The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P

J Exp Bot. 2014 Mar;65(4):1051-68. doi: 10.1093/jxb/ert457. Epub 2014 Jan 13.

Abstract

Trehalose 6-phosphate (Tre6P), the intermediate of trehalose biosynthesis, has a profound influence on plant metabolism, growth, and development. It has been proposed that Tre6P acts as a signal of sugar availability and is possibly specific for sucrose status. Short-term sugar-feeding experiments were carried out with carbon-starved Arabidopsis thaliana seedlings grown in axenic shaking liquid cultures. Tre6P increased when seedlings were exogenously supplied with sucrose, or with hexoses that can be metabolized to sucrose, such as glucose and fructose. Conditional correlation analysis and inhibitor experiments indicated that the hexose-induced increase in Tre6P was an indirect response dependent on conversion of the hexose sugars to sucrose. Tre6P content was affected by changes in nitrogen status, but this response was also attributable to parallel changes in sucrose. The sucrose-induced rise in Tre6P was unaffected by cordycepin but almost completely blocked by cycloheximide, indicating that de novo protein synthesis is necessary for the response. There was a strong correlation between Tre6P and sucrose even in lines that constitutively express heterologous trehalose-phosphate synthase or trehalose-phosphate phosphatase, although the Tre6P:sucrose ratio was shifted higher or lower, respectively. It is proposed that the Tre6P:sucrose ratio is a critical parameter for the plant and forms part of a homeostatic mechanism to maintain sucrose levels within a range that is appropriate for the cell type and developmental stage of the plant.

Keywords: Arabidopsis thaliana; signalling; sucrose; translation; trehalose-6-phosphate; trehalose-phosphate phosphatase; trehalose-phosphate synthase..

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / drug effects
  • Arabidopsis / enzymology
  • Arabidopsis / physiology*
  • Cycloheximide / pharmacology
  • Deoxyadenosines / pharmacology
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Gene Expression
  • Gene Expression Regulation, Plant*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Hexoses / metabolism
  • Oxidation-Reduction
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism
  • Plants, Genetically Modified
  • Seedlings / drug effects
  • Seedlings / enzymology
  • Seedlings / physiology
  • Sensitivity and Specificity
  • Signal Transduction*
  • Sucrose / metabolism*
  • Sugar Phosphates / metabolism*
  • Trehalose / analogs & derivatives*
  • Trehalose / metabolism

Substances

  • Deoxyadenosines
  • Escherichia coli Proteins
  • Hexoses
  • Sugar Phosphates
  • trehalose-6-phosphate
  • Sucrose
  • Cycloheximide
  • Trehalose
  • Glucosyltransferases
  • trehalose-6-phosphate synthase
  • OtsB protein, E coli
  • Phosphoric Monoester Hydrolases
  • cordycepin