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

Abstract

Trehalose 6-phosphate (Tre6P), the intermediate of trehalose biosynthesis, is an essential signal metabolite in plants, linking growth and development to carbon status. The Suc-Tre6P nexus model postulates that Tre6P is both a signal and negative feedback regulator of Suc levels, forming part of a mechanism to maintain Suc levels within an optimal range and functionally comparable to the insulin-glucagon system for regulating blood Glc levels in animals. The target range and sensitivity of the Tre6P-Suc feedback control circuit can be adjusted according to the cell type, developmental stage, and environmental conditions. In source leaves, Tre6P modulates Suc levels by affecting Suc synthesis, whereas in sink organs it regulates Suc consumption. In illuminated leaves, Tre6P influences the partitioning of photoassimilates between Suc, organic acids, and amino acids via posttranslational regulation of phosphoenolpyruvate carboxylase and nitrate reductase. At night, Tre6P regulates the remobilization of leaf starch reserves to Suc, potentially linking starch turnover in source leaves to carbon demand from developing sink organs. Use of Suc for growth in developing tissues is strongly influenced by the antagonistic activities of two protein kinases: SUC-NON-FERMENTING-1-RELATED KINASE1 (SnRK1) and TARGET OF RAPAMYCIN (TOR). The relationship between Tre6P and SnRK1 in developing tissues is complex and not yet fully resolved, involving both direct and indirect mechanisms, and positive and negative effects. No direct connection between Tre6P and TOR has yet been described. The roles of Tre6P in abiotic stress tolerance and stomatal regulation are also discussed.

Figure 1.

Tre6P signaling in plants. Tre6P is the phosphorylated intermediate of trehalose biosynthesis. It is a signal of Suc status in plants and influences many metabolic and developmental processes, either directly (green boxes) or indirectly as the precursor of trehalose (red boxes). Both Tre6P and trehalose are implicated in regulation of stomatal conductance (blue box). The central image is based on a drawing downloaded from www-plb.ucdavis.edu/labs/lucas/fig4.jpg.

Figure 2.

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.

Figure 3.

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.

Figure 4.

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.

Figure 5.

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.

Figure 6.

Trehalose metabolism in guard cells and regulation of stomatal conductance. AtTPS1, AtTPPG, and AtTRE1 are particularly highly expressed in Arabidopsis guard cells, with their expression being up-regulated by ABA. The AtTPPG and AtTRE1 gene promoters contain motifs that implicate MYB and WRKY family transcription factors in their regulation by ABA. The stomata in tppg and tre1 null mutants are insensitive to ABA, rendering the plants less tolerant of water deficit (Vandesteene et al., 2012; Van Houtte et al., 2013). ABA sensitivity is compromised by NO, whose production is dependent on nitrate reductase (NR; Chen et al., 2016). Upon illumination, the starch in guard cells is rapidly degraded, providing substrates for synthesis of malate that helps drive stomatal opening (Horrer et al., 2016). In Arabidopsis mesophyll cells, high [Tre6P] leads to posttranslational activation of NR and phosphoenolpyruvate carboxylase (PEPC) during the day and inhibition of transitory starch degradation at night (Martins et al., 2013; Figueroa et al., 2016), suggesting that the degradation of starch and synthesis of malate might also be regulated by Tre6P.