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. 2022 Dec 12;23(24):15775.
doi: 10.3390/ijms232415775.

Olfactory Gene Families in Scopula subpunctaria and Candidates for Type-II Sex Pheromone Detection

Ting-Ting Yuan  1   2 , Zi-Jun Luo  1 , Zong-Xiu Luo  1 , Xiao-Ming Cai  1 , Lei Bian  1 , Chun-Li Xiu  1 , Nan-Xia Fu  1 , Zong-Mao Chen  1 , Long-Wa Zhang  2 , Zhao-Qun Li  1
Affiliations

Olfactory Gene Families in Scopula subpunctaria and Candidates for Type-II Sex Pheromone Detection

Ting-Ting Yuan et al. Int J Mol Sci. .

Abstract

Scopula subpunctaria, an abundant pest in tea gardens, produce type-II sex pheromone components, which are critical for its communicative and reproductive abilities; however, genes encoding the proteins involved in the detection of type-II sex pheromone components have rarely been documented in moths. In the present study, we sequenced the transcriptomes of the male and female S. subpunctaria antennae. A total of 150 candidate olfaction genes, comprising 58 odorant receptors (SsubORs), 26 ionotropic receptors (SsubIRs), 24 chemosensory proteins (SsubCSPs), 40 odorant-binding proteins (SsubOBPs), and 2 sensory neuron membrane proteins (SsubSNMPs) were identified in S. subpunctaria. Phylogenetic analysis, qPCR, and mRNA abundance analysis results suggested that SsubOR46 may be the Orco (non-traditional odorant receptor, a subfamily of ORs) of S. subpunctaria. SsubOR9, SsubOR53, and SsubOR55 belonged to the pheromone receptor (PR) clades which have a higher expression in male antennae. Interestingly, SsubOR44 was uniquely expressed in the antennae, with a higher expression in males than in females. SsubOBP25, SsubOBP27, and SsubOBP28 were clustered into the moth pheromone-binding protein (PBP) sub-family, and they were uniquely expressed in the antennae, with a higher expression in males than in females. SsubOBP19, a member of the GOBP2 group, was the most abundant OBP in the antennae. These findings indicate that these olfactory genes, comprising five candidate PRs, three candidate PBPs, and one candidate GOBP2, may be involved in type II sex pheromone detection. As well as these genes, most of the remaining SsubORs, and all of the SsubIRs, showed a considerably higher expression in the female antennae than in the male antennae. Many of these, including SsubOR40, SsubOR42, SsubOR43, and SsubIR26, were more abundant in female antennae. These olfactory and ionotropic receptors may be related to the detection of host plant volatiles. The results of this present study provide a basis for exploring the olfaction mechanisms in S. subpunctaria, with a focus on the genes involved in type II sex pheromones. The evolutionary analyses in our study provide new insights into the differentiation and evolution of lepidopteran PRs.

Keywords: Scopula subpunctaria; olfactory gene; sex pheromone perception; transcriptomic analysis; type-II sex pheromone.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Phylogenetic analysis of SsubORs with other lepidopteran insects. The percentages on the branches show the bootstrap values. The group in purple was classified as “Orco”. The group in green was classified as “PRs for both types I and II”. The group in red was classified as “PRs especially for type-II”. The phylogenetic tree was constructed in PhyML3.1 using the maximum likelihood method.
Figure 2
Figure 2
Phylogenetic analysis of SsubOBPs with other lepidopteran insects. (A) Phylogenetic analysis of all SsubOBPs with other lepidopteran insects. (B) Phylogenetic analysis of candidate SsubPBPs and SsubGOBPs with other lepidopteran insects. The percentages on the branches show the bootstrap values. The group in purple was classified as “PBP”. The group in green was classified as “Minus-C”. The group in red was classified as “GOBP”. The dashed part was classified as “Plus-C”. The phylogenetic tree was constructed in PhyML3.1 using the maximum likelihood method.
Figure 3
Figure 3
Phylogenetic analysis of SsubIRs with other lepidopteran insects. The percentages on the branches show the bootstrap values. The group in purple was classified as “IR25a/IR8a”. The group in red was classified as “IR75”. The phylogenetic tree was constructed in PhyML3.1 using the maximum likelihood method.
Figure 4
Figure 4
Tissue expression profile of SsubORs. A, antenna; H, head; B, body without antennae, head, legs, or pheromone gland; L, leg; Pg, pheromone gland. The black columns represent female moths. The grey columns represent male moths. The expression levels are relative to those in female antennae.
Figure 5
Figure 5
Tissue expression profile of SsubIRs, SsubCSPs, SsubOBPs and SsubSNMPs. (A): Expression profiles of SsubIRs. (B): Expression profiles of SsubCSPs. (C): Expression profiles of SsubOBPs. (D): Expression profiles of SsubSNMPs. A, antenna; H, head; B, body without antennae, head, legs, or pheromone gland; L, leg; Pg, pheromone gland. The black columns represent female moths. The grey columns represent male moths. The expression levels are relative to those in female antennae.
Figure 6
Figure 6
Expression levels of ORs, OBPs, CSPs, and IRs in Scopula subpunctaria antennae based on the FPKM values. (A): FPKM values of ORs in S. subpunctaria antennae. (B): FPKM values of OBPs in S. subpunctaria antennae. (C): FPKM values of CSPs in S. subpunctaria antennae. (D): FPKM values of IRs in S. subpunctaria antennae. FA, antennae of female individuals; MA, antennae of male individuals.
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