Trehalose Mediated Growth Inhibition of Arabidopsis Seedlings Is Due to Trehalose-6-Phosphate Accumulation  

Abstract

Trehalose-6-phosphate (T6P) is required for carbon utilization during Arabidopsis development, and its absence is embryo lethal. Here we show that T6P accumulation inhibits seedling growth. Wild-type seedlings grown on 100 mM trehalose rapidly accumulate T6P and stop growing, but seedlings expressing Escherichia coli trehalose phosphate hydrolase develop normally on such medium. T6P accumulation likely results from much-reduced T6P dephosphorylation when trehalose levels are high. Metabolizable sugars added to trehalose medium rescue T6P inhibition of growth. In addition, Suc feeding leads to a progressive increase in T6P concentrations, suggesting that T6P control over carbon utilization is related to available carbon for growth. Expression analysis of genes from the Arabidopsis trehalose metabolism further supports this: Suc rapidly induces expression of trehalose phosphate synthase homolog AtTPS5 to high levels. In contrast, T6P accumulation after feeding trehalose in the absence of available carbon induces repression of genes encoding T6P synthases and expression of T6P phosphatases. To identify processes controlled by T6P, we clustered expression profile data from seedlings with altered T6P content. T6P levels correlate with expression of a specific set of genes, including the S6 ribosomal kinase ATPK19, independently of carbon status. Interestingly, Suc addition represses 15 of these genes, one of which is AtKIN11, encoding a Sucrose Non Fermenting 1 (SNF1)-related kinase known to play a role in Suc utilization.

A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis

“…It has been shown that T6P has a regulatory role in carbohydrate utilization during plant growth and development (Eastmond et al 2002;Schluepmann et al 2003Schluepmann et al , 2004van Dijken et al 2004). We have reported before that overexpression in Arabidopsis of its AtTPS1 homolog leads to a glucose and abscisic-acid insensitive phenotype and to stress tolerance, suggesting that trehalose metabolism plays an important role in signaling gene regulation to integrate environmental and metabolic cues during vegetative development (Avonce et al 2004).…”

“…Overexpression of the Arabidopsis AtTPS1 gene in its homologous background does not produce such drastic eVects but still there is a delay in Xowering (Avonce et al 2004). The accumulation of higher levels of T6P are probably causing these defects since T6P has turned out to be a Wne-tuned signaling molecule that has a regulatory role in carbohydrate utilization during plant growth, embryo development and Xowering (Eastmond et al 2002;Schluepmann et al 2003Schluepmann et al , 2004van Dijken et al 2004). Therefore, it was decided to construct a bifunctional TPS-TPP enzyme, which while maintaining trehalose biosynthesis capacity would not lead to excess accumulation of free T6P in the cytosol avoiding undesired secondary eVects in the transgenic plants.…”

Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase

“…Although the sucrose-related response required SnRK1 and was independent of changes in metabolites, glucoserelated activation of AGPase was independent of SnRK1 and involved a strong increase in hexose-P levels (16). To investigate a possible role of trehalose metabolism in these signaling events, tuber slices from wild-type and SnRK1 antisense lines were incubated with 100 mM trehalose for 1 h. It has been shown in Arabidopsis that feeding trehalose leads to an increase in its precursor T6P (23). Redox activation of AGPase was assessed Fig.…”

“…Studies on transgenic lines overexpressing TPS or TPP identified T6P as essential for sugar utilization and growth in Arabidopsis plants (22). External feeding of trehalose or sucrose to wild-type Arabidopsis led to an increase in T6P level within 30 min or 2 h, respectively, indicating a link between sugars and T6P that responds within a short time frame (23). However, the sites of T6P action remain largely unknown.…”

Overexpression of the Trehalase Gene AtTRE1 Leads to Increased Drought Stress Tolerance in Arabidopsis and Is Involved in Abscisic Acid-Induced Stomatal Closure

“…In most cases, the plants exhibited aberrant phenotypes such as stunted roots, lancet-shaped leaves, and growth retardation (Romero et al, 1997;Cortina and Culianez-Macia, 2005). The undesired abnormalities in these plants were ascribed to altered levels of T6P, perturbing the developmental processes influenced by this important signal metabolite (Eastmond et al, 2003;Schluepmann et al, 2003Schluepmann et al, , 2004. Plants with improved stress tolerance but no obvious morphological defects were obtained by introducing bifunctional TPS-TPP constructs (Garg et al, 2002;Karim et al, 2007;Miranda et al, 2007), by placing the introduced TPS genes under the control of droughtinducible or tissue-specific promoters (Garg et al, 2002;Karim et al, 2007), or by overexpressing the plant endogenous TPS1 in Arabidopsis (Avonce et al, 2004) and rice (Oryza sativa; Li et al, 2011).…”