Nitric oxide induces monosaccharide accumulation through enzyme S-nitrosylation

Plant Cell Environ. 2017 Sep;40(9):1834-1848. doi: 10.1111/pce.12989. Epub 2017 Jul 5.

Abstract

Nitric oxide (NO) is extensively involved in various growth processes and stress responses in plants; however, the regulatory mechanism of NO-modulated cellular sugar metabolism is still largely unknown. Here, we report that NO significantly inhibited monosaccharide catabolism by modulating sugar metabolic enzymes through S-nitrosylation (mainly by oxidizing dihydrolipoamide, a cofactor of pyruvate dehydrogenase). These S-nitrosylation modifications led to a decrease in cellular glycolysis enzymes and ATP synthase activities as well as declines in the content of acetyl coenzyme A, ATP, ADP-glucose and UDP-glucose, which eventually caused polysaccharide-biosynthesis inhibition and monosaccharide accumulation. Plant developmental defects that were caused by high levels of NO included delayed flowering time, retarded root growth and reduced starch granule formation. These phenotypic defects could be mediated by sucrose supplementation, suggesting an essential role of NO-sugar cross-talks in plant growth and development. Our findings suggest that molecular manipulations could be used to improve fruit and vegetable sweetness.

Keywords: monosaccharide catabolism; polysaccharide synthesis; starch granule.

MeSH terms

  • ATP Synthetase Complexes / metabolism
  • Adenosine Diphosphate Glucose / metabolism
  • Adenosine Triphosphate / metabolism
  • Arabidopsis / drug effects
  • Arabidopsis / enzymology
  • Arabidopsis / metabolism*
  • Glycolysis / drug effects
  • Monosaccharides / metabolism*
  • Mutation / genetics
  • Nitric Oxide / pharmacology*
  • Nitrosation
  • Oxidation-Reduction
  • Phenotype
  • Plant Development / drug effects
  • Plant Roots / anatomy & histology
  • Plant Roots / drug effects
  • Plant Roots / metabolism
  • Plant Shoots / drug effects
  • Plant Shoots / metabolism
  • Pyruvate Dehydrogenase Complex / metabolism
  • Solubility
  • Starch / metabolism
  • Sucrose / pharmacology
  • Thioctic Acid / analogs & derivatives
  • Thioctic Acid / metabolism
  • Uridine Diphosphate Glucose / metabolism

Substances

  • Monosaccharides
  • Pyruvate Dehydrogenase Complex
  • Adenosine Diphosphate Glucose
  • Nitric Oxide
  • Sucrose
  • Thioctic Acid
  • dihydrolipoic acid
  • Adenosine Triphosphate
  • Starch
  • ATP Synthetase Complexes
  • Uridine Diphosphate Glucose