Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture

Abstract

Background: Productive agriculture needs a large amount of expensive nitrogenous fertilizers. Improving nitrogen use efficiency (NUE) of crop plants is thus of key importance. NUE definitions differ depending on whether plants are cultivated to produce biomass or grain yields. However, for most plant species, NUE mainly depends on how plants extract inorganic nitrogen from the soil, assimilate nitrate and ammonium, and recycle organic nitrogen. Efforts have been made to study the genetic basis as well as the biochemical and enzymatic mechanisms involved in nitrogen uptake, assimilation, and remobilization in crops and model plants. The detection of the limiting factors that could be manipulated to increase NUE is the major goal of such research.

Scope: An overall examination of the physiological, metabolic, and genetic aspects of nitrogen uptake, assimilation and remobilization is presented in this review. The enzymes and regulatory processes manipulated to improve NUE components are presented. Results obtained from natural variation and quantitative trait loci studies are also discussed.

Conclusions: This review presents the complexity of NUE and supports the idea that the integration of the numerous data coming from transcriptome studies, functional genomics, quantitative genetics, ecophysiology and soil science into explanatory models of whole-plant behaviour will be promising.

Fig. 1.

Schematic presentation of the known localisation of NRT1, NRT2 and AMT genes in Arabidopsis. Two nitrate transport systems have been shown to coexist in plants and to act co-ordinately to take up nitrate from the soil solution and distribute nitrate within the whole plant. The role of each ammonium transporter has been shown by the study of single, double, triple and quadruple mutants.

Fig. 2.

Schematic presentation of key enzymes involved in nitrogen management in (A) young and (B) senescing leaves. (A) Nitrate reductase (NR) and asparagine synthetase (AS) are localized in the cytosol, and nitrite reductase (NiR), glutamine synthetase 2 isoenzyme (GS2), glutamate synthase (GOGAT) and carbamoylphosphate synthetase (CPSase) within the plastids of mesophyll cells. Glutamine synthetase isoenzyme 1 (GS1) and AS are located in the cytosol of companion cells. (B) Senescence-associated events include chloroplast degradation and translocation of plastid proteins to the central vacuole via senescence-associated vacuole (SAV) trafficking. Amino acid recycling occurred in mitochondria and cytosol of mesophyll cells and companion cells. Glutamate dehydrogenase (GDH), GS1 and AS are the major enzymes involved in the synthesis of glutamine, glutamate and asparagine in the phloem.

Fig. 3.

Nitrate uptake (HATS + LATS) is lower during seed maturation than in the vegetative stage but still operates. (A) Root nitrate influx in plants at the vegetative (Veg.) and reproductive (Repro.) stage. Nitrate influx was measured by supplying 6 mm ¹⁵NO₃⁻ for 5 min to plants grown with 10 mm nitrate. (B) Expression of NRT1-1 (left) and NRT2-1 (right) genes, at the vegetative (Veg.) and reproductive (Repro.) stage. Expression of nitrate transporter genes was measured using quantitative PCR and expressed as a percentage of the tubulin 4 gene, used as a control.

Fig. 4.

Asparagine synthetase AS1 might play a role in nitrogen recycling and mobilization. (A) Phenotypes of asn1 mutant (Gabi 829B05) and Col0 wild-type grown in greenhouse with 10 mm nitrate. (B) Hydroponically grown asn1 mutant (Gabi 829B05) and Col0 were labelled using ¹⁵NO₃⁻-containing nutritive solution for 4 weeks (from sowing to the end of the pulse period T₀). At T₀, plants were transferred to a ¹⁵NO₃⁻-free solution and chase period was performed over 2 weeks (T₁ = T₀ + 2 weeks). At T₁, partitioning of ¹⁵N (¹⁵N%, as percentage of whole plant) in roots, rosette (already emerged at T₀) and new leaves (emerged between T₀ and T₁) was monitored in ans1 mutant and Col0. Nitrogen remobilization from rosette to the new leaves occurring during the chase period (T₀ to T₁) was higher in asn1 mutant than in wild-type, as shown by the greater decrease of ¹⁵N% in rosette and the higher ¹⁵N% in new leaves of mutant. (C) Nitrogen remobilization from the vegetative tissues to the seeds was monitored according to Diaz et al. (2008). ¹⁵N labelling was performed once at the vegetative stage. At the end of the plant cycle, the dry weight of seeds and dry remains were recorded and used to calculate harvest index (HI, seed d. wt as a percentage of the whole-plant d. wt). The amount of ¹⁵N remobilized from the rosette to the seeds was estimated through the calculation of ¹⁵N partitioning in seeds (P%¹⁵N; ¹⁵N in seeds as a percentage of total ¹⁵N in the whole plant). Comparing P%¹⁵N/HI ratios facilitates comparison between plants with different HI. The mutant (M) displayed significantly higher HI than wild-type (WT) and might be impaired for N-remobilization to the seeds as shown by its slightly lower P%¹⁵N/HI ratio. Such preliminary finding needs confirmation using a second mutant allele.

Fig. 5.

Nitrogen absorption and nitrogen remobilization profiling of five Arabidopsis accessions. A core collection of 18 accessions of Arabidopsis grown with 10 mm nitrate was used to measure traits related to biomass, N uptake, N remobilization and NUE (C. Masclaux-Daubresse and F. Chardon, unpubl. res.). Five accessions representative of the main classes found are presented. Traits measured at the vegetative stage (40 d after sowing) are rosette dry weight (DW), nitrogen concentration in the rosette (N%) and N-uptake efficiency (NupE) as the quantity of ¹⁵N absorbed at 40 d after sowing divided by plant biomass. Traits measured at the end of the plant cycle are N remobilization efficiency (¹⁵NHI) expressed as the partitioning of ¹⁵N in seeds compared with whole plant (seeds + dry remains; see Diaz et al., 2008), harvest index (HI) expressed as the partitioning of biomass (dry matter) in seeds (DM of seeds/DM of the whole plant), N concentration in dry remains (%NDR) and N concentration in the seeds (%N_SEED). Individual values ranged between [−4; + 4] and centred around the mean value of the core collection (value 0). The small sample of accessions highlights the variation of performances. Plants, such as Col0 or Sha, have a relatively good N uptake. The highest N remobilization score was found in Stw-0 while plants with high N percentage and high biomass were Bur-0 and Tsu-0.

Fig. 6.

Heat map illustrating the natural variation in expression of genes involved in nitrogen metabolism. Signal levels of N genes in ten accessions were obtained from the Arabidopsis eFP-Browser. For each gene, high expression is depicted as dark shading, and low expression is depicted as light shading.