Abstract

The non-reducing disaccharide trehalose is widely distributed among various organisms. It plays a crucial role as an instant source of energy, being the major blood sugar in insects. In addition, it helps countering abiotic stresses. Trehalose synthesis in insects and other invertebrates is thought to occur via the trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) pathways. In many insects, the TPP gene has not been identified, whereas multiple TPS genes that encode proteins harboring TPS/OtsA and TPP/OtsB conserved domains have been found and cloned in the same species. The function of the TPS gene in insects and other invertebrates has not been reviewed in depth, and the available information is quite fragmented. The present review discusses the current understanding of the trehalose synthesis pathway, TPS genetic architecture, biochemistry, physiological function, and potential sensitivity to insecticides. We note the variability in the number of TPS genes in different invertebrate species, consider whether trehalose synthesis may rely only on the TPS gene, and discuss the results of in vitro TPS overexpression experiment. Tissue expression profile and developmental characteristics of the TPS gene indicate that it is important in energy production, growth and development, metamorphosis, stress recovery, chitin synthesis, insect flight, and other biological processes. We highlight the molecular and biochemical properties of insect TPS that make it a suitable target of potential pest control inhibitors. The application of trehalose synthesis inhibitors is a promising direction in insect pest control because vertebrates do not synthesize trehalose; therefore, TPS inhibitors would be relatively safe for humans and higher animals, making them ideal insecticidal agents without off-target effects.

Highlights

  • Reviewed by: Hans Uwe Dahms, Kaohsiung Medical University, Taiwan Jean-René Martin, CNRS, Neurobiology & Development (N&D), UPR-3294, France

  • The application of trehalose synthesis inhibitors is a promising direction in insect pest control because vertebrates do not synthesize trehalose; trehalose-6-phosphate synthase (TPS) inhibitors would be relatively safe for humans and higher animals, making them ideal insecticidal agents without off-target effects

  • How does trehalose synthesis proceed in invertebrates and is there another pathway in addition to the TPS/trehalose-6-phosphate phosphatase (TPP) pathway? Is the presence of just the TPS gene sufficient for trehalose synthesis because the encoded protein has both TPS and TPP domains? Do trehalose synthesis pathways vary between different insects? In this review, we summarize and discuss the current knowledge of the invertebrate trehalose synthesis pathway; the cloning and expression of the underlying genes identified so far; their role in development, stress conditions, and chitin metabolism regulation

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Summary

TREHALOSE AND ITS FUNCTION IN INVERTEBRATES

Trehalose is a non-reducing disaccharide in which two glycosyl moieties are linked together by an α,α-1,1 bond (Elbein et al, 2003; Bansal et al, 2013). Several approaches have been applied to study the trehalose synthesis genes TPS and TPP Their special functions in molecular mechanisms underlying different stresses and even in the regulation of chitin synthesis have been described in insects and other invertebrates (Chen et al, 2002, 2003; Tang et al, 2010; Chen and Zhang, 2015; Shi et al, 2016; Xiong et al, 2016; Yang et al, 2017), taking advantage of their ability to adapt to stress conditions (Chen and Haddad, 2004; Qin et al, 2012; Tang et al, 2014b; Guo et al, 2015). We point out the knowledge gaps that need to be filled, especially regarding future pest control by using inhibitors of trehalose synthesis, considering the absence of TPS in vertebrates

GENETIC ARCHITECTURE
TPS Gene Structure
Callinectes sapidus
TPS and the Trehalose Synthesis Pathway
Tissue Expression of TPS Genes
Aedes aegypti
Insect Development and TPS Gene Expression
Diversity of TPS Genes and Their Functions
Role of TPS in Regulating Sugar Metabolism
TPS Functions during Stress Conditions
Regulation of Chitin Metabolism by TPS
Findings
POTENTIAL TARGET FOR INSECTICIDES
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