Molecular characterization of insulin‐like peptides in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae)

Abstract

Insulin-like peptides (ILPs) including insulin, insulin-like growth factor (IGF) and relaxin are evolutionarily conserved hormones in metazoans, and they are involved in diverse physiological processes. The migratory brown planthopper (BPH), Nilaparvata lugens, encodes four ILP genes (Nlilp1, Nlilp2, Nlilp3 and Nlilp4) but their physiological roles are largely unknown. Sequence analysis showed that NlILP1 contained a relaxinspecific G protein-coupled receptor-binding motif and a variant motif of cysteine residues, and NlILP2 and NlILP4 resembled vertebrate IGFs. RNA interference (RNAi)-mediated gene silencing showed that depletion of each of Nlilp1, 2 and 3 significantly delayed the developmental duration of nymphs, and this effect could be exacerbated by double or triple gene depletion. Depletion of Nlilp1, Nlilp2 or Nlilp3 induces the accumulation of glucose, trehalose and glycogen, which is contradictory to depletion of the insulin receptor (NlInR1) in the BPH. Depletion of Nlilp1 significantly enhanced starvation resistance in both females and males although its extent was smaller than NlInR1 depletion. A parental RNAi assay showed that depletion of each of Nlilp1-4 dramatically impaired female fecundity. These findings indicate that NlILP1-4 have redundant and distinct roles in physiological processes in the BPH, thereby enhancing our understanding of the contribution of each NlILP to the ecological success of this species in natural habitats.

Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens

“…However, NlInR2 E4 adults had comparable glucose (Fig 2C ) and triglyceride (Fig 2D) contents compared to Wt SW controls. In addition, analogous to NlInR1 RNAi [47], NlInR2 E4 females showed~27% reduction in fecundity compared to Wt SW controls (Fig 2E) although NlInR2 E4 females had well-developed ovaries morphologically similar to those in Wt SW (S4 Fig), which were in stark contrast to immature ovaries in NlInR1 RNAi -treated females. In addition, the correlation coefficients between egg numbers and hind tibia length in Wt LW , Wt SW , and NlInR2 E4 were significantly low (< 0.009, Fig 2E), indicating that fecundity may be not correlated with its body size in BPH.…”

“…In contrary to extended adult lifespan and increased starvation tolerance derived from NlInR1 RNAi [ 47 ], depletion of NlInR2 had a marginal effect on adult lifespan ( Fig 2F ) and significantly reduced starvation tolerance ( Fig 2G ). Taken together, our findings indicate that Nl InR2 resembles Nl InR1 on nymphal development and fecundity, but differs from Nl InR1 on fuel metabolism, lifespan, and starvation tolerance.…”

“…BPH has four insulin-like peptides and two InR paralogues, NlInR1 and NlInR2 , and they share a high sequence similarity and resemble domain structures. However, only NlInR1 was functionally analogous to dInR with respect to development, metabolic homeostasis, stress responses, lifespan, reproduction, and starvation tolerance [ 25 , 46 , 47 ]. Activation of Nl InR1 activates of the phosphatidylinositol-3-OH kinase [ Nl PI(3)K]-protein kinase B ( Nl Akt) signaling cascade, which in turn inactivates the forkhead transcription factor subgroup O ( Nl FoxO), thus leading to the LW morph.…”

Identification of Gonadulin and Insulin-Like Growth Factor From Migratory Locusts and Their Importance in Reproduction in Locusta migratoria

“…Six of these are expressed mainly in the brain, two in the ovary (Bgilp2 and gonadulin), and a single aIGF expressed in the fat body ( 3 , 6 ). In two different hemipteran insects, the blood-sucking bug Rhodnius prolixus and the migratory brown planthopper Nilaparvata lugens , four ILPs have been characterized ( 7 , 8 ). In R. prolixus , one of the ILPs (RhoprIGF) is highly expressed in the fat body and is classified as an aIGF ( 9 ), whereas in N. lugens , two of them (NlILP2 and NlILP4) resemble IGFs ( 8 ).…”

“…In two different hemipteran insects, the blood-sucking bug Rhodnius prolixus and the migratory brown planthopper Nilaparvata lugens , four ILPs have been characterized ( 7 , 8 ). In R. prolixus , one of the ILPs (RhoprIGF) is highly expressed in the fat body and is classified as an aIGF ( 9 ), whereas in N. lugens , two of them (NlILP2 and NlILP4) resemble IGFs ( 8 ). A model insect widely used to study insulin signaling has been the lepidopteran silk moth Bombyx mori ; and indeed, the first ILP identified in insects was from this species ( 10 ).…”