A Novel Member of the Trehalose Transporter Family Functions as an H+-Dependent Trehalose Transporter in the Reabsorption of Trehalose in Malpighian Tubules

Abstract

In insects, Malpighian tubules are functionally analogous to mammalian kidneys in that they not only are essential to excrete waste molecules into the lumen but also are responsible for the reabsorption of indispensable molecules, such as sugars, from the lumen to the principal cells. Among sugars, the disaccharide trehalose is highly important to insects because it is the main hemolymph sugar to serve as a source of energy and carbon. The trehalose transporter TRET1 participates in the transfer of newly synthesized trehalose from the fat body across the cellular membrane into the hemolymph. Although transport proteins must play a pivotal role in the reabsorption of trehalose in Malpighian tubules, the molecular context underlying this process remains obscure. Previously, we identified a Tret1 homolog (Nlst8) that is expressed principally in the Malpighian tubules of the brown planthopper (BPH). Here, we used the Xenopus oocyte expression system to show that NlST8 exerts trehalose transport activity that is elevated under low pH conditions. These functional assays indicate that Nlst8 encodes a proton-dependent trehalose transporter (H-TRET1). To examine the involvement of Nlst8 in trehalose reabsorption, we analyzed the sugar composition of honeydew by using BPH with RNAi gene silencing. Trehalose was detected in the honeydew as waste excreted from Nlst8-dsRNA-injected BPH under hyperglycemic conditions. However, trehalose was not expelled from GFP-dsRNA-injected BPH even under hyperglycemic conditions. We conclude that NlST8 could participate in trehalose reabsorption driven by a H+ gradient from the lumen to the principal cells of the Malpighian tubules.

Herbivory-induced glucose transporter gene expression in the brown planthopper, Nilaparvata lugens

“…Main energy sources for various tissues in insects are hemolymph sugars, which are supplied from the fat body cells during starvation (Wyatt, 1961;Becker et al, 1996). Trehalose and myo-inositol are the main hemolymph sugars in BPH (Moriwaki et al, 2003;Kikuta et al, 2012). NlST11 may facilitate blood sugar effluxes produced in the fat body to maintain energy homeostasis.…”

“…fructose, resulting in high glucose and fructose concentrations in the midgut lumen (Price et al, 2007a). In contrast, the hemolymph in counter spaces across midgut cells contains little glucose and fructose, but mainly trehalose and myo-inositol (Moriwaki et al, 2003;Kikuta et al, 2012). The glucose and fructose gradients apparently occur from the midgut lumen to the hemolymph, causing glucose and fructose transportation into the hemolymph.…”

“…The property of NlST8, belonging to a trehalose transporter (TRET1) family in insects, was hypothesized to show facilitated diffusion as well as other TRET1 members using phylogenetic analyses. Biochemical analyses revealed that NlST8 was an H þ -dependent trehalose transporter, not showing facilitated diffusion (Kikuta et al, 2012).…”

Effect of host‐plant and infection with ‘Candidatus Liberibacter asiaticus’ on honeydew chemical composition of the Asian citrus psyllid, Diaphorina citri

“…Trehalose synthesized in the fat body is transported to the hemolymph where it is used as energy source (Candy et al, 1997;Kikuta et al, 2012). Trehalose in the hemolymph may also leak into the tubule lumens and be excreted in the honeydew (Kikuta et al, 2012).…”

Functional characterization of a putative disaccharide membrane transporter in crustacean intestine

“…Since molecular phylogeny reflects the evolutionary process, it provides the most reliable guide to the structure, function, and mechanism of biological macromolecules (Saier, 2000). Although it is very difficult to predict the functional characteristics of sugar transporters based on amino acid sequences because of the subtle difference that exist between various transport families, the amino acid sequence can indicate a general function exists between sugar transporters in a major facilitator superfamily (Kikuta, 2012).…”