Enzymatic control of anhydrobiosis‐related accumulation of trehalose in the sleeping chironomid, Polypedilum vanderplanki

Abstract

Larvae of an anhydrobiotic insect, Polypedilum vanderplanki, accumulate very large amounts of trehalose as a compatible solute on desiccation, but the molecular mechanisms underlying this accumulation are unclear. We therefore isolated the genes coding for trehalose metabolism enzymes, i.e. trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphate phosphatase (TPP) for the synthesis step, and trehalase (TREH) for the degradation step. Although computational prediction indicated that the alternative splicing variants (PvTpsα/β) obtained encoded probable functional motifs consisting of a typical consensus domain of TPS and a conserved sequence of TPP, PvTpsα did not exert activity as TPP, but only as TPS. Instead, a distinct gene (PvTpp) obtained expressed TPP activity. Previous reports have suggested that insect TPS is, exceptionally, a bifunctional enzyme governing both TPS and TPP. In this article, we propose that TPS and TPP activities in insects can be attributed to discrete genes. The translated product of the TREH ortholog (PvTreh) certainly degraded trehalose to glucose. Trehalose was synthesized abundantly, consistent with increased activities of TPS and TPP and suppressed TREH activity. These results show that trehalose accumulation observed during anhydrobiosis induction in desiccating larvae can be attributed to the activation of the trehalose synthetic pathway and to the depression of trehalose hydrolysis.

Multiple horizontally acquired genes from fungal and prokaryotic donors encode cellulolytic enzymes in the bdelloid rotifer Adineta ricciae

“…In some invertebrates, desiccation tolerance is attributed to the presence of oligosaccharides, mainly trehalose (Crowe, 2002;Sakurai et al, 2008;Mitsumasu et al, 2010;Tyson et al, 2012), which protect cell membrane integrity during dehydration and rehydration (Clegg, 2001), probably by organic glass formation in the dry state (Burke, 1986;Crowe et al, 1998). Other oligosaccharides such as sucrose, cellobiose or melibiose protect the activity of freezedried β-galactosidase (Heljo et al, 2011).…”

Carbohydrate Metabolism in Drosophila: Reliance on the Disaccharide Trehalose

“…These enzyme's activities increased during dehydration, whereas that of trehalase decreased. This was not only due to altered enzymatic activity, but also to transcriptional control, as the levels of the synthesis enzymes cDNAs increased at the beginning of dehydration, whereas that of trehalase increased only after forty eight hours since inititation of dehydration, perhaps as preparation for subsequent rehydration [63]. Other species also use trehalose as a protectant during anhydrobiosis: the crustacean Artemia salina and the nematode Avelenchus avenae.…”

The induction of anhydrobiosis in the sleeping chironomid: Current status of our knowledge

“…6). Functional and expression analyses showed that trehalose was abundantly synthesized as consistent with increased activities of TPS and TPP and suppressed TREH activity (70).…”