly up-regulated when [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} concentration decreases to a low level (<0.5 mm) in media containing a high concentration of [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NH₄^{{+}}\) {document} 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 [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} availability through a mechanism independent from that involving N metabolites. We show here that repression of both genes by high [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} is specifically mediated by the NRT1.1 [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} transporter. This mechanism warrants that either NRT1.1 or NRT2.1 is active in taking up [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} in the presence of a reduced N source. Under low [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}/{high{\,}NH}₄^{{+}}\) {document} 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 [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NH₄^{{+}}\) {document} toxicity because [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} taken up by the HATS in this situation prevents the detrimental effects of pure [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NH₄^{{+}}\) {document} nutrition. It is thus hypothesized that NRT1.1-mediated regulation of NRT2.1/NRT3.1 is a mechanism aiming to satisfy a specific [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} demand of the plant in relation to the various specific roles that [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document} 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 [fleqn,10pt,legalpaper]{article} {amssymb} {amsfonts} {amsmath} {empty} {document} \(NO₃^{{-}}\) {document}.