Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana

Nat Commun. 2021 Aug 16;12(1):4944. doi: 10.1038/s41467-021-25238-7.

Abstract

Plants use nitrate, ammonium, and organic nitrogen in the soil as nitrogen sources. Since the elevated CO2 environment predicted for the near future will reduce nitrate utilization by C3 species, ammonium is attracting great interest. However, abundant ammonium nutrition impairs growth, i.e., ammonium toxicity, the primary cause of which remains to be determined. Here, we show that ammonium assimilation by GLUTAMINE SYNTHETASE 2 (GLN2) localized in the plastid rather than ammonium accumulation is a primary cause for toxicity, which challenges the textbook knowledge. With exposure to toxic levels of ammonium, the shoot GLN2 reaction produced an abundance of protons within cells, thereby elevating shoot acidity and stimulating expression of acidic stress-responsive genes. Application of an alkaline ammonia solution to the ammonium medium efficiently alleviated the ammonium toxicity with a concomitant reduction in shoot acidity. Consequently, we conclude that a primary cause of ammonium toxicity is acidic stress.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids
  • Ammonium Compounds / metabolism*
  • Ammonium Compounds / toxicity*
  • Arabidopsis / drug effects*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / metabolism
  • Glutamate-Ammonia Ligase / drug effects
  • Glutamate-Ammonia Ligase / genetics
  • Glutamate-Ammonia Ligase / metabolism*
  • Nitrates / metabolism
  • Nitrogen / metabolism
  • Plant Shoots / metabolism
  • Plastids / metabolism*

Substances

  • Amino Acids
  • Ammonium Compounds
  • Arabidopsis Proteins
  • Nitrates
  • glutamine synthetase 2
  • GLN2 protein, Arabidopsis
  • Glutamate-Ammonia Ligase
  • Nitrogen