Adipokinetic Hormone Receptor Mediates Trehalose Homeostasis to Promote Vitellogenin Uptake by Oocytes in Nilaparvata lugens

Abstract

Adipokinetic hormones (AKHs) are well known to mobilize lipids and carbohydrates for energy-consuming activities in insects. These neuropeptides exert their functions by interacting with AKH receptors (AKHRs) located on the plasma membrane of fat body cells, which regulates energy mobilization by stimulating lipolysis of triacylglycerols (TAG) to diacylglycerols (DAG) and conversion of glycogen into trehalose. Here, we investigated the roles of AKH/AKHR signaling system in trehalose metabolism and vitellogenesis during female reproduction in the brown planthopper, Nilaparvata lugens. Knockdown of AKHR expression by RNA interference (RNAi) resulted in a decrease of the circulating trehalose in hemolymph and significantly increased levels of two trehalases in fat bodies, indicating that the modulation of hemolymph trehalose levels by AKHR may be mediated by regulating trehalose degradation. In addition, adult females that had been injected with double-stranded RNA (dsRNA) for AKHR exhibited delayed oocyte maturation, prolonged pre-oviposition period, as well as decline in egg number and reduction in fecundity. Considering that these phenotypes resulting from AKHR silencing are similar to those of vitellogenin receptor (VgR) RNAi, we further analyzed a possible connection between AKHR and vitellogenesis. Knockdown of AKHR showed no effects on the Vg synthesis in fat bodies, whereas it significantly reduced the levels of VgR in ovaries. With RNAi-females, we observed an increase of Vg accumulation in hemolymph and a decrease of Vg deposition in ovaries. Moreover, the decrease in VgR expression and Vg incorporation by developing oocytes could be partially rescued by injection of trehalose into AKHR RNAi females. The present study has implicated trehalose in the AKH/AKHR signaling-mediated control of reproduction and provided new insight into mechanisms of AKH/AKHR regulation of trehalose metabolism in insect vitellogenesis, oocyte maturation and fecundity.

The Effect of Different Dietary Sugars on the Development and Fecundity of Harmonia axyridis

“…In addition, studies have shown that the trehalose content affects food choices and feeding behavior. The physiological role of trehalose as insects' blood sugar during their reproductive processes has been reported previously (Lu et al, 2019). A parallel relationship between the hemolymph trehalose levels and ovarian maturation was observed, suggesting that trehalose supplies the energy required for the reproductive cycle processes (Huang and Lee, 2011).…”

“…Trehalose has been reported as the dominant sugar in the insect hemolymph and other tissues (Van Handel, 1969) as it provides energy for targeted activities (Lu et al, 2019). In our study, we detected that the ATP content in the Diet 2 and Diet 3 groups was significantly higher than that in the Diet 1 group.…”

“…In addition, studies have shown that the main parts of insects that produce and store glycogen and trehalose are fat bodies, ovaries, and flying muscles (Tang et al, 2012). Trehalose is the energy fuel for vitellogenin (Vg) formation and oocyte maturation (Lu et al, 2019). Therefore, it is speculated that eating artificial feedstuffs with glucose or trehalose could provide insects with sufficient energy to act on the ovary, thereby promoting the development of their ovaries and increasing spawning.…”

Research Progress on Oviposition-Related Genes in Insects

“…AKHs also function to mobilize lipids and carbohydrates in the progress of insect oviposition, and they may be involved in the reproductive regulation of oocytes. Inhibition of AKHR gene expression by RNAi leads to not only a decrease in AKH content in the circulating hemolymph but also an increase in Vg protein accumulation in the hemolymph and a decrease in Vg protein deposition in the ovaries, which is not conducive to the formation of ova ( Lu et al 2019b ). However, how the VgR receptor releases Vg protein into the hemolymph and how it affects the biochemical reaction of oocytes during oogenesis, as well as the localization mechanism of the VgR mRNA and protein in cells, are unknown ( Rika et al 2019 ).…”

Adipokinetic hormone enhances CarE‐mediated chlorpyrifos resistance in the brown planthopper, Nilaparvata lugens

“…Chemosynthetic AKH peptide (pQVNFSPNW‐NH 2 ) was dissolved in DMSO and adjusted to 4.5 μM (Lu et al ., 2019c). After anaesthetized with carbon dioxide, a sample of 100 pmol AKH (23 nl) was injected into the newly emerged BPH female with a Nanoject II microinjection device (Drummond Scientific).…”