Reciprocal roles of two trehalose transporters in aestivating cabbage stem flea beetles (Psylliodes chrysocephala)

Abstract

The cabbage stem flea beetle (Psylliodes chrysocephala, CSFB) is a significant pest of winter oilseed rape crops in northern Europe. CSFB adults aestivate during the summer to protect themselves from heat and desiccation stress. Trehalose, the primary hemolymph sugar, has been linked to energy homeostasis and stress resilience, but its regulation and function during aestivation remain poorly understood. Here, we investigated the roles of two trehalose transporters, Tret-1 and Tret-2, in modulating trehalose dynamics across different adult stages in CSFB. Through spatiotemporal transcript profiling, we found that Tret-1 was predominantly expressed in the fat body, where it facilitates trehalose export to the hemolymph, whereas Tret-2 expression was higher in the Malpighian tubules, mediating trehalose uptake from the hemolymph. RNA interference experiments revealed that Tret-1 is involved in transporting trehalose from the fat body into the hemolymph, while Tret-2 works reciprocally to transport trehalose from the hemolymph into the Malpighian tubules. The disruption of trehalose transportation resulted in excess glucose, glycogen, and triglyceride levels, mainly in pre-aestivation beetles. Furthermore, the knockdown of either trehalose transporter caused a compensatory increase in feeding activity in pre-aestivation beetles, while the knockdown of Tret-2 compromised resilience to heat stress. Our findings uncover the reciprocal functions of Tret-1 and Tret-2 in regulating trehalose distribution and maintaining metabolic stability during aestivation, offering insights into the physiological strategies underpinning insect survival during aestivation. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=128 SRC="FIGDIR/small/639621v1_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@1ec0817org.highwire.dtl.DTLVardef@107534eorg.highwire.dtl.DTLVardef@1ee4322org.highwire.dtl.DTLVardef@1797559_HPS_FORMAT_FIGEXP M_FIG C_FIG O_LITwo Trehalose transporters were investigated in aestivating P. chrysocephala C_LIO_LITret-1 mainly transports trehalose out of fat body C_LIO_LITret-2 mainly transports trehalose into Malpighian tubules C_LIO_LIDynamic trehalose transportation regulates other metabolites, including Glucose C_LIO_LITret-2, but not Tret-1, might be necessary for heat stress resilience C_LI