Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability

Plant J. 2016 Feb;85(3):410-23. doi: 10.1111/tpj.13114.

Abstract

Trehalose 6-phosphate (Tre6P) is an essential signal metabolite in plants, linking growth and development to carbon metabolism. The sucrose-Tre6P nexus model postulates that Tre6P acts as both a signal and negative feedback regulator of sucrose levels. To test this model, short-term metabolic responses to induced increases in Tre6P levels were investigated in Arabidopsis thaliana plants expressing the Escherichia coli Tre6P synthase gene (otsA) under the control of an ethanol-inducible promoter. Increased Tre6P levels led to a transient decrease in sucrose content, post-translational activation of nitrate reductase and phosphoenolpyruvate carboxylase, and increased levels of organic and amino acids. Radio-isotope ((14)CO2) and stable isotope ((13)CO2) labelling experiments showed no change in the rates of photoassimilate export in plants with elevated Tre6P, but increased labelling of organic acids. We conclude that high Tre6P levels decrease sucrose levels by stimulating nitrate assimilation and anaplerotic synthesis of organic acids, thereby diverting photoassimilates away from sucrose to generate carbon skeletons and fixed nitrogen for amino acid synthesis. These results are consistent with the sucrose-Tre6P nexus model, and implicate Tre6P in coordinating carbon and nitrogen metabolism in plants.

Keywords: Arabidopsis thaliana [L.] Heynh.; nitrate reductase; phosphoenolpyruvate carboxylase; protein phosphorylation; sucrose; trehalose-6-phosphate synthase; ubiquitination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / metabolism
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Carbon / metabolism*
  • Escherichia coli / enzymology
  • Escherichia coli / genetics
  • Gene Expression
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism*
  • Nitrate Reductase / genetics
  • Nitrate Reductase / metabolism*
  • Nitrogen / metabolism
  • Phosphoenolpyruvate Carboxylase / genetics
  • Phosphoenolpyruvate Carboxylase / metabolism*
  • Phosphorylation
  • Plants, Genetically Modified
  • Protein Processing, Post-Translational
  • Sucrose / analogs & derivatives
  • Sucrose / metabolism
  • Sugar Phosphates / metabolism*
  • Trehalose / analogs & derivatives*
  • Trehalose / metabolism
  • Ubiquitination

Substances

  • Amino Acids
  • Sugar Phosphates
  • sucrose-6-phosphate
  • trehalose-6-phosphate
  • Sucrose
  • Carbon
  • Trehalose
  • Nitrate Reductase
  • Glucosyltransferases
  • trehalose-6-phosphate synthase
  • Phosphoenolpyruvate Carboxylase
  • Nitrogen