Glutamate dehydrogenase mediated amino acid metabolism after ammonium uptake enhances rice growth under aeration condition

Plant Cell Rep. 2020 Mar;39(3):363-379. doi: 10.1007/s00299-019-02496-w. Epub 2019 Dec 9.

Abstract

Aeration stimulates the rice growth and nitrogen (N) metabolism; in which, the glutamate accumulation limited by the glutamate dehydrogenase pathway after ammonia uptake may control root N metabolism during aeration. Increasing rhizosphere oxygen content greatly improves rice growth and biomass. To study the intrinsic mechanism involved in nitrogen (N) metabolism, a hydroponic experiment was conducted by supplying two different oxygen levels to two different rice genotypes. Compared to the hypoxia-resistant cultivar (Nip; japonica rice 'Nipponbare'), the hypoxia-sensitive cultivar (U502; upland rice 'Upland 502') presented with severe oxidative damage under the lack of aeration. However, aeration significantly reduced root oxidative damage by enhancing root antioxidant capacity and leaf photosynthesis especially in U502, and significantly increased nitrate (NO3-) and ammonia (NH4+) uptake and upregulated the expression of the genes controlling these processes. Additional NO3- was mainly incorporated into amino acids in the leaves whereas NH4+ assimilation occurred mostly in the roots. The 15N gas chromatography-mass spectrometry analysis demonstrated that aeration had no influence on the compositions of the individual amino acids derived from 15NO3- in the roots, but increased labeled glutamic acid (Glu), asparagine, γ-aminobutyric acid, and alanine in 15NH4+-treated roots. Aeration inhibited root glutamate synthetase activity but this did not inhibit 15N-Glu production from 15NH4+. In contrast, aeration upregulated isocitrate dehydrogenase and glutamate dehydrogenase. These mechanisms and soluble carbohydrates may constitute an alternative pathway for Glu production in which amino acid metabolism is enhanced after NH4+ uptake during aeration. Therefore, the rice growth-enhancing effect of aeration is closely correlated with root redox equilibrium, N uptake, and amino acid metabolism. Glutamic acid accumulation is limited by the glutamate dehydrogenase pathway after NH4+ uptake and may control root N metabolism during aeration.

Keywords: Aeration; Ammonia; Glutamate; Glutamate dehydrogenase; Glutamate synthase; Nitrate; Rice.

MeSH terms

  • Amino Acids / metabolism*
  • Ammonia / metabolism
  • Ammonium Compounds / metabolism*
  • Antioxidants / metabolism
  • Biomass
  • Carbohydrate Metabolism / drug effects
  • Gene Expression Regulation, Plant / drug effects
  • Glutamate Dehydrogenase / metabolism*
  • Glutamate Synthase (NADH) / metabolism
  • Hydrogen Peroxide / metabolism
  • Malondialdehyde / metabolism
  • Nitrogen Isotopes
  • Oryza / drug effects
  • Oryza / enzymology*
  • Oryza / genetics
  • Oryza / growth & development*
  • Oxygen / pharmacology*
  • Plant Leaves / drug effects
  • Plant Leaves / metabolism
  • Plant Roots / drug effects
  • Plant Roots / enzymology
  • Seedlings / drug effects
  • Seedlings / growth & development

Substances

  • Amino Acids
  • Ammonium Compounds
  • Antioxidants
  • Nitrogen Isotopes
  • Nitrogen-15
  • Malondialdehyde
  • Ammonia
  • Hydrogen Peroxide
  • Glutamate Synthase (NADH)
  • Glutamate Dehydrogenase
  • Oxygen