Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana

Genes for trehalose metabolism are widespread in higher plants. Insight into the physiological role of the trehalose pathway outside of resurrection plant species is lacking. To address this lack of insight, we express Escherichia coli genes for trehalose metabolism in Arabidopsis thaliana, which manipulates trehalose 6-phosphate (T6P) contents in the transgenic plants. Plants expressing otsA [encoding trehalose phosphate synthase (TPS)] accumulate T6P whereas those expressing either otsB [encoding trehalose phosphate phosphatase (TPP)] or treC [encoding trehalose phosphate hydrolase (TPH)] contain low levels of T6P. Expression of treF (encoding trehalase) yields plants with unaltered T6P content and a phenotype not distinguishable from wild type when grown on soil. The marked phenotype obtained of plants accumulating T6P is opposite to that of plants with low T6P levels obtained by expressing either TPP or TPH and consistent with a critical role for T6P in growth and development. Supplied sugar strongly inhibits growth of plants with reduced T6P content and leads to accumulation of respiratory intermediates. Remarkably, sugar improves growth of TPS expressors over wild type, a feat not previously accomplished by manipulation of metabolism. The data indicate that the T6P intermediate of the trehalose pathway controls carbohydrate utilization and thence growth via control of glycolysis in a manner analogous to that in yeast. Furthermore, embryolethal A. thaliana tps1 mutants are rescued by expression of E. coli TPS, but not by supply of trehalose, suggesting that T6P control over primary metabolism is indispensable for development.