Regulation Of The High-affinity NO3- Uptake System By NRT1.1 ...

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Abstract

The NRT2.1 gene of Arabidopsis thaliana encodes a major component of the root high-affinity NO(3)(-) transport system (HATS) that plays a crucial role in NO(3)(-) uptake by the plant. Although NRT2.1 was known to be induced by NO(3)(-) and feedback repressed by reduced nitrogen (N) metabolites, NRT2.1 is surprisingly up-regulated when NO(3)(-) concentration decreases to a low level (<0.5 mm) in media containing a high concentration of NH(4)(+) or Gln (>or=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 NO(3)(-) availability through a mechanism independent from that involving N metabolites. We show here that repression of both genes by high NO(3)(-) is specifically mediated by the NRT1.1 NO(3)(-) transporter. This mechanism warrants that either NRT1.1 or NRT2.1 is active in taking up NO(3)(-) in the presence of a reduced N source. Under low NO(3)(-)/high NH(4)(+) 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 NH(4)(+) toxicity because NO(3)(-) taken up by the HATS in this situation prevents the detrimental effects of pure NH(4)(+) nutrition. It is thus hypothesized that NRT1.1-mediated regulation of NRT2.1/NRT3.1 is a mechanism aiming to satisfy a specific NO(3)(-) demand of the plant in relation to the various specific roles that NO(3)(-) 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 NO(3)(-).

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Figures

Figure 1.

Figure 1.

Changes in NRT2.1 mRNA accumulation…

Figure 1.

Changes in NRT2.1 mRNA accumulation in response to various formula image / formula image mixtures in the…

Figure 1. Changes in NRT2.1 mRNA accumulation in response to various formula image/formula image mixtures in the external medium. Plants were grown hydroponically for 6 weeks on complete nutrient solution containing 1 mm NH4NO3 before transfer to the various media indicated in the figure. A, Time-course response in plants transferred to nutrient solution containing 1 mm formula image plus 0.1 mm formula image. B, Effect of transfer for 4 d to media containing various combinations of formula image and formula image concentrations. Transcript accumulation was monitored in roots both by northern-blot analysis (gel-blot images) and real-time RT-PCR (bar graphs) on the same samples. A 25S rRNA signal is presented as a loading control for northern blots. Quantification by real-time RT-PCR was normalized using actin genes as controls. Errors bars represent se (n = 3). Different letters on top of the bars indicate statistically significant differences (P < 0.05; t test).
Figure 2.

Figure 2.

Effect of local changes in…

Figure 2.

Effect of local changes in the formula image / formula image external balance on NRT2.1 mRNA accumulation…

Figure 2. Effect of local changes in the formula image/formula image external balance on NRT2.1 mRNA accumulation in split-root plants. A, Representation of the experimental protocol. Plants were grown hydroponically for 5 weeks on complete nutrient solution containing 1 mm NH4NO3. After separation of their root system into two approximately equal sides, plants were transferred to specific containers and left undisturbed during 3 d in the 1 mm NH4NO3 solution before application of localized supplies with different formula image/formula image mixtures for 4 d, as indicated in the figure. B, NRT2.1 mRNA accumulation. Transcript accumulation was monitored in various sides of the split-root systems both by northern-blot analysis (gel-blot images) and real-time RT-PCR (bar graphs) on the same samples. The lane labels relate to the various localized treatments as shown in A. A 25S rRNA signal is presented as a loading control for northern blots. Quantification by real-time RT-PCR was normalized using actin genes as controls. Errors bars represent se (n = 3). Different letters on top of the bars indicate statistically significant differences (P < 0.05; t test).
Figure 3.

Figure 3.

Effect of various formula image / formula image mixtures…

Figure 3.

Effect of various formula image / formula image mixtures on NRT2.1 mRNA accumulation and root N uptake…

Figure 3. Effect of various formula image/formula image mixtures on NRT2.1 mRNA accumulation and root N uptake in Ws wild-type and atnrt2.1-1 mutant plants. The plants were grown hydroponically for 6 weeks on complete nutrient solution containing 1 mm NH4NO3 before transfer for 4 d to various media containing the same formula image concentration (1 mm), but various concentrations of formula image (0.1, 1, or 10 mm). A, NRT2.1 mRNA accumulation and root 15formula image influx. Transcript accumulation was monitored in roots both by northern-blot analysis (gel-blot images) and real-time RT-PCR (bar graphs) on the same samples. A 25S rRNA signal is presented as a loading control for northern blots. Quantification by real-time RT-PCR was normalized using actin genes as controls. Errors bars represent se (n = 3). Root 15formula image influx was assayed by 5-min labeling at 0.2 mm external 15formula image concentration to specifically determine activity of the HATS. Each value is the mean of eight to 12 replicates ± se. B, Root 15formula image influx. Root 15formula image influx was assayed by 5-min labeling at 1 mm external 15formula image concentration to determine the uptake activity at the same concentration as for growth and treatment of the plants. Each value is the mean of eight to 12 replicates ± se. N.D., Not determined. Different letters on top of the bars indicate statistically significant differences (P < 0.05; t test).
Figure 4.

Figure 4.

Relationship between NRT2.1 mRNA accumulation…

Figure 4.

Relationship between NRT2.1 mRNA accumulation and root formula image influx as a function of formula image concentration…

Figure 4. Relationship between NRT2.1 mRNA accumulation and root formula image influx as a function of formula image concentration in the presence of formula image in the external medium. Plants of Ws wild-type, atnrt1.2-1 mutant, and chl1-10 mutant were grown for 6 weeks on complete nutrient solution containing 1 mm NH4NO3, before transfer for 4 d to the nutrient solutions containing 1 mm formula image and formula image at various concentrations, as indicated in the figure. A, NRT2.1 mRNA accumulation. Transcript accumulation was monitored in roots both by northern-blot analysis (gel-blot images) and real-time RT-PCR (graph) on the same samples. A 25S rRNA signal is presented as a loading control for northern blots. Quantification by real-time RT-PCR was normalized using actin genes as controls. Errors bars represent se (n = 3). Differences between chl1-10 and the other genotypes are statistically significant at **P < 0.01 and ***P < 0.001 (t test). B, Root 15formula image influx. Root 15formula image influx was assayed by 5-min labeling at the external 15formula image concentration corresponding to that supplied to the plants during the 4-d treatment. Each value is the mean of six to 12 replicates ± se. C, Plot of NRT2.1 mRNA accumulation (A) against root 15formula image influx (B).
Figure 5.

Figure 5.

NRT2.1 and NRT3.1 coregulation. A,…

Figure 5.

NRT2.1 and NRT3.1 coregulation. A, Response of NRT3.1 mRNA accumulation in Ws, atnrt1.2 …
Figure 5. NRT2.1 and NRT3.1 coregulation. A, Response of NRT3.1 mRNA accumulation in Ws, atnrt1.2-1, and chl1-10 plants to the variation of formula image concentration in the presence of 1 mm formula image in the external medium. The experiment is the same as in Figure 5. B, Correlation between changes in NRT2.1 and NRT3.1 mRNA accumulation. All RNA samples used to determine changes in NRT2.1 expression presented in Figures 1 to 4 and Supplemental Figure S1 were analyzed for NRT3.1 mRNA accumulation. The figure presents the relative changes in transcript level for both NRT2.1 and NRT3.1 normalized to the control (Ws plants left on 1 mm NO3NH4) of each experiment. Gray squares, Experiment of Figure 1; white diamonds, experiment of Figure 2; gray triangles, experiment of Figure 3; white hexagons, experiment of Supplemental Figure S1; black circles, experiment of Figure 4.
Figure 6.

Figure 6.

Effect of NRT2.1 mutation on…

Figure 6.

Effect of NRT2.1 mutation on the protective effect of formula image against formula image toxicity. Images show…

Figure 6. Effect of NRT2.1 mutation on the protective effect of formula image against formula image toxicity. Images show the appearance of toxicity symptoms in shoots of Ws and atnrt2.1-1 mutant plants as a function of the N source supplied in the external medium (either 1 mm formula image alone or in combination with 0.1 mm formula image).
Figure 7.

Figure 7.

Shoot growth and root formula image uptake…

Figure 7.

Shoot growth and root formula image uptake of Ws and atnrt2.1 - 1 mutant plants…

Figure 7. Shoot growth and root formula image uptake of Ws and atnrt2.1-1 mutant plants supplied with 1 mm formula image with or without 0.1 mm formula image. Plants were grown hydroponically for 5 weeks on complete nutrient solution containing 1 mm NH4NO3 before transfer for 12 d to media containing either 1 mm formula image alone or 1 mm formula image plus 0.1 mm 15formula image. A, Shoot fresh weight. Values are the means of 10 to 18 replicates ± se. B, Cumulative 15formula image uptake from the 1 mm formula image plus 0.1 mm 15formula image solution during the 12-d period determined by total 15N analysis in both root and shoots at the end of the period. Values are the mean of 10 to 12 replicates ± se. Differences between wild type and mutant are statistically significant at **P < 0.01, ***P < 0.001 (t test). Ns, Not significant (P > 0.05).
Figure 8.

Figure 8.

Model for N regulation of …

Figure 8.

Model for N regulation of NRT2.1 expression in Arabidopsis roots. The model postulates…

Figure 8. Model for N regulation of NRT2.1 expression in Arabidopsis roots. The model postulates that, in addition to the induction by formula image, NRT2.1 is also under dual control by feedback repression by reduced N metabolites and NRT1.1-mediated repression by high external formula image availability, which are both required to suppress NRT2.1 expression.
All figures (8) See this image and copyright information in PMC

References

    1. Adriaanse FG, Human JJ (1993) Effect of time of application and nitrate: ammonium ratio on maize grain yield, grain N concentration and soil mineral N concentration in semi-arid region. Field Crops Res 34: 57–70
    1. Behl R, Tishner R, Raschke K (1988) Induction of a high-capacity nitrate-uptake mechanism in barley roots prompted by nitrate uptake through a constitutive low-capacity mechanism. Planta 176: 235–240 - PubMed
    1. Cao W, Tibbitts TW (1993) Study of various formula image/formula image mixtures for enhancing growth of potatoes. J Plant Nutr 16: 1691–1704 - PubMed
    1. Cerezo M, Tillard P, Filleur S, Munos S, Daniel-Vedele F, Gojon A (2001) Major alterations of the regulation of root formula image uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiol 127: 262–271 - PMC - PubMed
    1. Charrier B, Champion A, Henry Y, Kreis M (2002) Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase-polymerase chain reaction. Plant Physiol 130: 577–590 - PMC - PubMed
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