Abstract
Nitrate and ammonium are the main nitrogen sources in agricultural soils. In the last decade, ammonium (NH4+), a double-sided metabolite, has attracted considerable attention by researchers. Its ubiquitous presence in plant metabolism and its metabolic energy economy for being assimilated contrast with its toxicity when present in high amounts in the external medium. Plant species can adopt different strategies to maintain NH4+ homeostasis, as the maximization of its compartmentalization and assimilation in organic compounds, primarily as amino acids and proteins. In the present study, we report an integrative metabolic response to ammonium nutrition of seven plant species, belonging to four different families: Gramineae (ryegrass, wheat, Brachypodium distachyon), Leguminosae (clover), Solanaceae (tomato), and Brassicaceae (oilseed rape, Arabidopsis thaliana). We use principal component analysis (PCA) and correlations among metabolic and biochemical data from 40 experimental conditions to understand the whole-plant response. The nature of main amino acids is analyzed among species, under the hypothesis that those Asn-accumulating species will show a better response to ammonium nutrition. Given the provision of carbon (C) skeletons is crucial for promotion of the nitrogen assimilation, the role of different anaplerotic enzymes is discussed in relation to ammonium nutrition at a whole-plant level. Among these enzymes, isocitrate dehydrogenase (ICDH) shows to be a good candidate to increase nitrogen assimilation in plants. Overall, metabolic adaptation of different carbon anaplerotic activities is linked with the preference to synthesize Asn or Gln in their organs. Lastly, glutamate dehydrogenase (GDH) reveals as an important enzyme to surpass C limitation during ammonium assimilation in roots, with a disparate collaboration of glutamine synthetase (GS).
Highlights
Ammonium (NH4+) ion is a common metabolite in cells with an incongruous behavior
With the exception of Arabidopsis, the fact that isocitrate dehydrogenase (ICDH) activity highly correlated with glutamine synthetase (GS) activity (Figure 5) in the multi-species representation would indicate this C enzyme is well-coordinated with N assimilation, probably to sustain the 2-OG production for the enhanced synthesis of Glu + Gln. This multi-species study shows that NH4+ accumulation and the induction of its assimilatory mechanisms preferentially occur at root level and allow excluding NH4+ from the shoots
Total content of amino acids, as primary nitrogen-reduced product, is shown as universal biomarker of ammonium metabolism in plant tissues, internal NH4+ content would reflect an imbalance between the excessive NH4+ uptake and its assimilation capacity
Summary
Ammonium (NH4+) ion is a common metabolite in cells with an incongruous behavior. In plants, NH4+ can be taken up from the soil and incorporated into carbon (C) skeletons for the organic nitrogen (N) synthesis. At whole-plant level, ammonium homeostasis can be mediated by its storage preferentially in roots (Setién et al, 2013; Vega-Mas et al, 2015) or be translocated to leaves (Sun et al, 2017), which points out to selective mechanisms of loading into the xylem and to different thresholds of ammonium sensitivity for root and leaf cells It is well-known that the ammonium toxicity thresholds are very disparate among species (Cruz et al, 2006; Esteban et al, 2016), and vary depending on environmental conditions as light intensity, atmospheric CO2 or pH (Setién et al, 2014; Vega-Mas et al, 2015; Sarasketa et al, 2016). Internal NH4+ content could be hypothesized to act as primary metabolic marker of the stress degree, related with changes in C and N metabolism
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