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

Abstract

In insects, trehalose serves as the main sugar component of haemolymph. Trehalose is also recognized as a mediator of desiccation survival due to its proposed ability to stabilize membranes and proteins. Although the physiological role of trehalose in insects has been documented for decades, genetic evidence to support the importance of trehalose metabolism remains incomplete. We here show on the basis of genetic and biochemical evidence that the trehalose synthesis enzyme Tps1 is solely responsible for the de novo synthesis of trehalose in Drosophila. Conversely, a lack of the gene for the trehalose hydrolyzing enzyme Treh causes an accumulation of trehalose that is lethal during the pupal period, as is observed with Tps1 mutants. Lack of either Tps1 or Treh results in a significant reduction in circulating glucose, suggesting that the maintenance of glucose levels requires a continuous turnover of trehalose. Furthermore, changes in trehalose levels are positively correlated with the haemolymph water volume. In addition, both Tps1 and Treh mutant larvae exhibit a high lethality after desiccation stress. These results demonstrate that the regulation of trehalose metabolism is essential for normal development, body water homeostasis, and desiccation tolerance in Drosophila.

Adaptation to dietary conditions by trehalose metabolism in Drosophila

“…In addition, Treh 18 decreased the level of glucose but did not affect the levels of TAG and glycogen. These results are consistent with our previous report 9 . Because both Treh 18 and Treh 41 have a deletion/insertion within the intron region of the Treh gene, the hypomorphic phenotype of Treh 18 and Treh 41 is likely due to the reduced transcription and/or alterations of Treh mRNA, as reported 17 .…”

“…Tps1 lacW and Treh cs have been described previously 8, 9 . Treh EY06982 and Df ( 2R ) Exel6072 (a deficiency for the Treh locus) were obtained from the Bloomington Drosophila Stock Center.…”

“…The primers used to detect Treh ( common ), sTreh , cTreh , and rp49 levels were described previously 8, 9 .…”

“…Tps1 has two functionally distinct catalytic domains 8, 9 . The N-terminus trehalose-6-phosphate synthase (TPS) domain produces Tre6P from glycose-6-phophate (Glu-6P) and UDP-glucose.…”

Role of glycogen in development and adult fitness in Drosophila

“…This result is consistent with our previous report showing that maternal and zygotic mutation of Tps1 does not result in embryonic lethality (Matsuda et al, 2015). Because Tps1 and Treh mutant larvae are extremely sensitive to dietary deprivation (Matsuda et al, 2015;Yoshida et al, 2016), the physiological significance of trehalose synthesis during embryogenesis is the most likely explanation for survival immediately after hatching. These results are consistent with previous reports showing that global expression of genes involved in aerobic glycolysis occurs at the end of the embryonic stage for metabolic adaptation in larvae (Tennessen et al, 2011(Tennessen et al, , 2014.…”