Vestigial mediates the effect of insulin signaling pathway on wing-morph switching in planthoppers

Abstract

Wing polymorphism is an evolutionary feature found in a wide variety of insects, which offers a model system for studying the evolutionary significance of dispersal. In the wing-dimorphic planthopper Nilaparvata lugens, the insulin/insulin-like growth factor signaling (IIS) pathway acts as a ‘master signal’ that directs the development of either long-winged (LW) or short-winged (SW) morphs via regulation of the activity of Forkhead transcription factor subgroup O (NlFoxO). However, downstream effectors of the IIS–FoxO signaling cascade that mediate alternative wing morphs are unclear. Here we found that vestigial (Nlvg), a key wing-patterning gene, is selectively and temporally regulated by the IIS–FoxO signaling cascade during the wing-morph decision stage (fifth-instar stage). RNA interference (RNAi)-mediated silencing of Nlfoxo increase Nlvg expression in the fifth-instar stage (the last nymphal stage), thereby inducing LW development. Conversely, silencing of Nlvg can antagonize the effects of IIS activity on LW development, redirecting wing commitment from LW to the morph with intermediate wing size. In vitro and in vivo binding assays indicated that NlFoxO protein may suppress Nlvg expression by directly binding to the first intron region of the Nlvg locus. Our findings provide a first glimpse of the link connecting the IIS pathway to the wing-patterning network on the developmental plasticity of wings in insects, and help us understanding how phenotypic diversity is generated by the modification of a common set of pattern elements.

Photoperiod controls wing polyphenism in a water strider independently of insulin receptor signalling

“…Thus, wing morph variation in this species is an example of an environmentally induced polyphenism. The genetic basis of this polyphenism remains unknown, unlike studies on other environmentally induced wing polyphenisms where the IIS pathway is involved [14,15,37], our RNAi experiments demonstrate that knock down of genes in the IIS pathway do not alter induction of the different wing morphs. Thus, the nutrient-sensing IIS pathway is not ubiquitous in regulating insect wing polyphenism and our results therefore suggest that there are multiple genetic origins to how environmental cues are incorporated and result in wing polyphenism in insects.…”

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

“…To look into further how the LW phenotype developed in NlInR2 E4 mutants, we investigated wing-cell numbers in 5 th -instar nymphs by quantifying genomic DNA copy number using quantitative real-time PCR (qRT-PCR). Because wing buds grow explosively during an approximately 48 h time window at the beginning of the 5 th -instar nymph stage [ 48 ], fifth-instar nymphs were collected at 24 h intervals after ecdysis, and the wing buds were dissected from the second thoracic segment (T2W) and third thoracic segment (T3W) ( Fig 3A ). The number of cells in T2W from 5 th -intar NlInR2 E4 nymphs at 3 h after ecdysis (hAE) were comparable to that from Wt SW nymphs ( Fig 3B ).…”

Transcriptome Analysis of the Regulatory Mechanism of FoxO on Wing Dimorphism in the Brown Planthopper, Nilaparvata lugens (Hemiptera: Delphacidae)

“…Previous studies showed that inactivation of NlFoxO resulted in a switch from SW to LW morphs in BPH [ 4 , 5 , 35 ]. To further explore the molecular basis regulated by Nl FoxO, transcriptomic profiles were conducted on LW- and SW-destined wing buds of 5th-instar nymphs, the wing-morph decisive stage of BPH [ 7 ]. We showed that knockdown of NlFoxO significantly altered the expression of 2128, 2902, and 1813 genes in forewing buds of 5th-instar nymphs at 24, 36, 48 hAE, respectively, and simultaneously altered the expression of 3466, 2533, and 2279 genes in hindwing buds.…”

“…Our recent studies showed that the N. lugens FoxO homolog Nl FoxO relied on the insulin/insulin-like signaling (IIS) activity to direct wing buds developing into SW or LW morphs during the wing-morph decisive stage (the 5th-instar stage). High IIS activity inhibited Nl FoxO activity, leading to LW morphs, and vice versa [ 5 , 6 , 7 ]. However, the molecular basis by which Nl FoxO influences alternative wing morphs remains largely unknown.…”