Antennae-enriched expression of candidate odorant degrading enzyme genes in the turnip aphid, Lipaphis erysimi

Abstract

Aphids heavily rely on their olfactory system for foraging behavior. Odorant-degrading enzymes (ODEs) are essential in preserving the olfactory acuity of aphids by removing redundant odorants in the antennae. Certain enzymes within this group stand out as being enriched and/or biased expressed in the antennae, such as carboxylesterases (CXEs), cytochrome P450 (CYPs), glutathione S-transferases (GSTs), and UDP-glycosyltransferases (UGTs). Here, we performed a comparative transcriptome analysis of antennae and body tissue to isolate the antennal ODE genes of turnip aphid Lipaphis erysimi. A dataset of one CXE, seven CYPs, two GSTs, and five UGTs enriched in the antennae was identified and subjected to sequence analysis. Furthermore, qRT-PCR analyses showed that 13 ODE genes (LeCXE6, LeCYP4c1, LeCYP6a2, LeCYP6a13, LeCYP6a14.2, LeCYP6k1, LeCYP18a1, LeGST1, LeUGT1-7, LeUGT2B7, LeUGT2B13, LeUGT2C1.1, and LeUGT2C1.2) were specifically or significantly elevated in antennal tissues. Among these antennae-enriched ODEs, LeCYP4c1, LeCYP6a2, LeCYP6a13, LeCYP6a14.2, LeCYP18a1, LeUGT2B7, and LeUGT2B13 were found to exhibit significantly higher expression levels in alate aphids compared to apterous and nymph aphids, suggesting their putative role in detecting new host plant location. The results presented in this study highlight the identification and expression of ODE genes in L. erysimi, paving the path to investigate their functional role in odorant degradation during the olfactory processes.

1 Introduction

Insect antennae are intricate sensory organs essential in detecting a variety of lipophilic volatiles from the environment, helping insects secure food, find mates, lay eggs, and steer clear of potential predators (Leal, 2013; Cheema et al., 2021). During these biologic processes, the exogenous odor molecules are initially bound with insect odorant-binding proteins (OBPs) and chemosensory proteins (CSPs); they then move through the sensillum lymph and interact with olfactory receptors (ORs) situated on the membrane surface of olfactory sensory neurons. The ORs convert the chemical signals from the odor molecules into electrophysiological signals, which can be deciphered by the brain (Leal, 2013; Pelosi et al., 2018; Cheema et al., 2021; Zhou and Jander, 2022). Subsequently, antennal enzymes called odorant-degrading enzymes (ODEs) present in the vicinity of ORs become critical for the rapid degradation of odorant molecules, allowing for the insect’s olfactory system to recover and maintain its sensitivity (Younus et al., 2014; Blomquist et al., 2021; Chertemps and Maïbèche, 2021).

Insect ODEs are primarily recognized for their crucial role in metabolizing endogenous hormones and exogenous compounds like xenobiotics and allelochemicals. They include a few antennae-biased or antennae-enriched carboxylesterases (CXEs), cytochrome P450 (CYPs), glutathione S-transferases (GSTs), UDP-glycosyltransferases (UGTs), aldehyde oxidases (AOXs) (Younus et al., 2014; Blomquist et al., 2021). Among these ODEs, insect CXEs could degrade ester, amide, and carbamate bonds found in a range of plant volatiles, insect pheromones, hormones, and many pesticides (Leal, 2013; Ding et al., 2022). The first ODE identified was ApolSE, a CXE gene that was highly prevalent within the antennae of male silkmoths Antheraea polyphemus (Vogt and Riddiford, 1981); subsequent functional analyses determined that ApolSE functioned as a pheromone degrading enzyme, effectively breaking down the sex pheromone components [(6E, 11Z)-hexadecadienyl acetate, Z11-16:Ac] (Vogt et al., 1985; Ishida and Leal, 2005). Since then, several additional antennal CXEs have been functionally identified in various insects, such as the cotton leafworm Spodoptera littoralis (Durand et al., 2010), beet armyworm Spodoptera exigua (He et al., 2015), German cockroach Blattella germanica (Ma et al., 2023), and oriental fruit moth Grapholita molesta (Wei et al., 2021).

Insect CYPs are another well-studied group of antennal ODEs (Blomquist et al., 2021; Wu et al., 2022). While their primary function is to detoxify chemical insecticides within the body, studies in the pine beetle Dendroctonus ponderosae documented that several CYPs (e.g., CYP345E2, CYP6DE1, CYP6DJ1, CYP6BW1, and CYP6BW3) were capable of removing terpenoids from antennae and detoxifying host terpenoids to overcome plant defenses (Chiu et al., 2019a; Chiu et al., 2019b; Keeling et al., 2013). Additionally, certain enzymes within GST, UGT and AOX groups were reported to be linked to odorant and xenobiotic degradation (Rogers et al., 1999; Bozzolan et al., 2014; Li et al., 2018; Fraichard et al., 2020; Wang et al., 2021b; Liu et al., 2021). For example, a GST called GST-msolf1 restricted to pheromone sensilla could inactivate the sex pheromone blend in the tobacco hornworm, Manduca sexta (Rogers et al., 1999); UGT36E1, a UGT enzyme gene abundant in Drosophila antennal olfactory sensory neurons was involved in the clearance of pheromones (Fraichard et al., 2020), and the antennal aldehyde oxidase gene from the diamondback moth Plutella xylostella, PxylAOX3, oxidized both sex pheromone compounds and plant-derived aldehydes (Wang et al., 2021a).

The turnip aphid, Lipaphis erysimi Kaltenbach, poses a significant threat to the cultivation of Brassica vegetables and oilseed crops due to its direct feeding and/or transmission of harmful plant viruses. RNA interference (RNAi) has emerged as a promising strategy for controlling aphids, and antennal ODEs hold great promise as the optimal target genes for disrupting foraging behaviors (Yu et al., 2014; Yu et al., 2016; Wei et al., 2021; Wu et al., 2022; Ma et al., 2023). In this study, we aimed to identify antennae-enriched ODE genes of this aphid species by conducting as follows: 1) performing comparative analysis on the antennal and body transcriptomes of L. erysimi; 2) isolating and in silico analysis of candidate ODE genes; 3) identifying the expression profile of the ODE genes among different tissues and developmental stages.

2 Materials and methods

2.1 Insect rearing

The colony of L. erysimi utilized in this study was established in 2020, based on the field populations from Xinfeng in the Jiangxi province of China (Kuang et al., 2023). The population was continuously maintained on Chinese cabbage Shanghaiqing (Brassica rapa var. chinensis) without exposure to any insecticides under controlled conditions (27°C–28°C, 60%–65% RH, 14:10 L:D photoperiod).

2.2 Sample preparation, RNA extraction, and cDNA synthesis

Samples of L. erysimi were collected at five different stages, which include 1st instar nymph, 2nd instar nymph, 3rd instar nymph, 4th instar nymph, 1-day apterous and alate adults. The apterous aphids anesthetized on ice were dissected under a stereomicroscope to collect various tissues of L. erysimi, such as antenna, head, leg, and cuticle. Total RNA extraction was performed according to the manufacturer’s protocol of Trizol reagent (Sigma, St. Louis, MO, United States). The purity and concentration of RNAs were determined using a NanoDrop One^C spectrophotometer from Thermo Fisher Scientific (Waltham, MA, United States). The first-strand cDNA synthesis was synthesized with 500 ng of purified RNA, utilizing the highly effective EasyScript^® One-Step gDNA Removal and cDNA Synthesis SuperMix Kit (TransGen Biotech, Beijing, China). The resulting cDNA was properly stored at −20°C until ready to be used.

2.3 Comparative transcriptome analysis

To isolate the antennal-biased genes in L. erysimi, the high-throughput transcriptome data sets were retrieved from our former study (GenBank accession number PRJNA947784), which included conducting Illumina sequencing on the antennae and bodies (excluding antennae) of adult apterous aphids, transcriptome de novo assembly, as well as functional annotation of the unigenes (Kuang et al., 2023). The differential gene expression analysis was carried out using the antennal and body transcriptome data as described by Yu et al. (2023). Briefly, the transcript abundances were determined by RSEM (version 1.2.12); DESeq2 (version 1.4.5) was utilized to identify differentially expressed genes (DEGs) between samples, and a gene was considered differentially expressed if the corrected p-value was ≤ 0.05.

2.4 Identification of candidate ODE genes

The antennae-biased ODE genes with FPKM ≥10 were selected from the gene repertories obtained through comparative transcriptome analysis. Candidate ODEs were confirmed using the BLASTX algorithm, and their open reading frames (ORFs) were predicted using the ORF finder tool (http://www.ncbi.nlm.nih.gov/gorf/gorf.html). The amino acid components, theoretical isoelectric points (pIs), and molecular weights (MWs) of ODE genes were calculated using ExPASy (http://web.expasy.org/protparam/). The deduced protein sequences were submitted to the SignalP 5.0 server (https://services.healthtech.dtu.dk/services/SignalP-5.0/) for the prediction of the signal peptide sequences and their corresponding cleavage sites. Conserved domains were predicted with CDD-BLAST (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) and InterProScan (https://www.ebi.ac.uk/interpro/) servers.

2.5 Phylogenetic analysis

The dataset submitted for phylogenetic analysis comprised the candidate CXE, CYP, GST, and UGT genes of L. erysimi in this study, their homologs from Acyrthosiphon pisum (Ramsey et al., 2010), Aphis craccivora (Yang et al., 2021), Aphis gossypii (Pan et al., 2018), Myzus persicae (Pan et al., 2019), Nilaparvata lugens (Vontas et al., 2002; Zhou et al., 2013), Diaphorina citri (Yu and Killiny, 2018; Tian et al., 2019; Wu et al., 2020; Kuang et al., 2022), Anopheles gambiae (Ding et al., 2003), and Bombyx mori (Yu et al., 2008); in addition to some well-identified ODE genes, including the studied antennal CXEs (Ishida and Leal, 2005; 2008; Durand et al., 2010; Durand et al., 2011; He et al., 2015; Wei et al., 2021), CYPs (Keeling et al., 2013; Chiu et al., 2019a), GSTs (Rogers et al., 1999; Li et al., 2018; Liu et al., 2021; Xia et al., 2022), and UGTs (Wang et al., 1999; Bozzolan et al., 2014). The protein sequences were first aligned using CLUSTAL_X version 1.83. The joint unrooted phylogenetic tree was constructed with MEGA11 using the neighbor-joining method (Tamura et al., 2021). Branch support was evaluated through the bootstrap method which consisted of 1,000 replicates. The phylogenetic tree was visualized using iTOL web tool (https://itol.embl.de/).

2.6 Quantitative real-time PCR analysis

The quantitative real-time PCR (qRT-PCR) reactions were conducted in a 20 μL volume that comprised of 4 μL of diluted cDNA, 0.4 μM of each primer, and 10 μL of PerfectStart^® Green qPCR SuperMix (TransGen Biotech, Beijing, China). Reactions were performed on a Roche LightCycler 96^® system (Roche Diagnostics, Mannheim, Germany) with the following thermal program: initial denaturation for 10 min at 95°C, followed by a 40-cycle two-step amplification profile of 95°C for 5 s and 60°C for 30 s. Two reference genes, actin (GenBank accession number OQ626608) and GAPDH (GenBank accession number OQ626609), were employed to standardize the quantity of cDNA added to the PCR reactions. The relative expression of each ODE gene was analyzed using the 2^−ΔΔCt method (Livak and Schmittgen, 2001). Reactions were performed in triplicate, and the gene-specific primers are listed in Table 1.

2.7 Statistical analysis

The statistical differences of ODE gene expression levels among different developmental stages and tissues were analyzed using analysis of variance (ANOVA), followed by Tukey multiple comparison test. The statistical analysis was conducted using GRAPHPAD PRISM software (version 6.0; GraphPad Software Inc., La Jolla, CA, United States) and a p-value of ≤ 0.05 was set as the threshold for statistical significance.

3 Results

3.1 Differentially expressed genes analysis

Comparative analyses of the antennal and body transcriptomes in this study provide useful information to identify the antennae-abundant and/or antennae-biased genes. A total of 8,932 differentially expressed genes (DEGs) with a Q value ≤ 0.05 were identified, and 4,797 DEGs were significantly upregulated in the antennae (Figure 1). Among the antennae-abundant DEGs, one CXE, seven CYPs, two GSTs, and five UGTs were identified by blasting against the Nr database. The candidate ODEs were designated according to gene names of the top blast hits in NCBI. Detailed information on these ODE enzymes is shown in Table 2.

FIGURE 1

3.2 Identification of putative CXE genes

One putative CXE gene, LeCXE6, showed a high level of expression in the antennae, with FPKM values over 10 times higher than in the rest of the body. LeCXE6 encodes a 564 amino-acid protein, with a signal sequence cleavage site predicted between Gly-18 and Phe-19 at the N-terminus. The predicted protein has a theoretical molecular mass of 62.73 kDa and an isoelectric point of 5.57, as determined using ProtParam tool in Expasy server (Table 2). Conserved domain and sequence alignment analysis revealed that LeCXE6 contained the typical motif of carboxylesterase family, including a conserved pentapeptide (Gly-X-Ser-X-Gly) and an oxyanion hole (Gly-Gly-Ala; Supplementary Figure S1). Phylogenetic analysis showed that LeCXE6 fell into the beta-esterase clade and was closely clustered with the well-studied odorant-degrading enzymes, PjapPDE and ApolPDE (Figure 2).

FIGURE 2

3.3 Identification of putative CYP genes

Seven DEGs abundant in L. erysimi antennae were identified to be CYPs by blasting against the Nr database. All candidate LeCYPs were found to contain full-length ORFs without any predicted signal peptide sequences. Their antennal RPKM values ranged from 29.83 to 1,220.17, representing more than a ten-fold increase in comparison to the body group. Among them, LeCYP6a13 was the most abundant CYP gene in antennae with a value exceeding 1,200, followed by LeCYP18a1 and LeCYP6a2 (Table 2). Phylogenetic analysis showed that the selected CYPs were well categorized into four subclasses, namely, CYP2, CYP3, CYP4, and mitochondrial CYP. The CYP3 class comprised of five antennal LeCYPs, including LeCYP6a13, LeCYP6a2, LeCYP6k1, LeCYP6a14.1, and LeCYP6a14.2. LeCYP18a1 was classified as a member of the CYP2 clan, while LeCYP4c1 was categorized into the CYP4 clade (Figure 3).

FIGURE 3

3.4 Identification of putative GST genes

Two DEGs abundant in antennae were identified to be GSTs. Both LeGST1 and LeGST transcripts had full-length ORFs, encoding proteins that are 157 and 198 amino acids, respectively. It is noteworthy that LeGST1 showed an expression pattern that was particularly abundant in antennae, with an FPKM value of 93.81 that exceeded 18-fold higher than in the body (Table 2). Conserved domain analysis showed LeGST1 had a MAPEG (membrane-associated proteins in eicosanoid and glutathione metabolism) domain and was similar to the microsomal GST1, while LeGST had one GSH binding site (G-site) in the N-terminus and one hydrophobic substrate binding pocket (H-site) in the C-terminal region (Supplementary Figure S2). The phylogenetic analysis revealed that eight subclasses, namely, Microsomal-, Delta-, Epsilon-, Omega-, Sigma-, Theta-, Zeta-, and the unclassified-GST, were well clustered in their respective phylogenetic branches. LeGST1 was classified under the Microsomal-GST subclass, and LeGST was classified as a member of Sigma-GST (Figure 4).

FIGURE 4

3.5 Identification of putative UGT genes

A total of five antennal LeUGT genes were identified in the utilized transcript set. All LeUGT transcripts had full-length ORFs, encoding proteins ranging from 513 to 542 amino acids. Signal peptides were predicted in all candidate LeUGTs, with the exception of LeUGT2B13. FPKM analysis showed that LeUGT2B7 was the most antennae-abundant UGT with a value of 404.61, which was >20-fold higher than in the body (Table 1). Multiple alignments revealed the UGT motif signature sequence, (FVA)-(LIVMF)-(TS)-(HQ)-(SGAC)-G-X (2)-(STG)-X (2)-(DE)-X (6)-P-(LIVMFA)-(LIVMFA)-X (2)-P-(LMVFIQ)-X (2)-(DE)-Q, was situated at the C-terminus of LeUGTs (Supplementary Figure S3). Phylogenetic analysis showed that the candidate LeUGTs were grouped into three distinct subclades, with each subclade including several homologs from other aphid species. Specifically, LeUGT2B7, LeUGT2B13, and LeUGT2C1.2 were categorized into the UGT344 clade; LeUGT2C1.1 was clustered in the UGT343 subclade, and LeUGT1-7 was found to be a member of the UGT351 subclade (Figure 5).

FIGURE 5

3.6 Developmental and tissue expression analysis for candidate ODE genes

The developmental and tissue expression profiles of LeCXE, LeCYP, LeGST, and LeUGT genes were analyzed using qRT-PCR. Developmental expression data showed that the candidate ODE genes were consistently detected throughout the various developmental stages of L. erysimi, spanning from the first instar nymph to the adult stage. Notably, LeCYP4c1, LeCYP6a2, LeCYP6a13, LeCYP6a14.2, LeCYP18a1, LeUGT2B7, and LeUGT2B13 exhibited significantly higher expression levels in alate aphids compared to apterous and nymph aphids (Figure 6). Tissue expression analysis revealed that LeCYP6a14.1 and LeGST were highly expressed in both antenna and gut tissue, while the remaining 13 ODE genes displayed antennae-enriched expression profiles. In particular, the antennal expression levels of LeCYP6a13, LeCYP6k1, LeCYP6a14.2, LeGST1, LeUGT2B13, and LeUGT2C1.2 were >10-fold higher than in other tissues; LeCXE6, LeCYP4c1, LeCYP6a2, LeCYP18a1, LeUGT2B7, and LeUGT2C1.1 exhibited more than four times higher expression in antennae compared to non-olfactory tissues such as the head, leg, gut, and cuticle (Figure 7).

FIGURE 6

FIGURE 7

4 Discussion

Insects depend on their antennae to detect and process hydrophobic odorant molecules (Krieger and Breer, 1999; Leal, 2013). Discovering the ODEs within the antennae would provide crucial insights into the odorant recognition mechanism of L. erysimi, which may help us control this destructive agricultural pest more effectively. In this study, comparing the transcriptome data of the antennal and body tissues identified one CXE, seven CYPs, two GSTs, and five UGTs. The developmental and tissue expression profiles of these ODE genes were determined to reveal their implications in odorant degradation during the process of olfactory perception. To our knowledge, this is the first report documenting the identification of ODE genes in this aphid species.

The widespread occurrence of CXEs enables a tremendous decrease in the concentration of ester compounds in insects. This leads to improved sensitivity of the olfactory system and minimizes the possible toxic impact of these compounds. Several antennae abundant CXEs have been functionally studied and confirmed as ODEs, and employed for the purpose of eliminating odorants in the antennae (Ishida and Leal, 2005; 2008; Durand et al., 2010; Durand et al., 2011; He et al., 2015; Wei et al., 2021). For example, two CXEs, SlCXE7 and SlCXE10, are predominantly expressed in the antennal sensilla, and play a key role in the degradation of pheromones and plant volatile components in the cotton leafworm, S. littoralis (Durand et al., 2010; Durand et al., 2011). A similar study in G. molesta has uncovered four antenna-enriched CXEs play a crucial role in regulating the insect’s foraging and mating behaviors. Specifically, GmolCXE1 and GmolCXE5 are responsible for hydrolyzing the acetate sex pheromone (Z/E)-8-dodecenyl, while GmolCXE14 and GmolCXE21 are involved in metabolizing the ester host plant volatiles ethyl butanoate and ethyl hexanoate (Wei et al., 2021). In our study, combined transcriptome and qRT-PCR analysis revealed that LeCXE6 was highly enriched in the antennae. Further phylogenetic analysis indicated that LeCXE6 was grouped into the “beta esterases” clade along with two well-characterized pheromone-degrading enzymes, ApolPDE of A. polyphemus and PjapPDE of P. japonica (Ishida and Leal, 2005; 2008). These findings suggest that LeCXE6 may play a significant role in clearing redundant odorants during chemosensory processing.

CYPs represent an essential family of detoxification enzymes that widely occur in both vertebrates and invertebrates. Accumulating studies have shown that insect CYPs, especially those found abundantly in antennae, play a significant role as ODEs in the metabolism of host plant volatiles and sex pheromones (Chiu et al., 2019a; Chiu et al., 2019b; Chiu et al., 2019c; Wu et al., 2022). In this study, a total of seven antennae enriched LeCYP genes were identified. Our number of antennal CYP genes in L. erysimi is comparable to those found in other insect species, such as seven antennae-abundant CYPs were documented in D. citri (Kuang et al., 2022), as well as four CYPs (CYP4L4, CYP4S4, CYP9A13, and CYP4G20) of Mamestra brassicae and four CYPs (CYP6DE1, CYP6DJ1, CYP6BW1, and CYP6BW3) of D. ponderosae have been found to be highly expressed in the antennae (Maïbèche-Coisne et al., 2002; Maïbèche-Coisne et al., 2005; Chiu et al., 2019a; Chiu et al., 2019b; Chiu et al., 2019c). Insect P450 genes are commonly divided into four clades, which include CYP2, CYP3, CYP4, and the mitochondrial CYP. Herein, we found five LeCYPs (i.e., LeCYP6a13, LeCYP6a2, LeCYP6k1, LeCYP6a14.1, and LeCYP6a14.2) were grouped into the CYP3 clan. Recent research has demonstrated that many members of the CYP3 clan played an important role in facilitating herbivore adaptation to their host plants. For instance, two CYP3 genes (DponCYP345E2 and DponCYP6DE1) of D. ponderosae, were reported to catalyze the oxidation of monoterpene pine host volatiles such as α-pinene (Keeling et al., 2013; Chiu et al., 2019a), and the enhanced expression of CYP3 P450 genes has been observed in Dendroctonus armandi in response to host terpenoids such as pinene, 3-carene, and limonene (Dai et al., 2016).

Several GSTs, UGTs, and AOX enzymes expressed in insect antennae have been suggested to play crucial roles in the decomposition of odorous compounds. For instance, GST-msolf1 of M. sexta (Rogers et al., 1999), GmolGSTD1 of G. molesta (Li et al., 2018), PiGSTd1 of Plodia interpunctella (Liu et al., 2021), UGT36E1 of Drosophila melanogaster (Fraichard et al., 2020), and PxylAOX3 of P. xylostella (Wang et al., 2021a) have been implicated in this process. In our investigation, LeGST1 along with four UGTs (LeUGT2B7, LeUGT2B13, LeUGT2C1.1, and LeUGT2C1.2) displayed antennae-enriched expression profiles. However, no enrichment of any AOX genes was observed in the antennae of L. erysimi. Meanwhile, developmental expression analysis showed that LeCYP4c1, LeCYP6a2, LeCYP6a13, LeCYP6a14.2, LeCYP18a1, LeUGT2B7, and LeUGT2B13 exhibited significantly higher expression levels in alate aphids when compared to apterous and nymph aphids. Given that alate aphids often encountered complex surroundings consisting of a variety of odorants while navigating in search of new host plants, elevated levels of these ODEs may aid in maintaining their olfactory sensitivity.

In summary, this study has identified a dataset of CXE, CYP, GST, and UGT genes from L. erysimi, which might be involved in the processes of pheromone and/or plant volatile degradation. Previous studies have found that antennae-enriched ODEs offer great promise in the development of behavioral interference control strategies, in which ODE-silenced insects are expected to exhibit decreased or disordered foraging behaviors (Yu et al., 2016; Wei et al., 2021; Wu et al., 2022; Ma et al., 2023). Examples include RNAi of LmCYP6FD5, an antennae-specific P450 gene of Locusta migratoria, the EAG responses of locusts to the main volatiles of gramineous plants, including trans-2-Hexen-1-al, cis-3-Hexenyl acetate, and decanal, were significantly diminished (Wu et al., 2022). Therefore, future research on the physiological role of these ODE genes will pave the way toward understanding the olfactory mechanism of L. erysimi, and provide new targets for developing behavioral interference control strategies (e.g., RNAi) against this insect pest.

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