Changes in the C/N balance caused by increasing external ammonium concentrations are driven by carbon and energy availabilities during ammonium nutrition in pea plants: the key roles of asparagine synthetase and anaplerotic enzymes

Abstract

An understanding of the mechanisms underlying ammonium (NH4+) toxicity in plants requires prior knowledge of the metabolic uses for nitrogen (N) and carbon (C). We have recently shown that pea plants grown at high NH4+ concentrations suffer an energy deficiency associated with a disruption of ionic homeostasis. Furthermore, these plants are unable to adequately regulate internal NH4+ levels and the cell‐charge balance associated with cation uptake. Herein we show a role for an extra‐C application in the regulation of C–N metabolism in NH4+‐fed plants. Thus, pea plants (Pisum sativum) were grown at a range of NH4+ concentrations as sole N source, and two light intensities were applied to vary the C supply to the plants. Control plants grown at high NH4+ concentration triggered a toxicity response with the characteristic pattern of C‐starvation conditions. This toxicity response resulted in the redistribution of N from amino acids, mostly asparagine, and lower C/N ratios. The C/N imbalance at high NH4+ concentration under control conditions induced a strong activation of root C metabolism and the upregulation of anaplerotic enzymes to provide C intermediates for the tricarboxylic acid cycle. A high light intensity partially reverted these C‐starvation symptoms by providing higher C availability to the plants. The extra‐C contributed to a lower C4/C5 amino acid ratio while maintaining the relative contents of some minor amino acids involved in key pathways regulating the C/N status of the plants unchanged. C availability can therefore be considered to be a determinant factor in the tolerance/sensitivity mechanisms to NH4+ nutrition in plants.

Health‐promoting compounds of broccoli (Brassica oleracea L. var. italica) plants as affected by nitrogen fertilisation in projected future climatic change environments

“…A similar dependence was observed for the total GSL levels, and a correlation between the total GSL content and C:N ratio was found at ambient ( R = 0.71) and elevated ( R 2 = 0.81) [CO 2 ], indicating that the atmospheric CO 2 enrichment enhanced the plants' carbon supply and that the increasing C:N ratio affected the GSL content . Not only the GSL content but also the AA content was modified according to the C:N ratio, with a redistribution of N from AAs such as Glu to those with lower C:N ratios, such as Asn or Arg, characteristic of high NH 4 + concentrations . De novo synthesis of Arg is related to the NO 3 − /NH 4 + ratio and has been described as the major detoxification process of NH 4 + , preventing this ion from reaching a toxic level…”

“…57,58 Not only the GSL content but also the AA content was modified according to the C:N ratio, with a redistribution of N from AAs such as Glu to those with lower C:N ratios, such as Asn or Arg, characteristic of high NH 4 + concentrations. 59 De novo synthesis of Arg is related to the NO 3 − /NH 4 + ratio and has been described as the major detoxification process of NH 4 + , preventing this ion from reaching a toxic level. 60 The observed increase in Trp with decreasing NO 3 − /NH 4 + ratio was accompanied by progressive and significant accumulation of the indolic GSLs derived from Trp.…”

CO 2 enrichment modulates ammonium nutrition in tomato adjusting carbon and nitrogen metabolism to stomatal conductance

“…In our previous studies the tomato cultivar Agora Hybrid F1 behaved as tolerant given it grew similarly with nitrate and ammonium at moderate concentrations [8]. Nevertheless, the sensitivity to ammonium nutrition for a particular species or variety depends on environmental conditions as the external N concentration [30,34] the ratio of ammonium:nitrate availability [35], other nutrients concentration [36] or light conditions [8,13]. In the present study, different growth patterns were distinguished between ammonium-and nitrate-fed tomato plants cv Agora Hybrid F1 in response to changing atmospheric CO 2 levels (800 vs 400 ppm).…”

Heme‐heme oxygenase 1 system is involved in ammonium tolerance by regulating antioxidant defence in Oryza sativa

“…These toxic effects also resulted from physiological disorders, such as the increase of photorespiration and various free amino acids, etc. (Britto & Kronzucker 2002;Nimptsch & Pflugmacher 2007;Ariz et al 2013;Li et al 2014).…”