A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose

The Suc-Tre6P nexus in plants. The figure represents the core concept of the nexus model, which postulates that Tre6P is both a signal and negative feedback regulator of Suc levels in plants, thereby helping to maintain Suc levels within an optimal range (Yadav et al., 2014). Within the nexus, an increase or decrease in Suc leads to a respective rise or fall in Tre6P levels, via changes in the relative activities of TPS and TPP. In addition to this positive circuit, there is a negative feedback loop by which any increase or decrease in Tre6P leads to an opposite change in Suc levels, via reciprocal effects on Suc production and consumption. There are Tre6P-independent and Tre6P-dependent Suc signaling pathways stemming from the core nexus. This multiplicity of Suc-signaling pathways can give rise to conflicting sugar signals in mutants where imposed changes in Tre6P lead to an opposite and inappropriate change in Suc levels. Blue arrows indicate activation, and red lines indicate inhibition.

The Suc-Tre6P nexus in source leaves. It is proposed that the core Suc-Tre6P nexus and the associated signaling pathways are adapted to meet the particular needs of individual tissues. In illuminated source leaves (A), Tre6P regulates the partitioning of photoassimilates between Suc and organic and amino acids by influencing the posttranslational regulatory status of PEPC and NR. In source leaves at night (B), Tre6P regulates transitory starch breakdown, balancing the supply of substrates for Suc synthesis with the demand for Suc from sink organs. Blue arrows indicate activation, and red lines indicate inhibition. Solid lines show experimentally demonstrated interactions, while dashed lines represent hypothetical interactions.

The Suc-Tre6P nexus in sink organs. Growing sink tissues import Suc, which is catabolized by invertases and Suc synthase (SUS) to provide carbon and energy for growth and accumulation of storage reserves. Resynthesis of Suc via Suc-phosphate synthase (SPS) and Suc-phosphate phosphatase (SPP) can occur in parallel with net Suc catabolism. Tre6P regulates consumption of Suc in Suc-importing sink organs (e.g. meristems and developing seeds), mediated in part by inhibition of SnRK1. SnRK1 is activated by low energy status, so Tre6P might also influence SnRK1 activity indirectly via effects on Suc and energy levels. It is likely that Suc consumption is also regulated in ways that are not directly dependent on SnRK1. By analogy with source leaves, Tre6P might regulate turnover of transitory starch reserves in sink organs. Any changes in hexose levels or the Suc:hexose ratio are likely to trigger other sugar signaling responses mediated by TOR, hexokinase1 (HXK1), or REGULATOR OF G-PROTEIN SIGNALING1 (RGS1). Blue arrows indicate activation, and red lines indicate inhibition. Solid lines show experimentally demonstrated interactions, while dashed lines represent hypothetical interactions.

Is synthesis of Tre6P the only function of Arabidopsis TPS1? Arabidopsis has 11 TPS genes, divided into two distinct clades: class I (AtTPS1–AtTPS4) and class II (AtTPS5–AtTPS11). Three of the class I genes, AtTPS1, AtTPS2, and AtTPS4, encode catalytically active Tre6P synthases (AtTPS3 is most likely a pseudogene). The class II genes encode TPS-like proteins with no apparent Tre6P synthase activity and their functions are largely unknown. The figure shows the spatio-temporal expression patterns of class I TPS genes in developing Arabidopsis seeds, based on data from Le et al. (2010) and visualized using the BAR eGFP browser (http://bar.utoronto.ca/; Winter et al., 2007). Arabidopsis tps1 null mutants arrest at the torpedo stage of embryogenesis, even though the expression of AtTPS2 and AtTPS4 partially overlaps with AtTPS1 expression in the peripheral and chalazal endosperms at this stage in development. This implies that tps1 mutant seeds retain some capacity to synthesize Tre6P, raising the possibility that loss of noncatalytic functions of AtTPS1 contributes to the defective phenotype of tps1 mutants.