Sugar metabolism and the plant target of rapamycin kinase: a sweet operaTOR?

Abstract

In eukaryotes, the ubiquitous TOR (target of rapamycin) kinase complexes have emerged as central regulators of cell growth and metabolism. The plant TOR complex 1 (TORC1), that contains evolutionary conserved protein partners, has been shown to be implicated in various aspects of C metabolism. Indeed Arabidopsis lines affected in the expression of TORC1 components show profound perturbations in the metabolism of several sugars, including sucrose, starch, and raffinose. Metabolite profiling experiments coupled to transcriptomic analyses of lines affected in TORC1 expression also reveal a wider deregulation of primary metabolism. Moreover recent data suggest that the kinase activity of TORC1, which controls biological outputs like mRNA translation or autophagy, is directly regulated by soluble sugars.

Keywords: TOR serine-threonine kinases; myo-inositol-1-phosphate synthase; raffinose; starch; target of rapamycin.

FIGURE 1

The roles of theTOR kinase in the regulation of C metabolism. (A) Summary of the cross-talk between the TORC1 signaling pathway and the sugar metabolism. Glucose seems to induce TOR activity, which in turn activates glycolysis and raffinose synthesis in response to stresses. Conversely TOR represses the synthesis of reserve molecules. Animal reserve compounds are in red, plant ones are in green. Activation is shown by arrows. (B) Accumulation of starch following inactivation of the TORC1 complex in percentage of the control wild-type (WT). The effect of the inactivation of the TORC1 component LST8 on starch accumulation was investigated in insertion mutants. Results from the analysis of lst8 mutants are from Moreau et al. (2012) and are compared to the corresponding control WT (Col8). A time-course experiment shows the accumulation of starch following inactivation of TOR by ethanol-inducible RNAi (24–72 hours (h) after ethanol induction; Deprost et al., 2007). The 6 days (6d) point is from Caldana et al. (2013) using estradiol-inducible amiRNA lines.

FIGURE 2

Overview of the raffinose synthesis pathway and of its relationship with the sucrose and starch synthesis pathways. This figure shows that glucose 6-phosphate (Glc6P) can be used either for the synthesis of starch in chloroplasts or for the synthesis of sucrose or myo-inositol and raffinose in the cytosol. After TOR inactivation, or mutations in the TORC1 components RAPTOR and LST8, an accumulation of starch and sucrose was observed together with a decrease in the synthesis of raffinose in stress conditions. This suggests TOR inactivation triggers a redirection of C fluxes toward starch and sucrose for, respectively, storage and export. Pgm, phosphoglucomutase; StSynt, starch synthase; AGPase, ADPglucose pyrophosphorylase; UGPase, UDPglucose pyrophosphorylase; SucSynt, sucrose synthase; MIPS, myo-inositol 3-phosphate synthase; Ins(3P), myo-inositol (3 phosphate); InsPase, inositol monophosphate phosphatase; PtdIns, phosphatidylinositol; UDPGlcA, UDP-glucuronic acid; Gol(Synt), galactinol (synthase); Raf(Synt), raffinose (synthase).