响应槲皮素诱导的美国白蛾GST基因鉴定及表达分析

孟香; 潘忠玉; 陈敏

doi:10.12171/j.1000-1522.20220181

响应槲皮素诱导的美国白蛾GST基因鉴定及表达分析

北京林业大学林木有害生物防治北京市重点实验室，北京 100083

基金项目: 国家重点研发计划（2021YFD1400300）。

详细信息

作者简介:
孟香。主要研究方向：森林昆虫学。Email：Mengxiang@bjfu.edu.cn　地址：100083 北京市海淀区清华东路35号北京林业大学林学院

责任作者:
陈敏，教授。主要研究方向：森林昆虫学。Email： minch@bjfu.edu.cn　地址：同上。

中图分类号: S763.42
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出版历程
- 收稿日期: 2022-05-08
- 修回日期: 2022-05-14
- 录用日期: 2023-09-27
- 网络出版日期: 2023-10-10
- 刊出日期: 2023-11-29

Identification and expression analysis of GST genes in response to quercetin induction in Hyphantria cunea

Key Laboratory of Beijing for the Control of Forest Pests, Beijing Forestry University, Beijing 100083, China

摘要

摘要:
目的
谷胱甘肽S-转移酶（GSTs）是昆虫体内一种重要的解毒酶，在植食性昆虫对植物次生物质的解毒适应中发挥重要作用。本研究筛选和鉴定了美国白蛾中肠响应槲皮素诱导的GST基因，分析了槲皮素对GST基因的诱导表达模式，为阐明美国白蛾GST基因在解毒代谢槲皮素中的功能奠定基础。
方法
基于槲皮素诱导的美国白蛾中肠转录组，筛选和鉴定响应槲皮素诱导的GST基因；通过构建系统发育树分析GST基因的家族类别；采用实时荧光定量PCR技术研究槲皮素对GST基因诱导的剂量效应和时间效应。
结果
鉴定了美国白蛾响应槲皮素诱导的6个GST基因；系统发育分析显示HcGST-E1、HcGST-E2、HcGST-E3属于GST Epsilon家族，HcGST-S1、HcGST-S2属于GST Sigma家族，HcGST-O1属于GST Omega家族。不同质量分数槲皮素对GST基因的诱导作用不同，本实验质量分数（0.5%、1.0%、2.0%、4.0%）的槲皮素均能诱导HcGST-E1表达水平显著上调，0.5%、1.0%和 2.0%的槲皮素诱导HcGST-E3表达水平显著升高；0.5%的槲皮素诱导HcGST-O1的表达水平显著增加。本实验质量分数的槲皮素均诱导HcGST-S1显著下调表达；0.5%和1.0%的槲皮素诱导HcGST-S2的表达水平显著下调。3个上调GST基因均在24 h或36 h内显著上调表达响应槲皮素的诱导。
结论
槲皮素能显著诱导美国白蛾中肠6个GST基因的表达水平，但对不同基因诱导的表达模式不同。HcGST-E1、HcGST-E3和HcGST-O1显著上调表达响应不同质量分数槲皮素的诱导，推测这3个基因是参与美国白蛾解毒代谢槲皮素的关键基因。
- 美国白蛾 /
- GST基因 /
- 槲皮素 /
- 诱导 /
- 转录表达
Abstract:
Objective
Glutathione S-transferases (GSTs) are important detoxification enzymes in insects, playing an important role in the physiologhical adaptation of phytophagous insects to plant secondary substances. In this study, we screened and identified GST genes and analyzed their expression patterns induced by quercetin in Hyphantria cunea midgut, laying the foundation for elucidating the function of GST genes in detoxification and metabolism of quercetin in H. cunea.
Method
Based on the quercetin-induced midgut transcriptome of H. cunea, the GST genes in response to quercetin induction were screened and identified. The family categories of GST genes were analyzed by constructing phylogenetic tree. The dose effect and time effect of quercetin on GST gene induction were studied by real-time fluorescence quantitative PCR.
Result
Six GST genes were identified from the gut in response to quercetin induction. Phylogenetic analysis showed that HcGST-E1, HcGST-E2 and HcGST-E3 belong to the GST Epsilon family, HcGST-S1 and HcGST-S2 belong to the GST Sigma family, and HcGST-O1 belongs to the GST Omega family. Various mass fraction of quercetin had different induction effects on GST genes. The tested mass fraction of quercetin (0.5%, 1.0%, 2.0% and 4.0%) significantly up-regulated HcGST-E1 expression, below 2.0% of quercetin significantly increased HcGST-E3 expression, and 0.5% quercetin significantly enhanced HcGST-O1 expression. By contrast, the tested mass fraction of quercetin significantly induced the down-regulation of the expression level of HcGST-S1 and 0.5% and 1.0% of quercetin significantly down-regulated the expression level of HcGST-S2. Three up-regulated GST genes were significantly up-regulated within 24 h or 36 h by quercetin.
Conclusion
Quercetin could significantly induce the expression levels of six GST genes in the midgut of H. cunea, but the expression patterns are various for each induced gene. HcGST-E1, HcGST-E3 and HcGST-O1 are significantly up-regulated in response to the quercetin induction. It is, therefore, speculated that these 3 genes are the key genes involved in the detoxification of quercetin in H. cunea.
- Hyphantria cunea /
- GST gene /
- quercetin /
- induction /
- transcriptional expression

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图 1 美国白蛾与其他鳞翅目昆虫的GST基因系统发育树

Bm.家蚕；Ha.棉铃虫；Sf.草地贪夜蛾；Sl.斜纹夜蛾；Tn.粉纹夜蛾；Px.柑橘凤蝶；Se.甜菜夜蛾；Hc.美国白蛾。不同颜色代表不同GST基因家族；红色字体基因代表本研究鉴定的6条GST基因。节点处的数值为分支支持度。Bm, Bombyx mori; Ha, Helicoverpa armigera; Sf, Spodoptera frugiperda; Sl, Spodoptera litura; Tn, Trichoplusia ni; Px, Papilio xuthus; Se, Spodoptera exigua; Hc, Hyphantria cunea. Different colors represent different GST gene families. The red font genes represent the 6 GST genes identified in this study. The values at the node indicate branch support.

Figure 1. Phylogenetic tree of GST genes of Hyphantria cunea and other lepidoptera insects

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图 2 不同质量分数槲皮素诱导24 h后美国白蛾5个GST基因的相对表达水平

条形柱上的*代表不同质量分数槲皮素诱导后，GST基因相对表达量与对照组差异显著，*代表P < 0.05，**代表P < 0.01，***代表P < 0.001，****代表P < 0.000 1。下同。The * on the bar represents that the relative expression level of GST gene is significantly different from the control after induction with different mass fractions of quercetin. * represents P < 0.05, ** represents P < 0.01, *** represents P < 0.001, **** represents P <0.000 1. The same below.

Figure 2. Relative expression level of five GST genes of Hyphantria cunea after 24 h induction with different mass fractions of quercetin

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图 3 0.5%槲皮素诱导下美国白蛾中肠GST基因在转录组和RT-qPCR中的表达水平

虚线为对照组（CK）的相对表达水平。ns代表同一基因的两种表达量变化倍数差异不显著。The dotted line is the relative expression level of control group. ns represents there is no significant difference between the two expression multiples of the same gene.

Figure 3. Relative expression level in RNA-seq and RT-qPCR of GST genes in midgut of Hyphantria cunea induced by 0.5% quercetin

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图 4 0.5%槲皮素诱导24 h、36 h、48 h、72 h和96 h后美国白蛾3个GST基因的相对表达水平

Figure 4. Relative expression level of three GST genes of Hyphantria cunea after 24, 36, 48, 72, and 96 h induction with 0.5% quercetin

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表 1 RT-qPCR引物序列信息

Table 1 RT-qPCR primer sequence information

基因 Gene	引物序列（5′—3′） Primer sequence (5′−3′)	扩增效率 Amplification efficiency/%	相关系数 Correlation coefficient
HcGST-E1	F-CGAGAGCAAGACACACCTGA R-ATAGAGACGCGTGCTTTGGT	93.2	0.997
HcGST-E3	F-ACCCGCTACATACTATCCCGA R-AACGTTGATCCACTGTCGCT	110.0	0.996
HcGST-S1	F-ATGTGAGGGCTTTAGGTGAGG R-TCAGCCCATTGTTCAGGAGTT	96.2	0.997
HcGST-S2	F-CGGTAGCATGGTCGACTACTT R-ACGGACTTTCTTGAGGGCAG	93.3	0.994
HcGST-O1	F-GGTGATCCACTCCCGTCATAC R-GGCATTAAGCGCCAAGACAG	103.4	0.996
GAPDH	F-GACTGGCATGGCTTTCAGAG R-CATCGTAGCTAGCGGGTTTG	96.5	0.999
EF1α	F-TTATCGTCGCTGCTGGTACT R-GAGTGTGAAAGCGAGCAGAG	103.5	0.999

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表 2 响应槲皮素诱导的美国白蛾GST基因的BLASTX结果

Table 2 BLASTX results of quercetin-induced GST genes in Hyphantria cunea

基因名称 Gene name	登录号 Accession No.	转录水平 Transcription level	编码蛋白长度 Encoded protein length/aa	同源性比较最佳匹配结果 Homology comparison of best match result
基因名称 Gene name	登录号 Accession No.	转录水平 Transcription level	编码蛋白长度 Encoded protein length/aa	蛋白质名称 Protein name	物种 Species	E值 E value	一致性 Identity/%	登录号 Accession No.
HcGST-E1	OM323338	表达上调2.02倍 Up-regulated expression 2.02 times	228	Glutathione-S- transferase epsilon	海灰翅夜蛾 Spodoptera littoralis	4.00 × e⁻¹²³	73.68	AYM01156.1
HcGST-E2	OM323336	表达下调0.34倍 Down-regulated expression 0.34 times	216	Glutathione S- transferase epsilon 13	甜菜夜蛾 Spodoptera exigua	1.00 × e⁻¹¹³	72.64	ASN63944.1
HcGST-E3	OM323337	表达上调10.26倍 Up-regulated expression 10.26 times	216	Glutathione S- transferase 1	烟草天蛾 Manduca sexta	2.00 × e⁻¹⁰³	65.28	XP_030020682.1
HcGST-S1	OM287126	表达下调0.29倍 Down-regulated expression 0.29 times	203	Glutathione S- transferase 2-like	棉铃虫 Helicoverpa armigera	2.00 × e⁻⁸¹	61.76	XP_021186026.1
HcGST-S2	OM323334	表达下调0.19倍 Down-regulated expression 0.19 times	204	Glutathione S- transferase sigma 4	甜菜夜蛾 Spodoptera exigua	2.00 × e⁻⁹³	65.84	ASN63950.1
HcGST-O1	OM323335	表达上调2.17倍 Up-regulated expression 2.17 times	284	Glutathione S- transferase 8	小线角木蠹蛾 Streltzoviella insularis	3.00 × e⁻¹¹⁶	60.34	QLI62204.1

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