Molecular Characterization and Function Analysis of the Vitellogenin Receptor from the Cotton Bollworm, Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae)

Abstract

Developing oocytes accumulate plentiful yolk protein during oogenesis through receptor-mediated endocytosis. The vitellogenin receptor (VgR), belonging to the low-density lipoprotein receptor (LDLR) family, regulates the absorption of yolk protein. In this work, the full-length vitellogenin receptor (HaVgR) in the cotton bollworm Helicoverpa armigera was identified, encoding a 1817 residue protein. Sequence alignment revealed that the sequence of HaVgR contained all of the conservative structural motifs of LDLR family members, and phylogenetic analysis indicated that HaVgR had a high identity among Lepidoptera and was distinct from that of other insects. Consistent with other insects, HaVgR was specifically expressed in ovarian tissue. The developmental expression pattern showed that HaVgR was first transcribed in the newly metamorphosed female adults, reached a peak in 2-day-old adults and then declined. Western blot analysis also revealed an ovarian-specific and developing expression pattern, which was consistent with the HaVgR mRNA transcription. Moreover, RNAi-mediated HaVgR knockdown strongly reduced the VgR expression in both the mRNA and protein levels, which inhibited the yolk protein deposition in the ovaries, led to the dramatic accumulation of vitellogenin and the up-regulation of HaVg expression in hemolymph, and eventually resulted in a declined fecundity. Together, all of these findings demonstrate that HaVgR is a specific receptor in uptake and transportation of yolk protein for the maturation of oocytes and that it plays a critical role in female reproduction.

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“…This hypothesis is not inconsistent with patterns of gene expression observed in other species. For example, similar results were reported for H. armigera , where HaVg mRNA in haemolymph was upregulated after ds HaVgR injection (Zhang et al ., ), and Bdyp1 was upregulated by silencing of BdVgR in Ba. dorsalis (Cong et al ., ).…”

“…Other studies have reported that Vg expression is much higher in the female fat body than in other tissues, such as the ovary and gut, in Apolygus lucorum and N. lugens (Lu et al ., ; Li et al ., ), and that Vg1 and Vg2 mRNAs are highly expressed in adult females of Triatoma infestans (Blariza et al ., ). Tissue‐specific expression analyses revealed the specific expression of NlVgR , HaVgR and BmVgR in the ovary, but not in the head, fat body and midgut of N. lugens , H. armigera and Bombyx mandarina , respectively (Lu et al ., ; Qian et al ., ; Zhang et al ., ). BdVgR was highly expressed in the ovary of Ba.…”

“…lecularius Vg also reduced egg production, and led to atrophied ovaries and an inflated abdomen (Moriyama et al, 2016). RNAi-mediated HaVgR and BtVgR knockdown resulted in reduced fecundity in H. armigera and Bemisia tabaci, respectively (Upadhyay et al, 2016;Zhang et al, 2016b). Injection with NlVgR dsRNA led to the arrested development of ovaries and reproductive failure in N. lugens (Lu et al, 2015).…”

“…The LBDs contain several LDLR‐domain class A repeats, and the EGFs contain several epidermal growth factor/factor‐like domains and low‐density lipoprotein‐receptor Tyr‐Trp‐Thr‐Asp (YWTD) domains. Recent studies have shown that silencing of VgRs by RNAi in Bactrocera dorsalis (Cong et al ., ), Helicoverpa armigera (Zhang et al ., ), N. lugens (Lu et al ., ) and Dermacentor variabilis (Iii et al ., ) leads to malformed ovaries and decreased fecundity, phenotypes very similar to those obtained by silencing Vg . However, in vitro synthesized double‐stranded RNA (dsRNA) into the haemocoel did not cause an RNAi response in the locust ovary including VgR (Ren et al ., ).…”

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“…Vg is a major yolk protein precursor in insects for the developing oocytes to meet the nutrient requirements during egg development24. This female-specific protein is synthesized in the fat body and release into the hemolymph, from where it is absorbed by the growing oocytes2526.…”