Trehalose metabolism: from osmoprotection to signaling

Abstract

Trehalose is a non-reducing disaccharide formed by two glucose molecules. It is widely distributed in Nature and has been isolated from certain species of bacteria, fungi, invertebrates and plants, which are capable of surviving in a dehydrated state for months or years and subsequently being revived after a few hours of being in contact with water. This disaccharide has many biotechnological applications, as its physicochemical properties allow it to be used to preserve foods, enzymes, vaccines, cells etc., in a dehydrated state at room temperature. One of the most striking findings a decade ago was the discovery of the genes involved in trehalose biosynthesis, present in a great number of organisms that do not accumulate trehalose to significant levels. In plants, this disaccharide has diverse functions and plays an essential role in various stages of development, for example in the formation of the embryo and in flowering. Trehalose also appears to be involved in the regulation of carbon metabolism and photosynthesis. Recently it has been discovered that this sugar plays an important role in plant-microorganism interactions.

Keywords: abiotic stress; anhydrobiosis; arabidopsis; dehydration; drought tolerance; osmoprotectant; sugar sensing; transgenic plants; trehalose.

Figure 1.

Evolutionary history of trehalose biosynthesis. The trehalose biosynthetic pathways are present in the three domains of life tree. Phyla in bold letters show organisms that have at least one of the five routes of trehalose biosynthesis.

Figure 2.

Trehalose biosynthetic and catabolic pathways and distribution in eukaryotes and prokaryotes.

Figure 3.

The role of trehalose pathway in prokaryotes and eukaryotes. Trehalose in prokaryotes dramatically accumulates in osmotic or thermal stress conditions; it can signal from the bacteria to the plant cell stress tolerance and nitrogen and carbon metabolism. In plants, trehalose 6-phosphate (T6P) plays a central role regulating sugar metabolism and plant development. Glucose and trehalose are also important keys to several signaling and regulatory pathways and integrate external cues to adapt cells to abiotic stress, growth and development. It seems that TPS1 and ABI4 are part of the HXK1 signaling pathway. Other molecular actors in this network are the 14-3-3 proteins, which are known to interact with phosphoserine in diverse proteins including TPS; and SnRK1, which signals catabolism in starvation conditions, and is countered by T6P to induce anabolism. Thus, an important role of the trehalose biosynthesis pathway in higher plants would be the synthesis of small amounts of T6P and/or trehalose signaling molecules rather than accumulation of this latter as an osmoprotective compound.