In comparison with nitrate nutrition, ammonium nutrition increases growth of the frostbite1 Arabidopsis mutant

Plant Cell Environ. 2015 Jan;38(1):224-37. doi: 10.1111/pce.12404. Epub 2014 Aug 13.

Abstract

Ammonium nutrition inhibits the growth of many plant species, including Arabidopsis thaliana. The toxicity of ammonium is associated with changes in the cellular redox state. The cellular oxidant/antioxidant balance is controlled by mitochondrial electron transport chain. In this study, we analysed the redox metabolism of frostbite1 (fro1) plants, which lack mitochondrial respiratory chain complex I. Surprisingly, the growth of fro1 plants increased under ammonium nutrition. Ammonium nutrition increased the reduction level of pyridine nucleotides in the leaves of wild-type plants, but not in the leaves of fro1 mutant plants. The observed higher activities of type II NADH dehydrogenases and cytochrome c oxidase in the mitochondrial electron transport chain may improve the energy metabolism of fro1 plants grown on ammonium. Additionally, the observed changes in reactive oxygen species (ROS) metabolism in the apoplast may be important for determining the growth of fro1 under ammonium nutrition. Moreover, bioinformatic analyses showed that the gene expression changes in fro1 plants significantly overlap with the changes previously observed in plants with a modified apoplastic pH. Overall, the results suggest a pronounced connection between the mitochondrial redox system and the apoplastic pH and ROS levels, which may modify cell wall plasticity and influence growth.

Keywords: ammonium syndrome; apoplast; apoplastic pH; complex I; dysfunction of mtETC; mitochondria; redox homeostasis; respiration.

MeSH terms

  • Ammonium Compounds / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism*
  • Arabidopsis / ultrastructure
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Respiration
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism
  • Energy Metabolism
  • Gene Expression Regulation, Plant*
  • Homeostasis
  • Hydrogen-Ion Concentration
  • Metabolome
  • Mitochondria / metabolism
  • Mutation
  • NADH Dehydrogenase / genetics
  • NADH Dehydrogenase / metabolism*
  • Nitrates / metabolism*
  • Oxidation-Reduction
  • Plant Leaves / genetics
  • Plant Leaves / growth & development
  • Plant Leaves / metabolism
  • Plant Leaves / ultrastructure
  • Reactive Oxygen Species / metabolism

Substances

  • Ammonium Compounds
  • Arabidopsis Proteins
  • FRO1 protein, Arabidopsis
  • Nitrates
  • Reactive Oxygen Species
  • NADH Dehydrogenase
  • Electron Transport Complex IV