Downregulation of dTps1 in Drosophila melanogaster larvae confirms involvement of trehalose in redox regulation following desiccation

Abstract

As a survival strategy to environmental water deficits, desiccation-tolerant organisms are commonly known for their ability to recruit stress-protective biomolecules such as trehalose. We have previously reported the pivotal role of trehalose in larval desiccation tolerance in Drosophila melanogaster. Trehalose has emerged as a versatile molecule, serving mainly as energy source in insects and also being a stress protectant. While several recent reports have revealed the unconventional role of trehalose in scavenging reactive oxygen species in yeast and plants, this aspect has not received much attention in animals. We examined the status of desiccation-induced generation of reactive oxygen species in D. melanogaster larvae and the possible involvement of trehalose in ameliorating the harmful consequences thereof. Insect trehalose synthesis is governed by the enzyme trehalose 6-phosphate synthase 1 (TPS1). Using the ubiquitous da-GAL4-driven expression of the dTps1-RNAi transgene, we generated dTps1-downregulated Drosophila larvae possessing depleted levels of dTps1 transcripts. This resulted in the inability of the larvae for trehalose synthesis, thereby allowing us to elucidate the significance of trehalose in the regulation of desiccation-responsive redox homeostasis. Furthermore, the results from molecular genetics studies, biochemical assays, electron spin resonance analyses and a simple, non-invasive method of whole larval live imaging suggested that trehalose in collaboration with superoxide dismutase (SOD) is involved in the maintenance of redox state in D. melanogaster.

Invertebrate Trehalose-6-Phosphate Synthase Gene: Genetic Architecture, Biochemistry, Physiological Function, and Potential Applications

“…Drosophila larvae were shown to be unable to synthesize trehalose when dTPS1 transcript levels were decreased by the ubiquitous daGAL4-driven expression of the dTPS1 -RNAi transgene (Thorat et al, 2016 ). This result highlighted the significance of trehalose in the regulation of desiccation-responsive redox homeostasis (Thorat et al, 2016 ).…”

“…Drosophila larvae were shown to be unable to synthesize trehalose when dTPS1 transcript levels were decreased by the ubiquitous daGAL4-driven expression of the dTPS1 -RNAi transgene (Thorat et al, 2016 ). This result highlighted the significance of trehalose in the regulation of desiccation-responsive redox homeostasis (Thorat et al, 2016 ). The result on the function of TPS further demonstrated that the regulation of trehalose metabolism is essential for normal development, body water homeostasis, and desiccation tolerance in Drosophila (Yoshida et al, 2016 ).…”

“…The result on the function of TPS further demonstrated that the regulation of trehalose metabolism is essential for normal development, body water homeostasis, and desiccation tolerance in Drosophila (Yoshida et al, 2016 ). Dietary trehalose has also been shown to be directly transported to the hemolymph from the larval gut in insects (Shi et al, 2016 ), because feeding of trehalose dramatically increased the in vivo trehalose pools in D. melanogaster larvae treated with DmTPS RNAi (Thorat et al, 2016 ). In addition, the knockdown of LdTPS delayed larval development, strongly reduced hemolymph monosaccharides in the fat body, and potentiated sugar absorption in the larval gut of L. decemlineata (Shi et al, 2016 ).…”

Molecular characterization of Tps1 and Treh genes in Drosophila and their role in body water homeostasis

“…Although trehalose accumulation is not the only mechanisms involved in desiccation tolerance, it has been demonstrated to be an important factor for desiccation tolerance based on genetic evidence in diverse multicellular organisms such as the nematode C . elegans 16 , the mosquito Anopheles gambiae 18 , and the fruit fly Drosophila melanogaster 19 . The physiological role of trehalose in insects has been proposed for decades.…”

Seasonal changes in recombination rate, crossover interference, and their response to desiccation stress in a natural population ofDrosophila melanogasterfrom India

“…includes genes involved in signal transduction pathways and oxidoreductase activity. The role of oxidation/reduction in the acute adaptive response to desiccation stress is well-recognized [68,93,94]. In chromosome 2, interval (al-dp) is enriched by membrane formation and transmembrane transport genes;…”