Ammonium Accumulation Caused by Reduced Tonoplast V-ATPase Activity in Arabidopsis thaliana

Int J Mol Sci. 2020 Dec 22;22(1):2. doi: 10.3390/ijms22010002.

Abstract

Plant vacuoles are unique compartments that play a critical role in plant growth and development. The vacuolar H+-ATPase (V-ATPase), together with the vacuolar H+-pyrophosphatase (V-PPase), generates the proton motive force that regulates multiple cell functions and impacts all aspects of plant life. We investigated the effect of V-ATPase activity in the vacuole on plant growth and development. We used an Arabidopsisthaliana (L.) Heynh. double mutant, vha-a2 vha-a3, which lacks two tonoplast-localized isoforms of the membrane-integral V-ATPase subunit VHA-a. The mutant is viable but exhibits impaired growth and leaf chlorosis. Nitrate assimilation led to excessive ammonium accumulation in the shoot and lower nitrogen uptake, which exacerbated growth retardation of vha-a2 vha-a3. Ion homeostasis was disturbed in plants with missing VHA-a2 and VHA-a3 genes, which might be related to limited growth. The reduced growth and excessive ammonium accumulation of the double mutant was alleviated by potassium supplementation. Our results demonstrate that plants lacking the two tonoplast-localized subunits of V-ATPase can be viable, although with defective growth caused by multiple factors, which can be alleviated by adding potassium. This study provided a new insight into the relationship between V-ATPase, growth, and ammonium accumulation, and revealed the role of potassium in mitigating ammonium toxicity.

Keywords: ammonium; ion homeostasis; nitrate; potassium; proton pump; vacuole.

MeSH terms

  • Ammonium Compounds / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Plant
  • Homeostasis / drug effects
  • Homeostasis / genetics
  • Inorganic Pyrophosphatase / genetics
  • Inorganic Pyrophosphatase / metabolism
  • Ion Transport / drug effects
  • Ion Transport / genetics
  • Mutation
  • Nitrogen / metabolism
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / metabolism
  • Plant Shoots / genetics
  • Plant Shoots / growth & development
  • Plant Shoots / metabolism
  • Potassium / pharmacology
  • Proton-Motive Force
  • Vacuolar Proton-Translocating ATPases / genetics
  • Vacuolar Proton-Translocating ATPases / metabolism*
  • Vacuoles / genetics
  • Vacuoles / metabolism*

Substances

  • Ammonium Compounds
  • Arabidopsis Proteins
  • Vacuolar Proton-Translocating ATPases
  • Inorganic Pyrophosphatase
  • Nitrogen
  • Potassium