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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

Authors

  • Idoia Ariz,

    Corresponding author
    • Instituto de Agrobiotecnología, IdAB, CSIC – Universidad Pública de Navarra – Gobierno de Navarra, Pamplona, Navarra, Spain
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  • Aaron C. Asensio,

    1. Instituto de Agrobiotecnología, IdAB, CSIC – Universidad Pública de Navarra – Gobierno de Navarra, Pamplona, Navarra, Spain
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    • Present address: FideNa (Foundation for R&D in nanotechnology), Centro Jerónimo de Ayanz, C/ Tajonar s/n, 31006 Pamplona, Navarra, Spain

  • Angel M. Zamarreño,

    1. Research and Development Department, Inabonos-Roullier Group, Polígono Arazuri-Orcoyen, Orcoyen, Navarra, Spain
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  • Jose M. García-Mina,

    1. Research and Development Department, Inabonos-Roullier Group, Polígono Arazuri-Orcoyen, Orcoyen, Navarra, Spain
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  • Pedro M. Aparicio-Tejo,

    1. Instituto de Agrobiotecnología, IdAB, CSIC – Universidad Pública de Navarra – Gobierno de Navarra, Pamplona, Navarra, Spain
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  • Jose F. Moran

    1. Instituto de Agrobiotecnología, IdAB, CSIC – Universidad Pública de Navarra – Gobierno de Navarra, Pamplona, Navarra, Spain
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Correspondence

Corresponding author,

e-mail: idoia.ariz@unavarra.es

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.

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