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Article

Genome-Wide Identification, Evolution, and Female-Biased Expression Analysis of Odorant Receptors in Tuta absoluta (Lepidoptera: Gelechiidae)

by
Cong Huang
1,2,†,
Xiaolan Ou
1,2,†,
Yusheng Wang
2,
Yanan Zhou
2,
Guifen Zhang
2,
Wanxue Liu
2,
Fanghao Wan
2,
Hongbo Jiang
1,* and
Yibo Zhang
2,*
1
Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400716, China
2
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Life 2024, 14(7), 872; https://doi.org/10.3390/life14070872
Submission received: 19 May 2024 / Revised: 9 July 2024 / Accepted: 10 July 2024 / Published: 12 July 2024
(This article belongs to the Special Issue Recent Advances in Chemosensory-Based Behaviorally, Physiologically, and Molecularly Manipulated Technology of Pest Insects)
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Abstract

:
The tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), is a highly destructive invasive pest targeting Solanaceae crops. Its olfactory system plays a crucial role in host location, mate finding, and other behavioral activities. However, there is a notable gap in the literature regarding the characterization of its chemosensory genes. In this study, we conducted a genome-wide identification of 58 odorant receptors (ORs) of T. absoluta. The identified ORs exhibit coding sequence (CDS) lengths ranging from 1062 bp to 1419 bp, encoding proteins of 354 to 473 amino acids. Gene structure analysis showed that the majority of these ORs consist of five, seven, eight, or nine exons, collectively representing 67% of the total ORs identified. Through chromosomal mapping, we identified several tandemly duplicate genes, including TabsOR12a, TabsOR12b, TabsOR12c, TabsOR21a, TabsOR21b, TabsOR34a, TabsOR34b, TabsOR34c, TabsOR62a, and TabsOR62b. The phylogenetic analysis indicated that six TabsORs were clustered within the lepidopteran sex pheromone receptor clade, while an expansion clade containing ten TabsORs resulted from tandem duplication events. Additionally, five TabsORs were classified into a specific OR clade in T. absoluta. Furthermore, through RNA-Seq and RT-qPCR analyses, we identified five TabsORs (TabsOR21a, TabsOR26a, TabsOR34a, TabsOR34c, and TabsOR36) exhibiting female-antennae-biased expression. Our study provides a valuable foundation to further investigations into the molecular and ecological functions of TabsORs, particularly in relation to oviposition behavior. These findings provide foundational data for the future exploration of the functions of female-biased expression OR genes in T. absoluta, thereby facilitating the further development of eco-friendly attract-and-kill techniques for the prevention and control of T. absoluta.

1. Introduction

Insects rely heavily on their chemosensory system to locate mating partners, host plants, food, and oviposition sites. This system also aids in the identification of toxic compounds, evasion of natural enemies, and facilitation of communication [1,2]. Consequently, chemical communication plays a vital role in insect dispersal, reproductive success, and the extent of the damage they inflict. Central to this process are the odorant receptors (ORs), a crucial gene family within the insect chemosensory system. Insect ORs are composed of a conserved coreceptor (ORco) and a diverse array of odorant receptors (ORx). These receptors form the ORx–ORco complex, which acts as a ligand-gated cation channel in olfactory sensory neurons. This complex is responsible for transducing the chemical signals to electrical signals, ultimately eliciting corresponding behavioral responses [3].
The chemosensory mechanisms of female and male insects exhibit notable distinctions. In many insect species, males rely on olfaction to detect and respond to the sex pheromones released by females, facilitating mate finding. Conversely, females predominately locate appropriate oviposition locations by detecting host plant volatiles [4]. This sexual dimorphism extends to the differential expression profiles of OR genes between female and male insects [5]. Across various insect orders, a large number of male-biased PRs have been deorphanized and are primarily responsible for the perception of female sex pheromones. Examples include AlucOR4 of Apolygus lucorum in the Hemiptera [6], SfruOR13 and SfruOR16 of Spodoptera frugiperda in the Lepidoptera [7], CchlOR18 and CchlOR47 of Campoletis chlorideae in the Hymenoptera [8], HparOR14 of Holotrichia parallela in the Coleoptera [9], and MdesOR115 of Mayetiola destructor in the Diptera [10].
Conversely, the expressions of female-biased ORs predominately respond to host plant volatiles and are often associated with egg-laying behaviors. Instances of such ORs have been documented in Aedes aegypti [11], Aethina tumida [12], Bactrocera dorsalis [13], Campoletis chlorideae [14], and Anastatus japonicus [15]. In moths, female-biased ORs also play a role in detecting oviposition signals. For instance, in Helicoverpa assulta, the oviposition behavior regulated by host plant volatiles is mediated by two female-biased odorant receptors, HassOR67 and HassOR31 [16,17]. Similarly, in Helicoverpa armigera, the female-specific odorant receptor HarmOR56 mediates oviposition deterrence [18]. Comparable observations have been made in Plutella xylostella [19] and Manduca sexta [20].
The tomato leafminer Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae), native to Peru, South America, at present, has emerged and inflicted damage in more than 100 countries globally [21] and poses a significant threat to the sustainability and productivity of the tomato industry. When infestations occur, they can lead to significant losses in tomatoes, ranging from 80% to 100% of the yield [22]. Although insecticides have historically been the primary method of control, their heavy and frequent use has contributed to the development of resistance in T. absoluta populations [23,24]. As a more environmentally friendly alternative, attract-and-kill strategies have garnered attention. However, their efficacy is limited by factors such as the polyandrous mating behavior of males and the high fertility rates of females [25]. Consequently, there is an urgent need for the development of attractants targeting both sexes, with a particular emphasis on attracting females.
Previous studies have identified numerous volatile compounds from host plants that elicit the electrophysiological responses in the antennae of female T. absoluta [26,27,28]. However, the specific compounds capable of attracting females remain unclear. In recent years, a reverse chemical-ecology-based approach has been employed to discover attractants and repellents. This approach involves identifying and screening active compounds by elucidating the functions of odorant receptors [29,30,31,32,33]. However, the current understanding of the types, quantities, and expression patterns of the odorant receptors in T. absoluta is limited. This knowledge gap significantly impedes the development of female attractants.
In the present study, we conducted a comprehensive genome-wide analysis of OR genes, with a specific focus on identifying the female-biased expression ORs in T. absoluta. A total of 58 ORs were successfully identified, and their gene structures and chromosomal locations were systematically analyzed. Subsequently, we constructed a phylogenetic tree incorporating the OR genes from four lepidopteran insects (Bombyx mori, Helicoverpa armigera, and Spodoptera littoralis) to explore their evolutionary relationships. Additionally, we utilized transcriptome data to calculate the expression profiles of ORs across different tissues in female and male adults. Furthermore, the high expression levels of the identified ORs in the antennae of female adults were validated by a real-time reverse transcription-polymerase chain reaction (RT-qPCR) analysis. Our findings provide valuable insights into the evolutionary dynamics of OR genes in T. absoluta and provide essential data support for future endeavors aimed at developing female attractants.

2. Materials and Methods

2.1. Identification of OR Genes in T. absoluta

The protein sequences of ORs from three lepidopteran insects (B. mori, S. littoralis, and H. armigera) were collected from the published articles in which these ORs had been previously identified from their respective genomes [34,35,36]. These sequences were utilized as queries in iterative BLASTP searches against T. absoluta genomes [37], using an e-value threshold of 1 × 10−5. Subsequently, candidate OR genes were subjected to a local command line HMMER (version 3.1b2) search against the Pfam-A database, specifically targeting the 7tm_6 (PF02949) or 7tm_4 (PF13853) hidden Markov model (HMM) profiles for further validation.

2.2. Gene Structure Analysis and Chromosomal Location of OR Genes

The Generic Feature Format Version 3 (GFF3) format file containing all OR genes was initially extracted and subsequently submitted to the online web servers GSDS 2.0 for visualization and drawing of gene structures. Additionally, an in-house Python script (https://github.com/jackiexls/ChrLocPlotter, accessed on 10 June 2022) was used to generate distribution maps depicting the chromosomal locations of OR genes.

2.3. Phylogenetic Analysis

To investigate the evolutionary relationship of OR genes between T. absoluta and other lepidopteran moths, a total of 217 OR genes from four species (58 from T. absoluta, 54 from B. mori, 45 from H. armigera, and 60 from S. littoralis) were included in the phylogenetic analysis. Multiple sequence alignment of the protein sequences was performed using MAFFT v7 [38] with default parameters, followed by trimming of the alignment sequences using trimAl v1.2 [39] with the parameter “-automated1”. A maximum likelihood evolutionary tree was constructed using RAxML (version 8.2.12) [40], with the best-fit model (JTT + G + F) estimated with ProtTest3 software v3.4.2 [41]. Visualization and labeling of the phylogenetic tree were conducted using FigTree software v1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/, accessed on 10 June 2022) and Adobe Illustrator CC 2017.

2.4. Expression Profiles of 58 TabsORs in Female and Male Antennae

The expression levels of 58 TabsORs in the antennae of female and male adults were determined using transcriptome data (unpublished). Paired-end clean reads were mapped to the T. absoluta genome using HISAT2 version 2.2.1 [42]. Fragments per kilobase of transcript per million mapped reads (FPKMs) were calculated using StringTie version 2.1.7 software [43]. Subsequently, the FPKM values were transformed to log2(FPKM + 1) and utilized as inputs for generating a histogram in Excel 2021.

2.5. RT-qPCR Verification of the Candidate Female-Antennae-Biased Expression ORs

Antennae samples from female and male adults (1 to 2 days old) were collected and immediately snap-frozen in liquid nitrogen before storage at −80 °C. Total RNA was extracted using a Total RNA extraction Micro kit (Genstone Biotech, Beijing, China). The reverse-transcription reaction was performed using a Hifair® III 1st Strand cDNA Synthesis SuperMix for qPCR (gDNA digester plus) (Yeasen Biotechnology, Shanghai, China). In the first step, 15 μL of reaction mixture including 1 μg of total RNA, 3 μL 5×gDNA digester Mix, and RNase-free H2O was used to remove residual genomic DNA contamination in RNA templates. In the second step, a total of 20 μL of reaction mixture including 15 μL of reaction mixture from the first step and 5 μL 4×Hifair® III SuperMix Plus was used to perform the reverse transcription and generate the cDNA.
The resulting cDNA templates were diluted 10-fold with ddH2O, and 0.5 μL of the diluted cDNA was used as template for subsequent RT-qPCR analysis. RT-qPCR was conducted on an ABI 7500 Real-Time PCR System (Applied Biosystems, Foster City, CA, USA) with Hieff™ qPCR SYBR® Green Master Mix (Low Rox Plus) (Yeasen, Shanghai, China) to quantify the relative expression of TabsOR genes. RT-qPCR reactions were performed in a total volume of 10 µL, comprising an initial denaturation step at 95 °C for 5 min, followed by 40 cycles of denaturation at 95 °C for 10 s, and extension at 60 °C for 34 s, with a dissociation curve analysis. The process for each sample was performed in three duplicates. The relative expression levels of TabsOR genes were determined using the 2−∆∆CT method and normalized by ribosomal protein L5 (RPL5) expression. All primers used are listed in Supplementary Table S1.

2.6. Statistical Analysis

The expression levels of both the FPKM values and RT-qPCR results were analyzed by Student’s t-test. Data are presented as the mean ± standard error (mean ± SEM). Differences were considered statistically significant at p < 0.05 and highly significant at p < 0.01.

3. Results

3.1. Identification and Gene Structure Analysis of OR Genes in T. absoluta

A comprehensive search for the OR genes in T. absoluta was conducted using 159 OR genes from B. mori, H. armigera, and S. littoralis as the queries in a BLASTP search (e-value < 1 × 10−5) against the genome of T. absoluta. Subsequently, the best BLAST hits were used to identify the conserved domains using hidden Markov models (HMMs) through a hmmscan search against the Pfam database. A total of 58 TabsOR genes harboring the 7tm_6 (PF02949) or 7tm_4 (PF13853) HMM profile were successfully identified. The coding sequence (CDS) lengths of the 58 TabsOR genes ranged from 1062 bp to 1419 bp, encoding proteins consisting of 354 to 473 amino acids (Supplementary Table S2).
The analysis of the gene structures of the TabsOR genes revealed variation in the number of exons, ranging from 1 to 13. Notably, TabsOR9 has only one exon structure, while TabsOR34c and TabsOR36 possess three exons each. Furthermore, four genes (TabsOR12a, TabsOR2, TabsOR21a, and TabsOR3) have four exons, fifteen genes (TabsOR12b, TabsOR12c, TabsOR14, TabsOR21b, TabsOR27, TabsOR28, TabsOR32, TabsOR34a, TabsOR34b, TabsOR35, TabsOR37, TabsOR44, TabsOR45, TabsOR62a, and TabsOR62b) have five exons, five genes (TabsOR11, TabsOR25, TabsOR33, TabsOR47, and TabsOR49) have six exons, eight genes (TabsOR15, TabsOR30, TabsOR31, TabsOR39, TabsOR5, TabsOR53, TabsOR8, and TabsORco) have seven exons, eight genes (TabsOR16, TabsOR22, TabsOR23, TabsOR29, TabsOR3, TabsOR46, TabsOR48, and TabsOR7) have eight exons, eight genes (TabsOR13, TabsOR17, TabsOR18, TabsOR26a, TabsOR26b, TabsOR4, TabsOR41, and TabsOR6) have nine exons, four genes (TabsOR19, TabsOR24, TabsOR40, and TabsOR42) have ten exons, and two genes (TabsOR10 and TabsOR20) have eleven exons. TabsOR1 displayed the most complex structure, with 13 exons (Figure 1).

3.2. Chromosome Location of TabsOR Genes

All 58 TabsOR genes were mapped to the chromosomes of T. absoluta. The distribution of the TabsOR genes across the genome revealed that they are located on 19 different chromosomes (Figure 2). Notably, individual chromosomes exhibit varying numbers of TabsOR genes. Chromosomes 1, 3, 8, 11, and 13 each harbor a single TabsOR gene, while chromosomes 6, 12, 18, 22, and 27 contain two TabsOR genes each (Figure 2). Additionally, three TabsOR genes are located on chromosomes 2, 4, 14, 17, and 21, and four TabsOR genes are located on chromosome 9 and 23, respectively (Figure 2). Chromosomes 7 and 10 exhibit the highest number of TabsOR genes, with ten TabsOR genes located on each chromosome (Figure 2).

3.3. Phylogenetic Analysis of ORs

To explore the evolutionary relationship of the OR genes in T. absoluta with those of other lepidopteran species, a phylogenetic analysis was conducted using a dataset comprising 217 OR genes from T. absoluta, B. mori, H. armigera, and S. littoralis. The resulting phylogenetic tree revealed distinct clades representing different evolutionary lineages of OR genes. A subset of OR genes from T. absoluta, including TabsOR4, TabsOR7, TabsOR8, TabsOR17, TabsOR26a, and TabsOR26b, clustered together in a well-defined clade corresponding to the lepidopteran sex pheromone receptor clade (Figure 3). This clustering pattern suggests a shared evolutionary history and functional specialization related to sex pheromone perception in these genes.
Another notable observation was the presence of expanded OR gene families specific to T. absoluta, as evidenced by the clustering of genes such as TabsOR34a, TabsOR34b, TabsOR34c, TabsOR21a, TabsOR21b, TabsOR11, TabsOR62a, TabsOR62b, TabsOR25, and TabsOR44 (Figure 3). This expansion of the OR gene families may reflect adaptations to specific ecological niches or evolutionary pressures unique to T. absoluta. Furthermore, a distinct clade composed of TabsOR35, TabsOR14, TabsOR12a, TabsOR12b, and TabsOR12c genes was identified, suggesting the formation of a specific OR clade within T. absoluta (see Figure 3). The presence of this clade may indicate the functional divergence or specialization of these OR genes in T. absoluta compared to other lepidopteran species.

3.4. Expression of TabsOR Genes in Antennae of Female and Male Adults

The expression levels of the 58 TabsOR genes were assessed using the RNA-Seq data, allowing for a comparative analysis of the gene expression between female and male antennae tissues. The log-transformed fragments per kilobase of transcript per million mapped reads (log2(FPKM + 1)) values were utilized to facilitate the comparison of TabsOR gene expression levels. The analysis revealed significant differences in TabsOR gene expression between female and male antennae. Specifically, the genes exhibited significantly higher expression levels in female antennae than in male antennae. These genes include TabsOR11, TabsOR21a, TabsOR21b, TabsOR22, TabsOR26a, TabsOR26b, TabsOR34a, TabsOR34b, TabsOR34c, and TabsOR36 (Figure 4). Conversely, five TabsOR genes had higher expression levels in male antennae, including TabsOR12c, TabsOR14, TabsOR17, TabsOR4, and TabsOR8 (Figure 4).

3.5. RT-qPCR Analysis of Candidate Female-Antennae-Biased Expression ORs

To validate the differential expression of the TabsOR genes observed between female and male antennae and to corroborate the findings from the RNA-Seq analysis, we selected the ten OR genes exhibiting high expression levels in female antennae for an RT-qPCR analysis. The results showed that the expression levels of TabsOR21a, TabsOR26a, TabsOR34a, TabsOR34c, and TabsOR36 were consistent with the RNA-Seq data, exhibiting significantly higher expression in female antennae compared to male antennae (Figure 5). Conversely, no significant differences in the expression levels were observed for TabsOR11, TabsOR22, TabsOR21b, TabsOR26b, or TabsOR34b between the female and male antennae (Figure 5).

4. Discussion

Insects rely heavily on their acute olfactory system to locate food sources, potential mates, and suitable oviposition sites, with OR genes playing a crucial role in these olfactory processes. Therefore, a better understanding of the olfactory system as well as the female-biased ORs in T. absoluta, a highly invasive and destructive pest, could contribute to the development of more effective and sustainable pest control strategies, such as attract-and-kill techniques or other environmentally friendly control methods. Despite the crucial role of OR genes, the understanding of this gene family remains limited in T. absolute. In this study, we conducted a comprehensive analysis of the OR gene repertoire in T. absoluta using genomic and transcriptomic data. Previous research has highlighted substantial variations in the numbers and sequences of insect OR genes, attributed to their ability to recognize the diverse odor signals present in different ecological habitats. The identification of 58 OR genes in T. absoluta represents a significant step toward elucidating the molecular basis of olfaction in this pest species. The observed number of OR genes in T. absoluta is similar to the number observed in other insect species; for instance, it is comparable to the OR gene count in B. mori (54 ORs), Spodoptera exigua (53 ORs), and S. littoralis (60 ORs). However, it deviates from the counts observed in certain insect species, such as Cydia pomonella (85 ORs) and Spodoptera frugiperda (69 ORs), while being greater than the count in H. armigera (45 ORs).
Understanding the gene structure is crucial for exploring the evolutionary relationships and functional diversity of OR genes. In the current study, we analyzed the intron-exon organization of TabsOR genes, revealing a range of one to thirteen exons. Notably, genes with five coding exons were the most abundant, comprising a total of 15 OR genes, followed by genes with seven, eight, or nine coding exons. Previous research has demonstrated that the gene structure can have a significant effect on gene function [44,45], suggesting the potential for both the functional conservation and diversity of the TabsOR genes.
The chromosomal distribution of genes can provide valuable insights into their evolutionary relationships and functional characteristics. Previous studies have demonstrated that the OR genes in insects are often arranged in tightly clustered formations on chromosomes, predominantly as a result of tandem duplication events. This clustering suggests potential functional similarities among the duplicated genes [45,46,47,48,49]. For example, in C. pomonella, the tandemly duplicated OR genes CpomOR3a and CpomOR3b on chromosome 17 exhibit synergistic and complementary functions in the recognition of host plants and mates [49].
In our study, we identified five tandemly duplicated OR gene clusters in T. absoluta. Specifically, TabsOR34a, TabsOR34b, and TabsOR34c are tandemly arranged on chromosome 7, while TabsOR62a and TabsOR62b are in tandem on chromosome 9. Additionally, TabsOR12a, TabsOR12b, and TabsOR12c form a tandem cluster on chromosome 10, along with TabsOR26a and TabsOR26b. Moreover, TabsOR21a and TabsOR21b are tandemly duplicated on chromosome 22. The similar research results in other insects indicate that tandemly duplicated OR genes play an important role in the adaptation to their specific environmental conditions [49]. Therefore, our results suggest that these tandemly duplicated TabsOR genes may play crucial roles in odor recognition, potentially contributing to the species’ capacity to adapt to its environment.
Previous studies have indicated that the orthologous genes clustered within the same clade often exhibit similar biological functions. To explore the evolutionary relationships and functions of TabsOR genes, we selected OR genes from the well-characterized species B. mori, S. littoralis, and H. armigera to reconstruct the phylogenetic tree [34,35,36]. Our analysis revealed that six TabsOR genes—TabsOR4, TabsOR7, TabsOR8, TabsOR17, TabsOR26a, and TabsOR26b—were cluster in the sex pheromone receptor clade, suggesting their potential involvement in sex pheromone recognition. In another clade, the TabsOR genes have exhibit expansion due to the tandem duplication of several genes, including TabsOR34a, TabsOR34b, TabsOR34c, TabsOR21a, TabsOR21b, TabsOR11, TabsOR62a, TabsOR62b, TabsOR25, and TabsOR44. Previous studies have suggested that the ORs within this clade (Clade K) are rapidly evolving OR genes with well-characterized functions. For instance, in B. mori, BmorOR29 serves as a receptor for (±)-linalool, while BmorOR56 detects (Z)-jasmone [34]. In H. armigera, HarmOR27 is the receptor of butyl salicylate, HarmOR31 is the receptor of (Z)-3-hexenyl acetate, HarmOR40 is the receptor of geranyl acetate, and HarmOR55 is the receptor of (E)-nerolidol [36]; in S. littoralis, SlitOR29 is the receptor of ocimene [35]. The results suggest that the TabsOR genes within this clade may have a broad binding spectrum, indicating their potential roles in detecting diverse odorants. Furthermore, we identified a specific cluster of TabsOR genes comprising TabsOR35, TabsOR14, TabsOR12a, TabsOR12b, and TabsOR12c, suggesting their association with the unique biological characteristics of T. absoluta.
The expression patterns of genes are intricately linked to their functions [50]. In the case of insect ORs, the sex-biased expressions of ORs in antennae are very common. Typically, male-biased ORs are involved in detecting the sex pheromones released by females [8], whereas the female-biased ORs are associated with recognizing oviposition-related odors. Through the analysis of antenna transcriptome data and RT-qPCR detection, we identified TabsOR21a, TabsOR26a, TabsOR34a, TabsOR34c, and TabsOR36 in the female-biased expression of ORs. It is worth noting that there is a large deviation in the expression trend of the TabsOR26b gene between the RNA-Seq and RT-qPCR results; we inferred that the reason may be that the sequences of the TabsOR26a and TabsOR26b genes are too similar. Because RNA-Seq relies on the ability to uniquely map reads to the genome or transcriptome, when genes are highly similar, reads can be incorrectly assigned to one gene or the other, leading to biased expression estimates. Finally, we speculated that the female-biased expression of OR genes may be involved in the detection of oviposition-related odor. However, further studies should be performed to determine the detailed functions of the identified OR genes in mediating specific behaviors such as mating and oviposition.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/life14070872/s1, Table S1: Sequences of primers used for RT-qPCR studies; Table S2: Sequences of TabsOR genes.

Author Contributions

Conceptualization, C.H. and X.O.; methodology, C.H. and X.O.; software, C.H.; validation, C.H. and X.O.; formal analysis, C.H., X.O., Y.W. and Y.Z. (Yanan Zhou); investigation, C.H. and X.O.; resources, C.H., X.O., Y.W., Y.Z. (Yanan Zhou), G.Z., W.L. and F.W.; data curation, C.H. and X.O.; writing—original draft preparation, C.H. and X.O.; writing—review and editing, C.H. and X.O.; visualization, C.H. and X.O.; supervision, H.J. and Y.Z. (Yibo Zhang); project administration, H.J. and Y.Z. (Yibo Zhang); funding acquisition, H.J. and Y.Z. (Yibo Zhang). All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (2022YFC2601000 and 2021YFD1400200).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data described in the current work are available through access to the text or Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

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Life 14 00872 g001
Figure 1. Gene structure of TabsOR genes. Blue boxes represent exons, while black lines represent introns.
Figure 1. Gene structure of TabsOR genes. Blue boxes represent exons, while black lines represent introns.
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Figure 2. Chromosomal mapping of OR genes in T. absoluta.
Figure 2. Chromosomal mapping of OR genes in T. absoluta.
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Figure 3. Phylogenetic tree of ORs in four lepidopteran species. For the tip labels: ORs in T. absoluta are labeled in red, those in B. mori are labeled in blue, those in H. armigera are labeled in green, and those in S. littoralis are labeled in black. For the branch clades: the red-shaded clade is a sex pheromone clade.
Figure 3. Phylogenetic tree of ORs in four lepidopteran species. For the tip labels: ORs in T. absoluta are labeled in red, those in B. mori are labeled in blue, those in H. armigera are labeled in green, and those in S. littoralis are labeled in black. For the branch clades: the red-shaded clade is a sex pheromone clade.
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Figure 4. Expression levels in FPKM for TabsOR genes in the antennae of female and male adults. Asterisks indicate highly significant differences between mated females and males (** p < 0.01) (Student’s t-test).
Figure 4. Expression levels in FPKM for TabsOR genes in the antennae of female and male adults. Asterisks indicate highly significant differences between mated females and males (** p < 0.01) (Student’s t-test).
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Figure 5. Expression profile of TabsOR genes in the antennae of female and male adults of T. absoluta. Asterisks indicate significant differences between mated females and males (* p < 0.05, ** p < 0.01, ns: not significant) (Student’s t-test).
Figure 5. Expression profile of TabsOR genes in the antennae of female and male adults of T. absoluta. Asterisks indicate significant differences between mated females and males (* p < 0.05, ** p < 0.01, ns: not significant) (Student’s t-test).
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MDPI and ACS Style

Huang, C.; Ou, X.; Wang, Y.; Zhou, Y.; Zhang, G.; Liu, W.; Wan, F.; Jiang, H.; Zhang, Y. Genome-Wide Identification, Evolution, and Female-Biased Expression Analysis of Odorant Receptors in Tuta absoluta (Lepidoptera: Gelechiidae). Life 2024, 14, 872. https://doi.org/10.3390/life14070872

AMA Style

Huang C, Ou X, Wang Y, Zhou Y, Zhang G, Liu W, Wan F, Jiang H, Zhang Y. Genome-Wide Identification, Evolution, and Female-Biased Expression Analysis of Odorant Receptors in Tuta absoluta (Lepidoptera: Gelechiidae). Life. 2024; 14(7):872. https://doi.org/10.3390/life14070872

Chicago/Turabian Style

Huang, Cong, Xiaolan Ou, Yusheng Wang, Yanan Zhou, Guifen Zhang, Wanxue Liu, Fanghao Wan, Hongbo Jiang, and Yibo Zhang. 2024. "Genome-Wide Identification, Evolution, and Female-Biased Expression Analysis of Odorant Receptors in Tuta absoluta (Lepidoptera: Gelechiidae)" Life 14, no. 7: 872. https://doi.org/10.3390/life14070872

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