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Article

Genome-Wide Identification of the Genes of the Odorant-Binding Protein Family Reveal Their Role in the Olfactory Response of the Tomato Leaf Miner (Tuta absoluta) to a Repellent Plant

by
Ruixin Ma
†,
Donggui Li
†,
Chen Peng
,
Shuangyan Wang
,
Yaping Chen
,
Furong Gui
and
Zhongxiang Sun
*
State Key Laboratory of Conservation and Utilization of Biological Resources of Yunnan, College of Plant Protection, Yunnan Agricultural University, Kunming 650201, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(1), 231; https://doi.org/10.3390/agronomy14010231
Submission received: 17 December 2023 / Revised: 19 January 2024 / Accepted: 20 January 2024 / Published: 22 January 2024
(This article belongs to the Special Issue Adaptation and Responses of Insects under Abiotic, Biotic and Xenobiotic Constraints)
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Abstract

:
The remarkable biological and evolutionary adaptations of insects to plants are largely attributed to the powerful chemosensory systems of insects. The tomato leaf miner (Tuta absoluta) is a destructive invasive pest with a global distribution that poses a serious threat to the production of nightshade crops, especially tomatoes. Functional plants can attract or repel insect pests by releasing volatiles that interact with the olfactory system of insects, thereby reducing the damage of insect pests to target crops. However, there is limited research on the interaction between T. absoluta olfactory genes and functional plants. In this study, 97 members of the putative odorant-binding protein (OBP) family have been identified in the whole genome of T. absoluta. Phylogenetic analysis involving various Lepidopteran and Dipteran species, including D. melanogaster, revealed that OBP gene families present conserved clustering patterns. Furthermore, the Plus-C subfamily of OBP showed extremely significant expansion. Moreover, the expression levels of the OBP genes varied significantly between different developmental stages; that is, the highest number of OBP genes were expressed in the adult stage, followed by the larval stage, and fewer genes were expressed in high abundance in the egg stage. On the other hand, through a Y-tube olfactometer, we identified a functional plant—Plectranthus tomentosa—that significantly repels adult and larval T. absoluta. Finally, we screened the OBP genes in response to tomato and P. tomentosa volatiles at the genomic level of T. absoluta using RT-qPCR. These results laid a good foundation for controlling T. absoluta with functional plants and further studying olfactory genes.

1. Introduction

Agricultural pests are surrounded by various volatile substances in the farmland ecosystem, including plant volatiles, insect volatiles, etc. Insects can use the complex olfactory system to identify and sense odor molecules so that insects can locate oviposition sites, mates, and threats, thus helping them to survive and reproduce [1,2]. The olfactory proteins of insects mainly include odorant-binding proteins (OBPs), olfactory receptors, gustatory receptors, and inotropic receptors. OBPs are expressed in the olfactory sensillium, which transport odor molecules to olfactory receptors on the surfaces of neurons and are the first biochemical reaction for insects to specifically recognize external odors, which is of great significance for insects to communicate with the outside world [3,4,5]. Further studying the function of OBPs is crucial for revealing the interactions between insects and host plants.
Insects can use the olfactory system to recognize external volatiles and then make a taxis choice or escape behavior [6]. For example, tobacco cutworm (Spodoptera litura) and black cutworm (Agrotis ipsilon) can use OBPs to respond to a variety of sex pheromones and plant volatiles [7,8]. Plant volatiles are volatile organic chemicals (VOCs) produced by the leaves, flowers, and fruits of plants [9]. These volatile secondary substances include terpenes, alcohols, aldehydes, hydrocarbons, ketones, organic acids, and other organic compounds with a relative molecular weight of 100~300 kDa; they do not participate directly in the growth and development of plants but are the result of the interaction between plants, organisms and abiotics [10]. The insect preference for different host plants is very different, and this preference for selection is largely related to plant volatiles [11]. Functional plants refer to a class of plants that can play ecological functions in agriculture and forest ecosystems, including nectar source plants, attracting plants, associated plants, insect-repellent plants, barrier plants, deposit plants, etc. [12]. In modern biological control, functional plants are considered an important means of the ecological control of pests [13]. For example, the intercropping of high clover (Trifolium incarnatum) with cabbage (Brassica oleracea) significantly reduced the number of eggs deposited by diamondback moths (Plutella xylostella) in cabbage [14]; vetiver grass (Vetiveria zizanioides) released a large number of terpenoids, which significantly induced the transfer of female adult rice striped stem borers (Chilo suppressalis) from rice to vetiver to lay eggs [15]; and the insect-repellent plants basil (Ocimum basilicum) and citronella (Mosla chinensis) are effective repellents of cotton leafworm (Spodoptera litura), cabbage webworm (Hellula undalis), and flea beetle (Phyllotreta sinuata) from B. oleracea [16]. Although previous research has focused primarily on identifying repellent or attractant plants, studies exploring how insects’ olfactory systems respond to these plants or their volatile components remain limited.
The tomato leaf miner Tuta absoluta (Meyrick) is an invasive alien pest that causes great harm worldwide and is known as the ‘Ebola virus’ on tomatoes (Solanum lycopersicum L.) [17]. T. absoluta has a wide range of host plants, mainly destroying nightshade crops such as tomatoes, tobacco, potatoes, etc., but also laying eggs and developing in a variety of plants in Amaranthaceae, Convolvulaceae, Legumes and Malvaceae, causing damage to host plants [18]. T. absoluta originated in Peru, South America, and was introduced into Europe in 2006. Currently, T. absoluta has invaded 103 countries and regions of the world, seriously threatening the healthy development of the world food industry [19,20]. At present, the most important control method of T. absoluta is still chemical control, which can effectively control the pest when the pest has just invaded. However, a large amount of irrational pesticide use has also led to increased resistance and brought serious harm to the agricultural ecosystem, including intensifying environmental pollution, causing excessive drug residues in agricultural products, destroying the balance of the ecosystem, reducing the number of natural enemies, etc. [21]. These adverse effects have led people to seek better methods of crop protection with environmental compatibility [22]. Currently, the use of functional plants to control T. absoluta is mainly through the toxic or repellent effects of essential oils produced by functional plants [23]. Boni et al. used plant essential oil prepared with O. basilicum to explore its inhibitory effect on the laying of T. absoluta eggs [24]. Mirella et al. studied the effects of essential oils of majoram (Origanum vulgare), bay (Laurel nobilis), O. basilicum, garlic (Allium sativum), and mint (Mentha piperita), etc., on the egg laying and larval repellent of T. absoluta [25]. However, direct application of functional plants to control T. absoluta has not been reported. Furthermore, the limited research on the olfactory system of T. absoluta, including OBPs, restricts the potential use of olfactory-based pest-control methods.
In this study, we first identified putative OBP family genes in the whole genome of T. absoluta by homologous comparison and domain-based HMMER comparison. We then identified a functional plant that significantly repels T. absoluta. Finally, real-time quantitative PCR (RT-qPCR) was used to identify genome-level OBPs in response to host tomatoes and repellent plants.

2. Materials and Methods

2.1. Insect Strains

The T. absoluta larvae were collected from Yuxi City, Yunnan Province, China (102°17′32″ E, 24°08′30″ N) in 2021 and raised in the laboratory for more than 15 generations. The larvae were fed tomato plants in fine nylon mesh cages (45 × 45 × 45) cm in an artificial climate box (MG-300A, Shanghai Yiheng Scientific Instrument Co., Ltd., Shanghai, China) under certain conditions of temperature (27 ± 0.5 °C), relative humidity RH (70 ± 5%), and photoperiod (L:D = 16:8 h). Adults were given a 10% sucrose solution (CAS: 57-50-1, 98%, Shanghai Yuanye Biotechnology Co., Ltd., Shanghai, China) as an additional supplement.

2.2. Search and Identification of Odorant-Binding Protein Family Gene in T. absoluta

The whole-genome sequence genome assembly ZJU_Tuta_1.1 (GenBank assembly number: GCA_029230345.1), GFF annotation file, total CDS sequence, and total protein sequence file of T. absoluta were downloaded from the NCBI website (https://www.ncbi.nlm.nih.gov/datasets/genome/GCA_029230345.1/, accessed on 13 June 2023). Putative odorant-binding protein (OBP) family genes in T. absoluta were identified using two approaches: homologous comparison by BLAST with TBtools [26] and domain-based HMMER comparison with BITACORA [27]. The final identification results were combined with the results of these two software, and the incomplete annotation sequences were filtered.

2.3. Phylogenetic Analysis of OBP Genes in T. absoluta

The predicted full-length protein sequences of the OBP family genes of fruit fly (Drosophila melanogaster, 51 members) were downloaded from Flybase (http://flybase.org/, accessed on 20 July 2023), and the predicted full-length protein sequences of the OBP family genes of silkworm (Bombyx mori, 20 members), fall armyworm (Spodoptera frugiperda, 15 members), cotton bollworm (Helicoverpa armigera, 20 members), and cabbage caterpillar (Pieris rapae, 19 members) were downloaded from the NCBI website. Sequence IDs for each OBP used for phylogenetic analysis are listed in Supplemental Table S1. After aligning with MAFFT software (v7.520) [28], these sequences were used for phylogenetic analysis using IQ-TREE software (v2.0) [29]. The bootstrap operation was performed 1000 times. The optimal amino acid replacement model was LG+G. Genes from the same insect are represented by the same colors. The branch colors represent the Classic (yellow), Plus-C (blue), Minus-C (green), and Dimer (purple) subfamilies, according to Rondon et al. [30].

2.4. Developmental Stage-Specific Expression Profile of TaOBPs

T. absoluta is a holometabolous insect that has egg, larva (divided into four instars), pupa, and adult stages throughout its 30–35-day life cycle [31]. The developmental stage-related BioProject (PRJNA291932) of T. absoluta (including six developmental stages: Egg (SRR2147323), Larvae stage 1 (SRR2147324), Larvae stage 2 (SRR2147319), Larvae stage 3 (SRR2147320), Larvae stage 4 (SRR2147321) and Adult (SRR2147322)) was retrieved and downloaded from the NCBI SRA database (https://www.ncbi.nlm.nih.gov/sra, accessed on 1 August 2023). Expression levels of all genes of the OBP family in T. absoluta were calculated using kallisto [32], and expression levels were displayed by heat map based on the TPM value of the gene. Image GP [33] was used to analyze the expression of OBP genes identified in different development stages of T. absoluta.

2.5. Determination of the Taxis Behavior of T. absoluta to Plectranthus tomentosa

The behavior response of T. absoluta to Plectranthus tomentosa was measured using a Y-tube olfactometer according to a previous study [34,35], with some modifications. A schematic of the Y-tube was provided in our previous study [35]. For experiments with host tomatoes as controls, the odor source of the control arm was tomato, and the odor source of the treatment arm was the P. tomentosa plant. For experiments with pure air as control, the odor source of the control arm was pure air, and the odor source of the treatment arm was the P. tomentosa plant. Fresh tomato plants and P. tomentosa plants were placed in the glass jar of the odor source (the pot was wrapped in tin foil). The flow rate of the two arms of the Y-tube was adjusted to 20 mL/min, and the air was pumped for 10 min before each measurement so that the arms of the flavor source of the Y-tube were filled with volatile information substances. For testing, thirty larvae of the first day of the third instar or fifteen eclosion females and fifteen males within three days of T. absoluta were released from the finger tube to the base of the Y-tube, and the Y-tube was placed in a black blackout box to eliminate the effect of light on the behavioral response of T. absoluta. After 15 min, the behavioral response of T. absoluta to the odor source was observed and recorded. After each measurement, the clean Y-tube was replaced and then the next test was performed. After every three tests, the orientation of the two arms of the Y-tube was changed to eliminate the error caused by the position. Bioassays were performed in a blackout chamber illuminated by an incandescent lamp (18 W, 4500 lux light intensity) above the Y-tube. The response rate is equal to the number of T. absoluta selected on one side of the plant divided by the total number of T. absoluta used in one experiment.

2.6. Induction Treatment of T. absoluta Larvae and Adults by Plant Volatiles

The induction treatment of T. absoluta by plant volatiles was tested using a directed airflow apparatus based on previous methods [35] with some modifications. Fresh tomato or repellent plants were placed in the glass jar of the odor source (the pot was wrapped in tin foil), and air purified by activated carbon and moistened by distilled water was continuously injected by an air compressor (QC-1S; Beijing Municipal Institute of Labour Protection, Beijing, China), with the gas flow adjusted to 20 mL/min. The breathable box containing the third instar larvae or adult of T. absoluta was placed in the glass jar of the odor source and treated for 6 h. For larvae, five homogeneous larvae of the first day of the third instar were used for each treatment. For adults, ten females and ten males within three days of emergence were used for each treatment. Each experiment was carried out with five biological replicates. In the blank control group, no plants were placed in the glass jar of the odor source; that is, the insects were treated with pure air.

2.7. Total RNA Extraction and Reverse Transcription

After exposure to volatiles for 6 h, T. absoluta larvae and adults were collected for subsequent experiments. Total RNA from every five larvae was extracted with the Eastep™ Universal RNA Extraction Kit (catalog number: LS1030, Promega Corporation, Madison, WI, USA). For adults, the antennae and part of the head tissue connecting to the antennae were cut off with a thin blade under an anatomical mirror and quickly transferred to liquid nitrogen, and the tissues of every 10 females and 10 males were mixed into one sample for total RNA extraction. After measuring the concentration and confirming the integrity of the sample, 1 μg of total RNA was reverse transcribed using the GoScript Reverse Transcription System (catalog number: A5001, Promega Corporation, Madison, WI, USA).

2.8. Real-Time Quantitative PCR (RT-qPCR) Analyses of TaOBPs

The levels of mRNA expression of OBP family genes in T. absoluta were measured using the SYBR Green dye method. Real-time quantitative PCR (RT-qPCR) was performed with the qPCR Master Mix (catalog number: BM60304S, Baimeng Medical Co., Ltd., Fuzhou, Fujian, China) in the LightCycler480 system (Roche Diagnostics, Indianapolis, IN, USA). The 10 μL reaction system consisted of 5 μL 2 × qPCR Master Mix, 0.2 μL (10 μM) for each primer, and a 4.6 μL cDNA template. The amplification conditions were 95 °C for 30 s, 40 cycles of 95 °C for 5 s, 60 °C for 15 s, and 72 °C for 20 s. Each reaction was performed in triplicate with two technical replicates. Relative gene expression levels were calculated with the 2−ΔΔCT method [36] by normalizing with the reference of T. absoluta EF-1α (MZ054826) and GADPH (MZ054823). The primers were synthesized by Sangon Biotech Co., Ltd. (Shanghai, China), and all primer sequences are listed in Supplemental Table S2.

2.9. Data Analysis

Statistical analysis of the data was performed using IBM SPSS Statistics 27 (SPSS Inc., Chicago, IL, USA). In the Y-tube olfactory-selection experiment, the χ2 test was used to determine whether the theoretical distribution of H0 was assumed to be 50:50 between the two odor sources in the T. absoluta behavior-selection experiment. The χ2 and p values were calculated (*, p < 0.05; **, p < 0.01), and those who did not make a choice were not included in the selection rate. Different letters indicate significant differences (p < 0.05) following the use of Tukey’s honest significant difference multiple-range test. All data are presented as mean ± standard error (SE).

3. Results

3.1. Annotation and Identification of Genes from the Odorant-Binding Protein Family in T. absoluta

According to homologous gene analysis, intersection analysis was performed on the odorant-binding protein (OBP) family genes of T. absoluta identified by homologous comparison and domain-based recognition, and a total of 97 OBP genes were identified (Table 1). Molecular characteristics analysis showed that the average code sequence length was 571, the longest TabsOBP20 CDS length was 1158 bp, and the shortest TabsOBP63 CDS length was 261 bp (Table 1). The average number of exon fragments was 4, with TabsOBP72 containing the highest number of fragments at 9 exons (Table 1).

3.2. Phylogenetic Analysis and Chromosomal Location of OBP Genes in T. absoluta

To explore the evolutionary relationship of members of the OBP family in insects, parts of putative OBP genes from six representative species of two insect orders (Lepidoptera: Bm, Bombyx mori; Ha, Helicoverpa armigera; Ta, Tuta absoluta; Pr, Pieris rapae; Sf, Spodoptera frugiperda; Diptera: Dm, Drosophila melanogaster) were identified and phylogenetically analyzed (Figure 1). Phylogenetic trees of multiple species show that the OBP gene families present conserved clustering patterns in different Lepidoptera insects and even in Diptera D. melanogaster, since most of the OBP genes in these six insects were clustered (Figure 1). Furthermore, members of T. absoluta OBP family grouped in a large clade consisting of 56 members, suggesting that those OBPs may play a synergistic role in olfaction, and the remaining 41 members were scattered in other clades (Figure 1). For the OBP protein subfamilies, four subfamilies can also be distinguished in T. absoluta, i.e., 28 Classic OBPs, 11 Minus-C OBPs, 56 Plus-C OBPs, and 2 Dimer OBPs (Figure 1). The Plus-C subfamily has the largest number of members in T. absoluta and shows significant expansion compared to other insects.
The OBP genes identified in T. absoluta were located and analyzed on chromosomes (Figure 2). The results showed that the OBP genes of T. absoluta were widely distributed in 15 autosomes (chr1, chr2, chr3, chr4, chr9, chr10, chr12, chr14, chr15, chr16, chr17, chr18, chr20, chr21, and chr29) of the total 29 chromosomes, and the largest number of OBPs was on found on chromosome 16 (28 OBPs), followed by chromosome 15 (20 OBPs) and chromosome 17 (14 OBPs). The remaining OBP genes were randomly distributed on other chromosomes (Figure 2).

3.3. Developmental Stage-Specific Expression Profile of TaOBPs

Using transcriptomic data (BioProject: PRJNA291932), the expression levels of all genes in the OBP family were determined at the six developmental stages of T. absoluta (egg, first, second, third and fourth instar larvae, and adult). The results showed that the TaOBP genes showed very different abundances of expression at different stages of developmental (Figure 3). In the egg stage, OBP53, OBP65, and OBP41 showed high abundance (TPM value > 500). In the first instar larvae, OBP67, OBP54, OBP40, OBP57, OBP03, OBP65, OBP37, OBP26 and OBP80 showed high abundance. In the second instar larvae, OBP54, OBP67, OBP65, OBP56, OBP57, OBP40 and OBP03 showed high abundance. In the third instar larvae, OBP65, OBP54, OBP67, OBP57, OBP56, OBP66 and OBP40 showed high abundance. In the fourth instar larvae, OBP65, OBP54, OBP67, OBP57, and OBP66 showed high abundance. In the adults, OBP67, OBP60, OBP77, OBP54, OBP46, OBP58, OBP45, OBP12, OBP89, OBP55, and OBP62 showed a high abundance (Figure 3 and Supplemental Table S3).

3.4. Behavioral Responses of T. absoluta to Plectranthus tomentosa

The behavior response of the adult or larvae of T. absoluta to Plectranthus tomentosa was measured using a Y-tube olfactometer. The results of the behavior-selection experiment showed that in the tomato control group, P. tomentosa had a significant repellent effect on both adults (Figure 4A, 66.7% chose tomatoes vs. 20.0% chose P. tomentosa, p = 0.02) and larvae (Figure 4B, 60.0% vs. 23.3%, p = 0.04) of T. absoluta.
To further confirm the effect of P. tomentosa on the sexual behavior of T. absoluta and exclude the attraction effect of tomato volatiles, we conducted a selection experiment with pure air as the control group. The results indicated that the volatiles of P. tomentosa alone could also significantly repel adults of T. absoluta (Figure 4C, 60.0% vs. 26.7%, p < 0.01), and the degree of repelling was reduced in larvae (Figure 4D, 53.3% vs. 26.7%, p = 0.22).

3.5. Transcriptional Responses of TaOBPs to Tomatoes and P. tomentosa

OBP proteins are key proteins used by insects to recognize volatile external signals. To further study the olfactory response mechanism of T. absoluta to volatile compounds from the most suitable host plant tomato and the repellent plant P. tomentosa, after being exposed to volatiles of tomatoes or P. tomentosa for a while, transcriptional expression levels of OBP genes were determined throughout the genome of T. absoluta using real-time quantitative PCR (RT-qPCR).
The results showed that compared to the control exposed to pure air, the treatment of tomato volatiles induced the up-regulation (fold change >1.5) of 10 OBP genes in adult T. absoluta (Figure 5). More obviously, 20 OBP genes were up-regulated in adults after exposure to the volatiles of P. tomentosa, and the expression ratio was higher than that induced by volatiles of tomatoes (Figure 5). Among them, OBP09, OBP19, OBP22, OBP23, OBP24, OBP29, OBP37, OBP40, OBP41, OBP46, OBP58, OBP60, OBP65, OBP77, OBP85 and OBP92 showed significantly higher regulation than the pure air group or the tomato volatiles group (Figure 6, p < 0.05).
However, in larvae, only a relatively small number of OBP genes were affected by volatiles of tomatoes and P. tomentosa, and the amplitude of gene up-regulation was significantly smaller than that of the adults (Figure 7). That is, the expression levels of OBP3 and OBP24 were down-regulated after exposure to volatiles of P. tomentosa compared to the control exposed to pure air (Figure 7).

4. Discussion

As Tuta absoluta is a devastating global quarantine pest, its comprehensive control has become one of the hotspots of plant protection research in recent years [21]. As a promising ecological control measure, the ‘push and pull’ strategy based on functional plants has become a new method, playing an increasingly important role in the comprehensive control of many agricultural pests [37]. However, the direct application of functional plants to the control of T. absoluta is rarely reported. In this study, we identified Plectranthus tomentosa, which significantly repels adult and larval T. absoluta through a Y-tube olfactometer (Figure 4). P. tomentosa is a perennial shrub herb of the genus Spicularia in the Labiaceae family. It is known as ‘touch fragrance’ because it emits a comfortable aroma after touching, which has the effects of being refreshing, repelling mosquitoes, and reducing swelling [38]. Sun et al. have demonstrated that P. tomentosa has strong repellent effects against Tetranychus kanzawai [39]. Next, GC-MS combined with an olfactory tube experiment can be used to screen and identify specific compounds with repellent effects in P. tomentosa, and the potential of using P. tomentosa and its volatiles to control T. absoluta can be further verified through an envelope experiment and greenhouse experiment. In addition to the ‘push and pull’ strategy, agricultural control (such as the selection of resistant varieties) [40], cultivation management control (including reducing nitrogen fertilizer use) [41], biological control [42], physical control, and other applications have been applied to the prevention and control of T. absoluta [43]. Continued research on functional plants and the ‘push and pull’ strategy holds significant promise for improving the ecological control of T. absoluta.
In general, insects use olfactory-related proteins, such as odorant-binding proteins (OBPs), to make taxis between plants [6]. Here, we first identified 97 OBPs at the genome-wide level of T. absoluta (Table 1). We identified 97 OBP genes in T. absoluta, which is a significantly higher number compared to other reported insects (51 in Spodoptera frugiperda, 43 in Bombyx mori, 49 in Manduca sexta, 51 in Heliconius melpomene, 32 in Danaus plexippus) [44]. This significant expansion of OBP genes in T. absoluta suggests a potential role in its rapid invasion and extensive host adaptation capabilities. The multispecies phylogenetic tree reveals conserved clustering patterns in OBP gene families across Lepidoptera and even in Diptera, as the OBP genes of these five insects are mostly clustered together (Figure 1). In addition, a branch was clustered by 56 OBP members, suggesting that these OBPs may work synergistically in olfaction (Figure 1). Furthermore, the Plus-C subfamily of OBPs has the largest number of members (56 OBPs) in T. absoluta and shows significant expansion compared to other insects (Figure 1). The Plus-C subfamily of OBPs in Drosophila shows a striking level of divergence, with many of these sequences lacking the typical hydrophobic ligand-binding domain of OBPs [30]. The extremely significant expansion of the Plus-C subfamily may be involved in the rapid adaptation of T. absoluta to the host plant and the external odor environment, thus facilitating the rapid expansion and spread of T. absoluta.
The highest number of these OBP genes were highly expressed in the adult stage, followed by the larval stage, suggesting their crucial role in olfactory selection in both stages of life (Figure 3). Our study revealed that P. tomentosa exerts repellent effects on both adults and larvae of T. absoluta, as evidenced by tests using tomato and pure air as controls (Figure 4). To pinpoint specific OBPs responding to plant volatiles, we identified several potential OBPs in T. absoluta through RT-qPCR. In adults, sixteen OBPs were significantly up-regulated after exposure to P. tomentosa, with the TabsOBP39 gene showing a remarkable 588-fold increase (Figure 6). We hypothesized that these genes may be involved in the regulation of the repellent behavior of adult insects.
However, compared to adults, a small number of OBP genes in larvae were affected by volatiles of tomatoes and P. tomentosa, with a markedly lower amplitude of up-regulation (Figure 7). For a long time, studies on the olfactory system of insects have focused mainly on adult insects. However, Lepidoptera pests damage crops mainly at the larval stage, and so far, studies on the olfactory system of larvae have been very scarce [45]. In recent years, researchers have found that olfactory-related proteins are not only expressed in the larval stage of Lepidoptera insects but also play an important role in the selection of insect food [45,46]. For example, research has shown that Spodoptera littoralis larvae are significantly attracted to Z9, E11-14:Ac, a major component of adult sex pheromones—a discovery that could inform new pest-control strategies [46]. Only two OBP genes were significantly decreased in larvae, which may be consistent with the results of taxis behavior. The repellent effect of P. tomentosa on larvae was lower than that of adults, and there was no significant difference between the control group and the air control group (Figure 4D). T. absoluta was able to use those OBPs to identify external volatiles, leading to trend- or escape-selection behavior. In the future, we can further study how the key OBP recognizes the external volatiles, how to further regulate the signaling pathway of insects, and finally produce selection behavior.

5. Conclusions

In summary, we identified 97 putative members of the OBP family from the whole genome of T. absoluta. We then described the basic characteristics, phylogenetic analysis, and the developmental stage-specific expression profile of these gene family members. On the other hand, we identified the functional plant P. tomentosa, which significantly repels T. absoluta, and further pinpointed key OBP genes in T. absoluta that respond to the induction of volatiles of P. tomentosa. These findings provide preliminary information on the response mechanism of T. absoluta to tomato plants and repellent plants such as P. tomentosa. This research improves our understanding of the mechanisms of olfactory response in T. absoluta and offers potential avenues for environmentally sustainable pest-control strategies.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14010231/s1, Table S1: The sequence IDs for each OBP used for phylogenetic analysis; Table S2: Primers used in the qRT-PCR analysis; Table S3: Developmental stage-specific expression profile of TaOBPs based on TPM value.

Author Contributions

Conceptualization, Z.S. and F.G.; methodology, Z.S., R.M., D.L., C.P. and S.W.; software, Z.S.; formal analysis, Z.S. and Y.C.; investigation, Z.S., R.M., D.L., C.P. and S.W.; writing—original draft preparation, Z.S. and R.M.; writing—review and editing, Z.S. and F.G.; project administration, Z.S. and F.G.; funding acquisition, Z.S. and F.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key R&D Program of China (grant No. 2021YFD1400200), the National Natural Science Foundation of China (grant No. 32260668, 32360667), the Basic Research Project of Yunnan Province (grant No. 202301AT070485), and the Young Talents Special Project of Yunnan Xingdian Talent Support Plan (grant No. XDYC-QNRC-2022-0717).

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Phylogenetic relationship among OBP family members from six different insect species belonging to two orders. Bm, Bombyx mori; Dm, Drosophila melanogaster; Ha, Helicoverpa armigera; Ta, Tuta absoluta; Pr, Pieris rapae; Sf, Spodoptera frugiperda. Genes from the same insect are represented by the same colors. Branch colors represent the Classic (yellow), Plus-C (blue), Minus-C (green), and Dimer (purple) subfamilies.
Figure 1. Phylogenetic relationship among OBP family members from six different insect species belonging to two orders. Bm, Bombyx mori; Dm, Drosophila melanogaster; Ha, Helicoverpa armigera; Ta, Tuta absoluta; Pr, Pieris rapae; Sf, Spodoptera frugiperda. Genes from the same insect are represented by the same colors. Branch colors represent the Classic (yellow), Plus-C (blue), Minus-C (green), and Dimer (purple) subfamilies.
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Figure 2. Chromosome localization of OBP genes in T. absoluta genome. All the identified OBP genes were mapped onto the T.absoluta chromosomes using TBtools software (v0.665) and BITACORA software (v1.3) based on the genome annotation document. The length of each chromosome is indicated by the sale on the left.
Figure 2. Chromosome localization of OBP genes in T. absoluta genome. All the identified OBP genes were mapped onto the T.absoluta chromosomes using TBtools software (v0.665) and BITACORA software (v1.3) based on the genome annotation document. The length of each chromosome is indicated by the sale on the left.
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Figure 3. Heatmap of the expression level of OBP genes in different developmental stages of TaOBPs. L-1, L-2, L-3, and L-4 represent the first, second, third, and fourth instar larvae, respectively. The heat map is the expression after Z-transformation.
Figure 3. Heatmap of the expression level of OBP genes in different developmental stages of TaOBPs. L-1, L-2, L-3, and L-4 represent the first, second, third, and fourth instar larvae, respectively. The heat map is the expression after Z-transformation.
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Figure 4. Behavioral responses of T. absoluta to P. tomentosa. (A) Taxis behavior of adult in tomato control group; (B) Taxis behavior of larvae in tomato control group; (C) Taxis behavior of adult in pure air control group; (D) Taxis behavior of larvae in pure air control group. * p < 0.05; ** p < 0.01.
Figure 4. Behavioral responses of T. absoluta to P. tomentosa. (A) Taxis behavior of adult in tomato control group; (B) Taxis behavior of larvae in tomato control group; (C) Taxis behavior of adult in pure air control group; (D) Taxis behavior of larvae in pure air control group. * p < 0.05; ** p < 0.01.
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Figure 5. Transcriptional responses of TaOBPs in adult T. absoluta to tomatoes and P. tomentosa. The amount of gene expression in the heat map is the amount of tomato volatiles treated or P. tomentosa volatiles divided by the amount of expression treated with pure air. The logarithmic conversion of the relative expression value with base 10 was performed.
Figure 5. Transcriptional responses of TaOBPs in adult T. absoluta to tomatoes and P. tomentosa. The amount of gene expression in the heat map is the amount of tomato volatiles treated or P. tomentosa volatiles divided by the amount of expression treated with pure air. The logarithmic conversion of the relative expression value with base 10 was performed.
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Figure 6. Significantly up-regulated OBPs in adult T. absoluta after exposure to P. tomentosa volatiles. Different letters indicate significant differences (p < 0.05) by using Tukey’s honest significant difference multiple-range test. All data are presented as the mean ± standard error (SE).
Figure 6. Significantly up-regulated OBPs in adult T. absoluta after exposure to P. tomentosa volatiles. Different letters indicate significant differences (p < 0.05) by using Tukey’s honest significant difference multiple-range test. All data are presented as the mean ± standard error (SE).
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Figure 7. Transcriptional responses of TaOBPs in larvae of T. absoluta to tomatoes and P. tomentosa. The amount of gene expression in the heat map is the amount of tomato volatiles treated or P. tomentosa volatiles divided by the amount of expression treated with pure air. The relative expression value was homogenized.
Figure 7. Transcriptional responses of TaOBPs in larvae of T. absoluta to tomatoes and P. tomentosa. The amount of gene expression in the heat map is the amount of tomato volatiles treated or P. tomentosa volatiles divided by the amount of expression treated with pure air. The relative expression value was homogenized.
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Table 1. Identification and characteristics of the TaOBPs.
Table 1. Identification and characteristics of the TaOBPs.
Gene NameGenome IdentifierLocusCDS (bp)No of ExonsNo of TMSs
Chr.StartingEnding
TabsOBP01Tabs020023.1chr120,474,93120,476,48248340
TabsOBP02Tabs003327.1chr122,042,22422,045,78840540
TabsOBP03Tabs020567.1chr122,052,31222,054,42740240
TabsOBP04Tabs001544.1chr124,733,63124,739,56276850
TabsOBP05Tabs020984.1chr26,902,0036,930,20977450
TabsOBP06Tabs001496.1chr26,933,2006,936,25275060
TabsOBP07Tabs011682.1chr26,937,6976,941,22478950
TabsOBP08Tabs011532.1chr26,944,1086,949,33273550
TabsOBP09Tabs001649.1chr26,966,5956,982,92675050
TabsOBP10Tabs003077.1chr310,972,25110,992,14875350
TabsOBP11Tabs004058.1chr47,306,4167,306,92940220
TabsOBP12Tabs012945.1chr47,307,8577,309,32842620
TabsOBP13Tabs014664.1chr48,793,7868,795,95758850
TabsOBP14Tabs017562.1chr410,087,50210,091,19065140
TabsOBP15Tabs018202.1chr410,265,53510,282,89877160
TabsOBP16Tabs012221.1chr410,349,99310,352,26970241
TabsOBP17Tabs000652.1chr410,360,25110,364,95047760
TabsOBP18Tabs000441.1chr95,168,1875,198,93755560
TabsOBP19Tabs006266.1chr1015,096,64915,106,36479860
TabsOBP20Tabs007711.1chr1215,334,10915,335,900115850
TabsOBP21Tabs006148.1chr148,101,3918,108,16031230
TabsOBP22Tabs006809.1chr148,109,1878,117,80532730
TabsOBP23Tabs014933.1chr151,281,8311,284,78156150
TabsOBP24Tabs011481.1chr155,249,0115,251,11144450
TabsOBP25Tabs001448.1chr155,256,7325,261,75655250
TabsOBP26Tabs015427.1chr157,017,1697,026,00573851
TabsOBP27Tabs004992.1chr157,048,2607,058,57968150
TabsOBP28Tabs021922.1chr157,069,0407,080,09073251
TabsOBP29Tabs016278.1chr157,313,7487,321,38776850
TabsOBP30Tabs003939.1chr157,330,3687,333,80485250
TabsOBP31Tabs012068.1chr157,334,8217,338,35177150
TabsOBP32Tabs003951.1chr157,339,5017,342,29478050
TabsOBP33Tabs019705.1chr157,348,2697,352,52977750
TabsOBP34Tabs010627.1chr157,363,7767,375,21875350
TabsOBP35Tabs017381.1chr157,391,7707,405,77069050
TabsOBP36Tabs002475.1chr1513,600,55313,615,47572650
TabsOBP37Tabs010825.1chr1513,619,53513,625,21572950
TabsOBP38Tabs019998.1chr1513,634,51213,639,05471751
TabsOBP39Tabs014722.1chr1513,749,59813,752,42872650
TabsOBP40Tabs021282.1chr1519,271,02219,286,59672950
TabsOBP41Tabs017578.1chr1519,308,96419,326,11571160
TabsOBP42Tabs008070.1chr1519,340,22919,355,38994260
TabsOBP43Tabs021817.1chr162,311,5432,313,13150430
TabsOBP44Tabs020287.1chr162,314,2952,317,20562130
TabsOBP45Tabs021019.1chr162,318,8592,320,13348930
TabsOBP46Tabs016106.1chr162,322,2672,324,74949230
TabsOBP47Tabs020787.1chr162,327,7682,328,71448030
TabsOBP48Tabs019694.1chr162,329,1572,330,09049230
TabsOBP49Tabs008083.1chr162,685,3032,710,26050130
TabsOBP50Tabs015113.1chr162,998,2042,999,67637230
TabsOBP51Tabs018547.1chr165,453,2775,462,809146440
TabsOBP52Tabs002572.1chr1610,456,81410,458,60847730
TabsOBP53Tabs012705.1chr1610,473,03910,473,97837520
TabsOBP54Tabs011469.1chr1610,482,87210,483,85638120
TabsOBP55Tabs006705.1chr1610,487,71510,489,71738730
TabsOBP56Tabs011723.1chr1610,494,90510,496,37039330
TabsOBP57Tabs017738.1chr1610,504,93910,506,57746541
TabsOBP58Tabs004569.1chr1610,517,39310,525,94139020
TabsOBP59Tabs016148.1chr1610,526,59910,527,49736920
TabsOBP60Tabs002679.1chr1610,530,59010,531,70536020
TabsOBP61Tabs016850.1chr1610,533,21010,534,50038420
TabsOBP62Tabs006415.1chr1610,547,65710,549,20739640
TabsOBP63Tabs000522.1chr1610,554,29910,556,47126130
TabsOBP64Tabs011176.1chr1610,560,33010,561,03336620
TabsOBP65Tabs021726.1chr1610,562,75710,563,44936320
TabsOBP66Tabs016239.1chr1610,569,16510,570,12336320
TabsOBP67Tabs008941.1chr1610,571,90510,572,95237820
TabsOBP68Tabs020095.1chr1610,654,20410,658,84075360
TabsOBP69Tabs012728.1chr1611,298,06911,299,74437820
TabsOBP70Tabs003652.1chr1611,407,38011,408,98237820
TabsOBP71Tabs009636.1chr174,447,7374,453,66444150
TabsOBP72Tabs013199.1chr174,461,6014,476,79490690
TabsOBP73Tabs009535.1chr174,479,2654,484,32427340
TabsOBP74Tabs001054.1chr174,487,4174,489,14433040
TabsOBP75Tabs013797.1chr174,498,7254,501,47736640
TabsOBP76Tabs006184.1chr174,504,8234,507,64336640
TabsOBP77Tabs003612.1chr174,522,4284,526,31045350
TabsOBP78Tabs003709.1chr174,527,1884,531,69743560
TabsOBP79Tabs021931.1chr174,535,6394,539,65648050
TabsOBP80Tabs014350.1chr174,540,6374,544,98646251
TabsOBP81Tabs018171.1chr174,548,5674,556,91945050
TabsOBP82Tabs016909.1chr174,557,3284,563,31343550
TabsOBP83Tabs011627.1chr174,566,9654,576,76743250
TabsOBP84Tabs005154.1chr174,930,9784,938,96769951
TabsOBP85Tabs000196.1chr1810,446,35210,450,29642060
TabsOBP86Tabs016953.1chr202,752,0272,757,02545340
TabsOBP87Tabs019360.1chr203,696,6243,697,26564211
TabsOBP88Tabs003259.1chr205,312,4485,312,89745010
TabsOBP89Tabs015434.1chr205,314,6705,315,57334220
TabsOBP90Tabs007749.1chr205,328,2865,336,56858250
TabsOBP91Tabs014543.1chr208,925,4258,931,90466030
TabsOBP92Tabs014416.1chr211,643,7341,656,13974760
TabsOBP93Tabs006243.1chr2112,411,67812,418,07965750
TabsOBP94Tabs003544.1chr2112,420,71112,425,86158840
TabsOBP95Tabs015492.1chr2112,628,57112,631,36745940
TabsOBP96Tabs017882.1chr2114,305,70814,309,043108330
TabsOBP97Tabs017358.1chr297,179,4427,199,08763360
TMSs: Transmembrane Segments.
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Ma, R.; Li, D.; Peng, C.; Wang, S.; Chen, Y.; Gui, F.; Sun, Z. Genome-Wide Identification of the Genes of the Odorant-Binding Protein Family Reveal Their Role in the Olfactory Response of the Tomato Leaf Miner (Tuta absoluta) to a Repellent Plant. Agronomy 2024, 14, 231. https://doi.org/10.3390/agronomy14010231

AMA Style

Ma R, Li D, Peng C, Wang S, Chen Y, Gui F, Sun Z. Genome-Wide Identification of the Genes of the Odorant-Binding Protein Family Reveal Their Role in the Olfactory Response of the Tomato Leaf Miner (Tuta absoluta) to a Repellent Plant. Agronomy. 2024; 14(1):231. https://doi.org/10.3390/agronomy14010231

Chicago/Turabian Style

Ma, Ruixin, Donggui Li, Chen Peng, Shuangyan Wang, Yaping Chen, Furong Gui, and Zhongxiang Sun. 2024. "Genome-Wide Identification of the Genes of the Odorant-Binding Protein Family Reveal Their Role in the Olfactory Response of the Tomato Leaf Miner (Tuta absoluta) to a Repellent Plant" Agronomy 14, no. 1: 231. https://doi.org/10.3390/agronomy14010231

APA Style

Ma, R., Li, D., Peng, C., Wang, S., Chen, Y., Gui, F., & Sun, Z. (2024). Genome-Wide Identification of the Genes of the Odorant-Binding Protein Family Reveal Their Role in the Olfactory Response of the Tomato Leaf Miner (Tuta absoluta) to a Repellent Plant. Agronomy, 14(1), 231. https://doi.org/10.3390/agronomy14010231

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