Trehalose Metabolites in Arabidopsis—elusive, active and central

Abstract

Trehalose is an alpha,alpha-1,1-linked glucose disaccharide. In plants, trehalose is synthesized in two steps. Firstly, trehalose-6-phosphate synthase (TPS) converts UDP-glucose and glucose-6-phosphate to trehalose-6-phosphate (T6P); secondly, T6P-phosphatase (TPP) converts T6P into trehalose and Pi. Trehalose is further cleaved into glucose by trehalase. In extracts of most plants, including Arabidopsis, levels of both trehalose and T6P are low, nearing detection limits, and this has delayed research into their function. Trehalose is transported widely in plants, but transport of T6P is not thought to occur except possibly at the subcellular level. Feeding trehalose to Arabidopsis seedlings alters carbon allocation with massive starch accumulation in cotyledons and leaves and absence of starch and growth in shoot and root apices.The Arabidopsis genome has experienced extensive radiation of genes likely encoding enzymes of T6P metabolism: 4 and 10 genes are found with homology to TPS and TPP respectively and 7 genes are found with homology to both TPS and TPP. Complementation of Saccharomyces cerevisiae mutants has shown that AtTPS1, AtTPPA and AtTPPB are functional enzymes. In contrast just a single gene encoding a protein with trehalase activity has been found. Whilst most TPS proteins appear cytosolic, strikingly, some TPPs appear targeted to chloroplasts; trehalase on the other hand is extracellular. Transporters of trehalose and T6P have yet to be described. Arabidopsis tps1 mutants are embryo lethal and results suggest that T6P is essential for several other steps in development including root growth and floral transition. Accordingly, altering T6P content has a profound effect on plant habitus and impacts metabolite profiles, sugar utilization and photosynthesis. These large effects have hindered dissection of cause and effect. In contrast, plants with large alterations in sucrose-6-phosphate concentrations are indistinguishable from wild type, suggesting very different functions for these compounds. Recently, T6P at low micromolar concentrations has been shown in vitro and in vivo to inhibit SnRK1 of the SNF1/AMPK group of protein kinases. This supports a function for T6P as a sugar signaling molecule integrating metabolism and development in plants in relation to carbon supply.Genetic engineering of Arabidopsis as well as tobacco, potato and rice with TPS or TPS/TPP protein fusions reveals that trehalose metabolism also mediates multiple abiotic stress tolerances. Trehalose applications also mediate biotic stress resistances. Both Escherichia coli and Saccharomyces cerevisiae TPS/TPP protein fusions can be used to engineer stress tolerance suggesting that metabolites rather than proteins of the trehalose pathway are key stress tolerance elicitors. Results underscore the central role of trehalose metabolites in integrating carbon metabolism and stress responses with plant development.

Inhibition of SNF1-Related Protein Kinase1 Activity and Regulation of Metabolic Pathways by Trehalose-6-Phosphate

“…The distribution of T6P between cell types is not yet known, and current estimates of T6P concentrations represent an average of all cells. Local concentrations of T6P higher than those predicted from measurements of whole seedling extracts are likely, given that expression patterns of trehalose pathway genes are strongly cell specific, for example, the TPP gene responsible for RAMOSA3 (Satoh-Nagasawa et al, 2006) and TPS and TPP genes in root cells (Birnbaum et al, 2003;Brady et al, 2007;Schluepmann and Paul, 2009).…”

Comprehensive Dissection of Spatiotemporal Metabolic Shifts in Primary, Secondary, and Lipid Metabolism during Developmental Senescence in Arabidopsis

“…Of particular interest might be the accumulation of trehalose during leaf senescence. In plants, trehalose is produced in a two-step biochemical reaction involving trehalose 6-phosphate (T6P) synthase, which converts UDP-Glc and Glc-6-P to T6P, and T6P phosphatase, which hydrolyzes T6P to trehalose (Eastmond and Graham, 2003;Paul et al, 2008;Schluepmann and Paul, 2009). T6P has been identified as a signaling molecule for high carbon availability and to be involved in the regulation of a number of developmental processes in plants (Paul et al, 2008;Schluepmann et al, 2012).…”

TANG1, Encoding a Symplekin_C Domain-Contained Protein, Influences Sugar Responses in Arabidopsis

“…Trehalose metabolism and signaling have emerged as centrally important mechanisms controlling sugar responses and growth Tsai and Gazzarrini, 2014). Although present at very low levels, trehalose-6-phosphate (T6P) plays an essential role in the coordination of metabolism and development in response to carbon availability and stress (Avonce et al, 2004;Schluepmann et al, 2004Schluepmann et al, , 2012Paul et al, 2008;Primavesi et al, 2008;Schluepmann and Paul, 2009;Wahl et al, 2013). T6P suppresses the activity of SnRK1 in monocots and dicots, indicating that the function of T6P may be conserved in plants (Zhang et al, 2009;Delatte et al, 2011;Martínez-Barajas et al, 2011;Nunes et al, 2013).…”