title: Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability.
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.
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Carlos M
authors.initials: CM
authors.lastname: Figueroa
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Regina
authors.initials: R
authors.lastname: Feil
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Hirofumi
authors.initials: H
authors.lastname: Ishihara
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Mutsumi
authors.initials: M
authors.lastname: Watanabe
authors.affiliation: Department of Biology, Institute of Agricultural Sciences, ETH Zurich, Zurich, 8092, Switzerland.
authors.forename: Katharina
authors.initials: K
authors.lastname: Kölling
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Ursula
authors.initials: U
authors.lastname: Krause
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Melanie
authors.initials: M
authors.lastname: Höhne
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Beatrice
authors.initials: B
authors.lastname: Encke
authors.affiliation: Department of Biology and Department of Biomedical and Molecular Sciences, Queen's University, Kingston, Ontario, K7L 3N6, Canada.
authors.forename: William C
authors.initials: WC
authors.lastname: Plaxton
authors.affiliation: Department of Biology, Institute of Agricultural Sciences, ETH Zurich, Zurich, 8092, Switzerland.
authors.forename: Samuel C
authors.initials: SC
authors.lastname: Zeeman
authors.affiliation: Department of Plant Systems Biology, University of Hohenheim, Stuttgart, 70593, Germany.
authors.forename: Zhi
authors.initials: Z
authors.lastname: Li
authors.affiliation: Department of Plant Systems Biology, University of Hohenheim, Stuttgart, 70593, Germany.
authors.forename: Waltraud X
authors.initials: WX
authors.lastname: Schulze
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Rainer
authors.initials: R
authors.lastname: Hoefgen
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: Mark
authors.initials: M
authors.lastname: Stitt
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, 14476, Germany.
authors.forename: John E
authors.initials: JE
authors.lastname: Lunn
mesh_terms: D000596:Amino Acids / Q000378:metabolism; D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics; D002244:Carbon / Q000378:metabolism*; D004926:Escherichia coli / Q000201:enzymology / Q000235:genetics; D015870:Gene Expression; D005964:Glucosyltransferases / Q000235:genetics / Q000378:metabolism*; D050901:Nitrate Reductase / Q000235:genetics / Q000378:metabolism*; D009584:Nitrogen / Q000378:metabolism; D010730:Phosphoenolpyruvate Carboxylase / Q000235:genetics / Q000378:metabolism*; D010766:Phosphorylation; D030821:Plants, Genetically Modified; D011499:Protein Processing, Post-Translational; D013395:Sucrose / Q000031:analogs & derivatives / Q000378:metabolism; D013403:Sugar Phosphates / Q000378:metabolism*; D014199:Trehalose / Q000031:analogs & derivatives* / Q000378:metabolism; D054875:Ubiquitination
chemical_list: D000596:Amino Acids; D013403:Sugar Phosphates; C535046:sucrose-6-phosphate; C082722:trehalose-6-phosphate; D013395:Sucrose; D002244:Carbon; D014199:Trehalose; D050901:Nitrate Reductase; D005964:Glucosyltransferases; C023180:trehalose-6-phosphate synthase; D010730:Phosphoenolpyruvate Carboxylase; D009584:Nitrogen
keywords: Arabidopsis thaliana [L.] Heynh.; nitrate reductase; phosphoenolpyruvate carboxylase; protein phosphorylation; sucrose; trehalose-6-phosphate synthase; ubiquitination