The Role of Trehalose Metabolism in Chloroplast Development and Leaf Senescence

Abstract

Trehalose (α-D-glucopyranosyl-(1,1)-α-D-glucopyranoside) is a non-reducing disaccharide that acts as a storage carbohydrate, transport sugar and stress protectant in microorganisms and invertebrate animals. In plants, trehalose synthesis is catalyzed by trehalose 6-phosphate synthase (TPS) followed by trehalose 6-phosphate phosphatase (TPP). Despite activity of this biosynthetic pathway, trehalose does not usually accumulate to large amounts in plant tissues. The low content of trehalose indicates that the conventional role as carbon source or compatible solute is unlikely in plants. Instead, sucrose has assumed this role, while trehalose metabolism mainly appears to fulfill a signaling function. Work with transgenic plants has revealed a role of trehalose 6-phosphate (T6P), the precursor of trehalose in the biosynthetic pathway, as signal for high availability of carbon, in particular in the form of sucrose. While T6P is likely to be synthesized in the cytosol, it stimulates starch synthesis in the chloroplasts. In seedlings, T6P activates pathways for the synthesis of amino acids, proteins and nucleotides, but also represses photosynthesis genes. These changes in gene expression can be explained by inhibition of the activity of sucrose non-fermenting-1-related protein kinase 1 (SnRK1) by T6P in growing tissues. Since SnRK1 serves as an integrator of transcriptional networks in starvation signaling, the inhibitory effect of T6P is consistent with its role as a high carbon signal. High T6P also improves sucrose utilization and growth of seedlings. In mature leaves, however, T6P does not inhibit SnRK1. Although photosynthesis on a leaf area basis is enhanced in response to high T6P content, altered leaf shape restricts overall plant carbon gain and growth. Transgenic plants expressing genes for trehalose synthesis generally show improved photosynthetic function during stress. More recently, enhanced stress tolerance, while avoiding negative effects of T6P on leaf development, has been achieved by expressing TPS/TPP fusion constructs or by targeting trehalose synthesis to the chloroplast. This suggests a protective role of T6P and/or trehalose in the chloroplast, although trehalose content was probably too low to act as a compatible solute. Trehalose metabolism also affects reproductive plant development, including a role of T6P in floral initiation as well as in the regulation of leaf senescence. Development of photosynthesis is therefore regulated by trehalose metabolism in many different ways, with T6P typically acting as a signal for high carbon availability.