Rapid Ammonia Gas Transport Accounts for Futile Transmembrane Cycling Under NH3/NH4+ Toxicity in Plant Roots

Plant Physiol. 2013 Dec;163(4):1859-67. doi: 10.1104/pp.113.225961. Epub 2013 Oct 17.


Futile transmembrane NH3/NH4(+) cycling in plant root cells, characterized by extremely rapid fluxes and high efflux to influx ratios, has been successfully linked to NH3/NH4(+) toxicity. Surprisingly, the fundamental question of which species of the conjugate pair (NH3 or NH4(+)) participates in such fluxes is unresolved. Using flux analyses with the short-lived radioisotope (13)N and electrophysiological, respiratory, and histochemical measurements, we show that futile cycling in roots of barley (Hordeum vulgare) seedlings is predominately of the gaseous NH3 species, rather than the NH4(+) ion. Influx of (13)NH3/(13)NH4(+), which exceeded 200 µmol g(-1) h(-1), was not commensurate with membrane depolarization or increases in root respiration, suggesting electroneutral NH3 transport. Influx followed Michaelis-Menten kinetics for NH3 (but not NH4(+)), as a function of external concentration (Km = 152 µm, Vmax = 205 µmol g(-1) h(-1)). Efflux of (13)NH3/(13)NH4(+) responded with a nearly identical Km. Pharmacological characterization of influx and efflux suggests mediation by aquaporins. Our study fundamentally revises the futile-cycling model by demonstrating that NH3 is the major permeating species across both plasmalemma and tonoplast of root cells under toxicity conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ammonia / metabolism*
  • Ammonia / toxicity*
  • Ammonium Compounds / toxicity*
  • Biological Transport / drug effects
  • Cell Membrane / metabolism*
  • Cell Respiration / drug effects
  • Hordeum / drug effects
  • Hordeum / metabolism*
  • Hydrogen-Ion Concentration / drug effects
  • Models, Biological
  • Plant Roots / drug effects
  • Plant Roots / metabolism*
  • Seedlings / drug effects
  • Seedlings / metabolism


  • Ammonium Compounds
  • Ammonia