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

Miki Yoshida,Takashi Nishimura,Hiroko Matsuda,Hitomi Kubo

doi:10.1038/srep30582

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.

Highlights

Organisms live in variable environments, and adaptive strategies have evolved to cope with adverse environmental conditions such as starvation, low oxygen levels, and lack of water
Trehalose has been recognized to be an important osmoprotectant and a mediator of desiccation tolerance because of its stability and inert chemical properties[9,10,11,12,13]. Many of these roles have been documented in the budding yeast Saccharomyces cerevisiae, where trehalose is proposed to play a protective role by functioning as a chemical chaperone, which prevents protein denaturation and aggregation and influences protein folding through trehalose-protein interactions[14,15]
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. elegans16, 1Laboratory for Growth Control Signaling, RIKEN Center for Developmental Biology (CDB), 2-2-3 MinatojimaMinamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan. 2Graduate School of Biological Science, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0101, Japan. †Present address: Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7, Konan, Minato-ku, Tokyo 108-8477, Japan. *These authors contributed to this work.Correspondence and requests for materials should be addressed to T.N. www.nature.com/scientificreports/

Summary

Introduction

Organisms live in variable environments, and adaptive strategies have evolved to cope with adverse environmental conditions such as starvation, low oxygen levels, and lack of water. Maintenance of systemic water homeostasis and fluid balance is critical in most organisms, including humans, to tolerate changes in osmolarity and prevent desiccation[1,2,3]. We previously reported that larvae lacking trehalose exhibit diet-dependent phenotypes relating to growth and survival in the genetically tractable organism, D. melanogaster[25]. In this manuscript, we describe the molecular characterization of the genes responsible for trehalose metabolism, Tps[1] and Treh. Defects in trehalose metabolism affect water homeostasis and desiccation tolerance

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Conclusion