Abstract
Nitrate (NO3–) and ammonium (NH4+) are prevalent nitrogen (N) sources for plants. Although NH4+ should be the preferred form of N from the energetic point of view, ammonium nutrition often exhibits adverse effects on plant physiological functions and induces an important growth-limiting stress referred as ammonium syndrome. The effective incorporation of NH4+ into amino acid structures requires high activity of the mitochondrial tricarboxylic acid cycle and the glycolytic pathway. An unavoidable consequence of glycolytic metabolism is the production of methylglyoxal (MG), which is very toxic and inhibits cell growth in all types of organisms. Here, we aimed to investigate MG metabolism in Arabidopsis thaliana plants grown on NH4+ as a sole N source. We found that changes in activities of glycolytic enzymes enhanced MG production and that markedly elevated MG levels superseded the detoxification capability of the glyoxalase pathway. Consequently, the excessive accumulation of MG was directly involved in the induction of dicarbonyl stress by introducing MG-derived advanced glycation end products (MAGEs) to proteins. The severe damage to proteins was not within the repair capacity of proteolytic enzymes. Collectively, our results suggest the impact of MG (mediated by MAGEs formation in proteins) in the contribution to NH4+ toxicity symptoms in Arabidopsis.
Highlights
Plants acquire inorganic nitrogen (N) mainly as nitrate (NO3−) and ammonium (NH4+)
NH4+ is a toxic compound, it does not accumulate in plant cells to levels that may be dangerous for cell functioning (Britto and Kronzucker, 2002), as it is efficiently incorporated into amino acid structures due to glutamine (Gln) synthetase (GS) activity coupled with glutamine:2-oxoglutarate (2-OG) aminotransferase (GOGAT) activity in the GS-GOGAT cycle
The activity of PPi-dependent PFK was undetectable in the leaf extracts of NO3−-grown plants, but Arabidopsis thaliana grown under long-term ammonium nutrition exhibit severe growth inhibition (Figure 1) to our previous observations (Podgórska et al, 2013) and as it was reported for various plant species such as tobacco and cucumber (Walch-Liu et al, 2000; Roosta and Schjoerring, 2007; Hachiya et al, 2012)
Summary
Plants acquire inorganic nitrogen (N) mainly as nitrate (NO3−) and ammonium (NH4+). For many plants, the preferred form of N is NO3−, even though it must be reduced to NH4+ in energetically expensive reactions before assimilation, whereas the NH4+ oxidation state eliminates the need for reduction in the cell (Salsac et al, 1987). Excess NH4+ in the soil leads to severe growth retardation and other toxicity symptoms in many plants commonly referred to as ammonium syndrome (Britto and Kronzucker, 2013). NH4+ is a toxic compound, it does not accumulate in plant cells to levels that may be dangerous for cell functioning (Britto and Kronzucker, 2002), as it is efficiently incorporated into amino acid structures due to glutamine (Gln) synthetase (GS) activity coupled with glutamine:2-oxoglutarate (2-OG) aminotransferase (GOGAT) activity in the GS-GOGAT cycle. The production of MG has been estimated to be approximately 0.1–0.4% of the glycolytic flux (Thornalley, 1991), but it varies based on the organism, tissue, cell metabolism, and physiological conditions (Allaman et al, 2015). MG is produced in different metabolic pathways such as amino acid catabolism and lipid peroxidation (Allaman et al, 2015)
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