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Transcript Profiling in the chl1-5 Mutant of Arabidopsis Reveals a Role of the Nitrate Transporter NRT1.1 in the Regulation of Another Nitrate Transporter, NRT2.1

Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, Agro-M/Centre National de la Recherche Scientifique/Institut National de la Recherche Agronomique/Université Montpellier 2, 34060 Montpellier, Cedex 1, France

² To whom correspondence should be addressed. E-mail gojon{at}ensam.inra.fr; fax 33-4-67-52-57-37.

Arabidopsis thaliana mutants deficient for the NRT1.1 NO₃^– transporter display complex phenotypes, including lowered NO₃^– uptake, altered development of nascent organs, and reduced stomatal opening. To obtain further insight at the molecular level on the multiple physiological functions of NRT1.1, we performed large-scale transcript profiling by serial analysis of gene expression in the roots of the chl1-5 deletion mutant of NRT1.1 and of the Columbia wild type. Several hundred genes were differentially expressed between the two genotypes, when plants were grown on NH₄NO₃ as N source. Among these genes, the N satiety-repressed NRT2.1 gene, encoding a major component of the root high-affinity NO₃^– transport system (HATS), was found to be strongly derepressed in the chl1-5 mutant (as well as in other NRT1.1 mutants). This was associated with a marked stimulation of the NO₃^– HATS activity in the mutant, suggesting adaptive response to a possible N limitation resulting from NRT1.1 mutation. However, derepression of NRT2.1 in NH₄NO₃-fed chl1-5 plants could not be attributed to lowered production of N metabolites. Rather, the results show that normal regulation of NRT2.1 expression is strongly altered in the chl1-5 mutant, where this gene is no more repressible by high N provision to the plant. This indicates that NRT1.1 plays an unexpected but important role in the regulation of both NRT2.1 expression and NO₃^– HATS activity. Overexpression of NRT2.1 was also found in wild-type plants supplied with 1 mM NH₄⁺ plus 0.1 mM NO₃^–, a situation where NRT1.1 is likely to mediate very low NO₃^– transport. Thus, we suggest that it is the lack of NRT1.1 activity, rather than the absence of this transporter, that derepresses NRT2.1 expression in the presence of NH₄⁺. Two hypotheses are discussed to explain these results: (1) NRT2.1 is upregulated by a NO₃^– demand signaling, indirectly triggered by lack of NRT1.1-mediated uptake, which overrides feedback repression by N metabolites, and (2) NRT1.1 plays a more direct signaling role, and its transport activity generates an unknown signal required for NRT2.1 repression by N metabolites. Both mechanisms would warrant that either NRT1.1 or NRT2.1 ensure significant NO₃^– uptake in the presence of NH₄⁺ in the external medium, which is crucial to prevent the detrimental effects of pure NH₄⁺ nutrition.

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