- Research article
- Open Access
Characterization and expression profiling of glutathione S-transferases in the diamondback moth, Plutella xylostella (L.)
- Yanchun You†1, 2, 3,
- Miao Xie†1, 2, 3,
- Nana Ren1, 3,
- Xuemin Cheng1, 3,
- Jianyu Li1, 2, 3,
- Xiaoli Ma1, 3,
- Minming Zou1, 3,
- Liette Vasseur1, 4,
- Geoff M Gurr1, 3, 5 and
- Minsheng You1, 3Email author
© You et al.; licensee BioMed Central. 2015
- Received: 12 September 2014
- Accepted: 12 February 2015
- Published: 5 March 2015
Glutathione S-transferases (GSTs) are multifunctional detoxification enzymes that play important roles in insects. The completion of several insect genome projects has enabled the identification and characterization of GST genes over recent years. This study presents a genome-wide investigation of the diamondback moth (DBM), Plutella xylostella, a species in which the GSTs are of special importance because this pest is highly resistant to many insecticides.
A total of 22 putative cytosolic GSTs were identified from a published P. xylostella genome and grouped into 6 subclasses (with two unclassified). Delta, Epsilon and Omega GSTs were numerically superior with 5 genes for each of the subclasses. The resulting phylogenetic tree showed that the P. xylostella GSTs were all clustered into Lepidoptera-specific branches. Intron sites and phases as well as GSH binding sites were strongly conserved within each of the subclasses in the GSTs of P. xylostella. Transcriptome-, RNA-seq- and qRT-PCR-based analyses showed that the GST genes were developmental stage- and strain-specifically expressed. Most of the highly expressed genes in insecticide resistant strains were also predominantly expressed in the Malpighian tubules, midgut or epidermis.
To date, this is the most comprehensive study on genome-wide identification, characterization and expression profiling of the GST family in P. xylostella. The diversified features and expression patterns of the GSTs are inferred to be associated with the capacity of this species to develop resistance to a wide range of pesticides and biological toxins. Our findings provide a base for functional research on specific GST genes, a better understanding of the evolution of insecticide resistance, and strategies for more sustainable management of the pest.
- Transcriptome analysis
- Phylogenetic analysis
- Insect pest
The diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Plutellidae), is a world-wide destructive pest of wild and cultivated crucifers . The larvae feed on cruciferous plants and may cause significant reductions in yield and quality of economically important crops such as canola and cabbage. Historical reliance on insecticides has led to the rapid development of resistance in P. xylostella populations , making it difficult to control.
Several studies have examined the potential mechanisms underlying the development of insecticide resistance in P. xylostella [3-5]. One of the proposed mechanisms is metabolic resistance through the multifunctional glutathione S-transferases (GSTs, EC22.214.171.124). These enzymes can catalyze electrophilic compounds, making them water soluble and readily excreted . GSTs are known more generally by insects to detoxify various xenobiotics, including insecticides and plant allelochemicals . The recent work has focused on the potential role of GSTs in oxidative stress responses [6,8-11].
Insect GSTs are classified as cytosolic and microsomal. The number of microsomal GSTs is much lower than that of cytosolic GSTs, which have been grouped into six subclasses . Delta and Epsilon subclasses are insect specific, while the other four subclasses, Omega, Sigma, Theta, and Zeta, are found in various animal taxa [10,13,14].
GSTs are involved in the resistance of insects to organophosphate (OPs), chlorine, and pyrethroid insecticides [15,16]. Recombinant GST enzymes from P. xylostella and Drosophila melanogaster have been shown to play a role in the metabolism of organophosphate insecticides [17,18]. It has been suggested that, under elevated GST activity conditions, Anopheles subpictus can detoxify fenitrooxon activation products, leading to organophosphate resistance . The silkworm Zeta GST recombinant protein (rbmGSTz) has been found to initiate the dechlorination of permethrin and to be abundantly distributed in a permethrin-resistant strain . Similarly, an Omega GST is highly expressed in a fenitrothion-resistant strain of silkworm and its recombinant protein (rbmGSTo) shows high affinity with organophosphate insecticides, indicating that it may contribute to insecticide resistance and oxidative stress responses . The antennae-specific GST was found being involved with detoxification of xenobiotics and detection of sex pheromones in Manduca sexta .
The GSTs were found to be one of the major enzyme families in the P. xylostella genome and to be linked to detoxification of plant defense compounds and insecticides . A recent study on the identification and characterization of multiple glutathione S-transferase genes  based on the DBM transcriptome database [24,25] provides a primary base for further investigation of this important gene family. In the present study, the P. xylostella GSTs (PxGSTs) were identified and compared with the equivalent information from published insect genomes to better reveal their phylogenetic relationships and intron-exon organization. We profiled and analyzed expression patterns of the PxGSTs using the published transcriptome  and reverse transcription-quantitative polymerase chain reaction (qRT-PCR) in different life stages and tissues from insecticide susceptible or resistant strains. We then examined the major characteristics of GST subclasses and some particular GST genes in relation to their potential roles in P. xylostella insecticide resistance.
Identification of the PxGSTs
Description of 22 identified cytosolic GSTs in the P. xylostella genome
Gene size (bp)
Gene ID a
Comparison of GST gene numbers of various insect species*
Phylogenetic analysis of the PxGSTs
Delta and Epsilon GST subclasses are unique to insects and have been suggested to be implicated in insecticide resistance [10,36,37]. The earlier diverging insects Hymenoptera and Exopterygota do not have Epsilon subclass GSTs. Hymenoptera has a few genes present in the Delta subclass but none for Exopterogota suggesting that these orders may be from an evolutionary older lineage . Our tree suggests that Delta and Epsilon GSTs have diverged more recently from the other subclasses.
The range of amino acid identities in the insect-specific GSTs of P. xylostella are fairly variable, ranged from 38.39 ~ 84.75% in Delta and 23.05 ~ 60.91% in Epsilon (Additional file 4: Table S1). Except for PxGSTe1, the remaining Epsilon PxGSTs were clustered in a monophyletic clade of Lepidoptera (Figure 1), suggesting a lineage-specific expansion within the Epsilon subclass in lepidopteran order.
Characterization of the PxGST introns
In the PxGSTs, the splice sites of introns were classified into three phases: 0 with 45 introns, 1 with 17 introns, and 2 with 18 introns, according to their positions in the codons. The phase-1 introns were present only in the Omega, Zeta and Sigma subclasses. Most phase-2 introns were found in insect-specific subclasses (Delta and Epsilon) as well as in Zeta subclass. Most of the PxGST introns spliced in a given site tended to be from the same phase, suggesting that they might be relatively conserved (Figure 2).
Intron sites are similar across different PxGST subclasses. There are three highly conserved sites of introns within the Delta and Epsilon GST subclasses, except for the PxGSTd1 and PxGSTe1. These were between the 47th and 51st, the 114th and 118th and the 180th and 186th amino acids. Most of the PxGSTs tended to have a nearby conserved site of the introns located between the 111th and 125th amino acids belonging to phase 0. Both of the intron sites and phases were strongly conserved within Sigma and Zeta subclasses (Figure 2), implying that these genes might have similar functions. There appeared to be a correlation between the intron conservation and the phylogenetic cluster within a given PxGST subclass, indicating that gene structure evolution might be involved in the phylogenetic development of a specific subclass.
Despite the conserved nature of intron sites and phases, the lengths were highly variable in the PxGSTs ranging from 28 to 17,644 bp with a larger proportion ranging from 300 to 399 bp (Additional file 5: Figure S1) and an average of 918 bp. The shortest intron was PxGSTu1 (28 bp), while the longest were PxGSTo3 (17,644 bp) and PxGSTz2 (13,241 bp). A previous study has shown that long introns were considered to involve more functional elements than short introns and could effectively regulate gene expressions, possibly via the formation of pre-mRNA secondary structures . However, the function of the longest introns in PxGSTo3 and PxGSTz2 needs to be further investigated.
GSH and substrate binding sites in the PxGSTs
Stage-specific expression profiling
Strain- and tissue-specific expression profiling
To date, this is the most comprehensive study on genome-wide identification, characterization and expression profile of the GSTs in P. xylostella. Twenty-two GSTs were found in P. xylostella, which is similar in number to another lepidopteran species, B. mori. Variable features and different expression patterns of the genes reveal that the P. xylostella GSTs are evolutionary and functionally diversified, and may be involved in the evolution of adaptive capacity in response to environmental variation. Because GST enzymes are considered to be important in insecticide resistance, many of these newly identified genes are potential candidates for inhibiting the pathway of insecticide resistance and targeting lepidopteran-selective insecticides. Thus, further functional research on the PxGSTs is essential to identify the key genes and their roles in xenobiotic detoxification of insects, and understand the mechanisms underlying the insecticide resistance.
Experimental DBM strains
The experimental population of P. xylostella was derived from a susceptible strain (SS) that was collected from a vegetable field of Fuzhou (26.08°N, 119.28°E) in 2004 and used for genome sequencing . Since then this initial population was reared on potted radish seedlings (Raphanus sativus L.) at 25 ± 1°C, 65 ± 5% RH and L:D = 16:8 h in a separate greenhouse without exposure to insecticides over the past ten years. Two insecticide resistant strains (chlorpyrifos- and fipronil-resistant strains (CRS and FRS)) were selected from this susceptible strain, and detailed in DBM transcriptome .
Identification of P. xylostella GST genes
To identify putative GST genes from the DBM genome database [23,27], the GST protein sequences of D. melanogaster, C. quinquefasciatus, A. aegypti, A. gambiae, T. castaneum, A. mellifera, N. vitripennis, A. pisum, P. humanus, B. mori and other lepidopteran insects were downloaded from their genome databases [53-57] and/or GenBank (http://www.ncbi.nlm.nih.gov/) and Uniprot (http://www.uniprot.org/). These insect GST protein sequences were used as queries to perform local TBLASTN searches against the DBM genome database. The putative genomic sequences were retrieved, and then predicted using Fgenesh + (http://www.softberry.com/). The DBM GST protein sequences were confirmed using online BLASTP in NCBI.
The GSTs of A. aegypti (Aa), A. gambiae (Ag), D. melanogaster (Dm), A. mellifera (Am), N. vitripennis (Nv), Papilio polytes (Pp), Danaus plexippus (Dp), B. mori (Bm) and P. xylostella (Px) were used for the phylogenetic analysis. Putative amino acid sequences of the GSTs were aligned using Clustal X2.0 , and then gaps and missing data were manually trimmed. A phylogenetic tree was constructed with the neighbor-joining method  using MEGA 5.10 . Bootstrap analysis with 1,000 replicates was used to evaluate the significance of the nodes. Poisson correction amino acid model and pairwise deletion of gaps were selected for the tree reconstruction.
RNA extraction and cDNA synthesis
DBM eggs, 1st- to 4th-instar larvae, pupae and adults from susceptible and resistant strains were frozen in liquid nitrogen. Total RNA was extracted using the RNAiso Plus (Takara, Code: D9108A, Japan). The 4th-instar larvae were surface sterilized in 75% ethanol, then dipped in DNAase and RNAse free water and dissected. Tissues (head, midgut, Malpighian tubules, fatbody and epidermis) from resistant strains were briefly immersed in RNAlater™ RNA Stabilization Reagent (QIAGEN, Code: 76104, Germany) then stored at 4°C. Total RNA was extracted with the RNeasy Plus Micro Kit (QIAGEN, Code: 74034, Germany) and RNA concentration was determined using a spectrophotometer (Nanodrop 2000: Thermo, USA).
The cDNA template for PCR was synthesized with 1 μg of total RNA using PrimeScript®RT reagent Kit with gDNA Eraser (Perfect Real Time) (Takara, Code: DRR047A, Japan).
Validation of gene expression by qRT-PCR
The qRT-PCR primers used in the validation of gene expression were identified based on the encoding sequences of the DBM GSTs (Additional file 9: Table S5). DBM ribosomal protein L8 (RPL8) was used as reference gene for different strains and tissues, and DBM ribosomal protein S4 (RPS4) for different stages/instars. The assays were run in triplicate in CFX96 Touch™ Real-Time PCR Detection Systems (Bio-Rad, USA). PCR amplification was performed in a total reaction volume of 20 μL reaction mixture, containing 20 ng cDNA, 10 μL 2 × SYBR® Premix Ex Taq™ (Takara, DRR420A, Japan), 0.2 μM of each primer. PCR was conducted with standard thermal cycle conditions using the two-step qRT-PCR method: an initial denaturation at 95°C for 30s followed by 40 cycles of 3s at 95°C and 30s at 60°C. Specificity of the PCR products was assessed by melting curve analysis for all samples. For each treatment (tissues, strains and developmental stages), there were three biological replicates.
The 2−ΔCt method was used to analyze the qRT-PCR-based expression patterns. One-way ANOVA, using PASW Statistics 18, followed by a Duncan’s multiple range test was used to evaluate significant differences among patterns. The results were presented by mean ± standard deviation of the relative mRNA expressions.
Availability of supporting data
The nucleic acid sequences and protein sequences have been deposited in the published DBM genomic database (DBM-DB: http://iae.fafu.edu.cn/DBM/family/PxGSTs.php). Other supporting data are presented in Additional file 7: Tables S3 and Additional file 8: Table S4, and also deposited in the same database.
We are grateful to Liying Yu for her advice on analysis of gene family and phylogenetic analysis, and to Drs. Simon W. Baxter and Mark S. Goettel for their comments on our manuscript at early stage. We thank Yimin Zhuo, Jinyang Cai, Qiuye Qiu, Wenxiu Xie, Xianbin Huang and Xiaohui Huang for their technical assistance in rearing diamondback moth and preparing samples. The work was supported by National Natural Science Foundation of China (No. 31320103922 and No. 31230061) and National Key Project of Fundamental Scientific Research (“973” Programs, No. 2011CB100404) in China. LV is supported by the Minjiang Scholar Program in Fujian Province (PRC), and GMG by the National Thousand Talents Program in China.
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