Molecular identification and functional analysis of Niemann-Pick type C2 proteins，carriers for semiochemicals and other hydrophobic compounds in the brown dog tick, Rhipicephalus linnaei.

Olfaction plays a crucial role in many important behavioral activities of insects, such as finding sexual partners, locating hosts, and selecting oviposition sites. Ionotropic receptors (IRs) play a central role in detecting chemosensory information from the environment and guiding insect behaviors and are potential target genes for pest control. Empoasca onukii Matsuda is a major pest of the tea plant Camellia sinensis (L.) O. Ktze, and seriously influences tea yields and quality. In this study, the ionotropic receptor gene EnouIR25a in E. onukii was cloned, and the expression pattern of EnouIR25a was detected in various tissues. Behavioral responses of E. onukii to volatile compounds emitted by tea plants were determined by the olfactometer bioassay and field trials. To further explore the function of EnouIR25a in olfactory recognition of compounds, RNAi (RNA interference) of EnouIR25a was carried out by ingestion of in vitro synthesized dsRNAs. The CDS length of EnouIR25a was 1266 bp and it encoded a 48.87 kD protein. EnouIR25a was enriched in the antennae of E. onukii. E. onukii were more significantly attracted by 1-phenylethanol at concentration of 100 &amp;micro;l/ml. Feeding with dsRNA-IR25a significantly downregulated the expression level of EonuIR25a, after 3 h of treatment, which disturbed the behavioral responses of E. onukii to 1-phenylethanol at concentration of 100&amp;micro;l/ml. The response rate of E. onukii to 1-phenylethanol was significantly decreased after dsRNA-IR25a treatment for 12 h. In summary, the ionotropic receptor gene EnouIR25a was highly expressed in the antennae of E. onukii and was involved in olfactory recognition of the tea plant volatile 1-phenylethanol. The present study may help us to use the ionotropic receptor gene as a target for the behavioral manipulation of E. onukii in the future. 

The Key Roles of Ionotropic Receptor Gene EnouIR25a in Host-Plant Finding by the Tea Green Leafhopper, Empoasca onukii Matsuda

As a new protein class of semiochemical binding and transporting, Niemann-Pick proteins type C2 (NPC2) in arthropods have received more attentions in recent decade. However, the gene function has not been studied in phytoseiid mites with biocontrol potential. In the current study, we cloned a NPC2 gene PpNPC2a from the transcriptome of Phytoseiulus persimilis Athias-Henriot. By encoding 181 amino acids with a conserved ML domain, PpNPC2a was found a homolog of NPC2-1 in Galendromus occidentalis Nesbitt. We then measured the spatio-temporal expression of PpNPC2a in P. persimilis, and found the highest expression in female adults compared to other stages. Due to the tiny body size of predatory mites, we only examined tissue expressions in two sections: the anterior part (gnathosoma and the first pair of legs) and the posterior part (idiosoma without the first pair of legs). Higher transcription of PpNPC2a was found in the posterior part. To investigate the potential function of PpNPC2a in P. persimilis, we interfered gene expression in female adults by feeding dsRNA, which resulted in a decrease of relative expression by 59.1 and 78.2% after 24 and 72 h, respectively. Compared with the control, dsNPC2a-treated P. persimilis were insensitive to the scent of leaves or plants infested by spider mites, suggesting a role of PpNPC2a in response to plant volatiles. However, the dsNPC2a-interfered mites could still respond to four representative compounds of herbivore-induced plant volatiles, including 4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), methyl salicylate (MeSA), β-caryophyllene and linalool. In short, our results indicated PpNPC2a may be involved in the chemosensory process of P. persimilis in response to whole-plant volatiles. 

Expression and functional analysis of Niemann–Pick C2 gene in Phytoseiulus persimilis

Reverse chemical ecology has been widely applied for the functional characterization of olfactory proteins in various arthropods, but few related studies have focused on parasitic wasps. Here, the odorant carrier Niemann–Pick C2 protein of Baryscapus dioryctriae (BdioNPC2b) was studied in vitro and in vivo. Ligand binding analysis revealed that BdioNPC2b most strongly bound to 2-butyl-2-octenal and which compound could elicit an EAG response and attracted B. dioryctriae adults. Moreover, this odorant attractant significantly improved the reproductive efficiency of B. dioryctriae compared to that of the control. Then, the relationship between BdioNPC2b and 2-butyl-2-octenal was validated by RNAi, and site-directed mutagenesis revealed the involvement of three key residues of BdioNPC2b in binding to 2-butyl-2-octenal through hydrogen bonding. Our findings provide not only a deeper understanding of the olfactory function of NPC2 in wasps but also useful information for improving the performance of the parasitoid B. dioryctriae as a biological control agent. 

Functional Characterization of the Niemann–Pick C2 Protein BdioNPC2b in the Parasitic Wasp Baryscapus dioryctriae (Chalcidodea: Eulophidae)

Tick chemosensation and implications for novel control strategies.

Studies have shown that the main pathway for tick host localization and perception of mating information may be chemosensory. However, chemical communication in ticks is poorly understood, especially in those other than the Ixodes ticks. Niemann–Pick C2 (NPC2) protein and ionotropic receptors (IRs) are considered to be closely related to the perception of infochemicals in arthropods. Through bioinformatic analysis, eight NPC2 and four IR candidate genes were identified through screening and identification of the transcriptome sequencing database of Haemaphysalis longicornis. Phylogenetic tree analysis indicated that H. longicornis possesses similar homology to the genus Ixodes. A comparison of the expression of NPC2 and IR in tick forelegs (first pair of legs), hind legs (fourth pair of legs), and capitula using RT-PCR revealed that, barring HlonNPC2-8, 11 candidate genes were highly expressed in the foreleg and capitulum, which are the main sensory organs of ticks. They were also expressed in the hind legs, except for six genes that were not expressed in the males. RT-qPCR analysis showed upregulation and higher relative expression of HlonNPC2-1, HlonNPC2-3, HlonNPC2-6, and HlonNPC2-8 when stimulated by ammonium hydroxide, whereas the others were downregulated and demonstrated lower relative expression. These results further support the putative role of NPC2s as a new odorant carrier in ticks and present 12 promising candidate genes for understanding tick olfactory communication, enriching the data on these genes, especially outside the genus Ixodes. 

Identification and expression of potential olfactory-related genes related to Niemann–Pick C2 protein and ionotropic receptors in Haemaphysalis longicornis

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Identification and expression of potential olfactory-related genes related to Niemann–Pick C2 protein and ionotropic receptors in Haemaphysalis longicornis