Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (14): 3004-3016.doi: 10.3864/j.issn.0578-1752.2021.14.007

• PLANT PROTECTION • Previous Articles     Next Articles

Resistance Monitoring to Thiamethoxam and Expression Analysis of Cytochrome P450 Genes in Leptinotarsa decemlineata from Xinjiang

SHI Xin1(),LI Sha1,WANG ZhiMin1,FU KaiYun2,FU WenJun3,JIANG WeiHua1()   

  1. 1College of Plant Protection, Nanjing Agricultural University, Nanjing 210095
    2Research Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences/Key Laboratory of Intergraded Management of Harmful Crop Vermin of China North-Western Oasis, Ministry of Agriculture and Rural Affairs, Urumqi 830091
    3Agricultural Technology Extension Master Station of Yili Prefecture, Yining 835000, Xinjiang
  • Received:2020-10-30 Accepted:2020-11-21 Online:2021-07-16 Published:2021-07-26
  • Contact: WeiHua JIANG E-mail:907094441@qq.com;jwh@njau.edu.cn

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Abstract:

【Objective】Colorado potato beetle (CPB), Leptinotarsa decemlineata, is a significant agricultural pest in potato worldwide. The objective of the study is to identify the main cytochrome P450 genes involved in metabolic regulation of neonicotinoid insecticide thiamethoxam in L. decemlineata.【Method】In this study, the resistance level to thiamethoxam was assayed using topical applications in 11 field populations of L. decemlineata from Qapqal (QPQL), Yining (YN), Tacheng (TC), Urumqi (URMQ), Jimusar (JMS) of Xinjiang in 2018 and 2019. The activities of three detoxifying enzymes including cytochrome P450 monooxygenase (P450), glutathioneS-transferase (GST) and esterase (EST), exposed to LD50of thiamethoxam for 72 h were analyzed by in vitro enzyme activity assay. The differentially expressed genes (DEGs) of L. decemlineata adults susceptible and resistant to thiamethoxam were detected by Illumina HiSeqTM 2500 sequencing platform. The expression verification of three P450 genes and the expression change of six P450 genes in different populations and the beetles exposed to LD50 of thiamethoxam for 72 h were performed by real-time quantitative PCR (qRT-PCR).【Result】Resistance monitoring results showed that the adults of YN1, URMQ1, TC and QPQL1 populations in 2018 and YN2 and JMS in 2019 developed low to moderate level resistance to thiamethoxam with resistance ratio (RR) ranging from 5.99 to 20.33 times. The P450 activities of adults from two sensitive populations URMQ2 and URMQ3 and two resistant populations YN2 and JMS after treatment with thiamethoxam LD50for 72 h were significantly increased to 1.76, 2.75, 1.91 and 1.66 times as high as the control, respectively. In addition, the GST (CDNB and DCNB as substrates) of URMQ3 population and the EST activities of URMQ2 and YN2 populations were obviously increased to 1.19, 2.10 and 1.35, 1.91 times of the control, respectively. Based on Illumina RNA sequencing, the raw reads (56 872 051 and 62 249 136), clean reads (55 903 706 and 61 082 076), clean bases (8.39 and 9.16 G) and error of basic group (0.03%) were obtained for the thiamethoxam-susceptible and -resistant samples of adult populations, respectively. Thirteen differentially expressed P450 genes were identified in the thiamethoxam-resistant sample, of which two genes were significantly up-regulated. The expression levels of three P450 genes, namely CYP4C1,CYP9e2and CYP305a1by RNA sequencing were validated by qRT-PCR analysis. Furthermore, CYP9Ya, CYP9Yc, CYP4C1, CYP305a1 and CYP9Z25 were up-regulated in the thiamethoxam-resistant adults, and the expression of CYP9Ya, CYP9Yc increased significantly in the 4th instar larvae and adults under thiamethoxam treatment. It was found by correlation analysis that there was a significant positive correlation between resistance level to thiamethoxam and CYP9Ya expression of adults. 【Conclusion】CYP9Ya may be involved in the production of thiamethoxam resistance in L. decemlineata, and the role of other genes cannot be ruled out.

Key words: Leptinotarsa decemlineata, thiamethoxam, resistance, cytochrome P450, gene expression

Table 1

Sampling information of L. decemlineatapopulations "

采集时间 Sampling time 种群 Population 采集地点 Sampling location
2018-06 察布查尔QPQL1 察布查尔县扎库齐牛录乡Zhakuqiniulu Town, Qapqal County
2018-06 伊宁YN1 伊宁县英塔木乡Yingtamu Town, Yining County
2018-06 塔城TC 塔城市阿西尔乡Axier Town, Tacheng City
2018-07 乌鲁木齐URMQ1 乌鲁木齐市安宁渠镇Anningqu Town, Urumqi City
2019-06 察布查尔QPQL2 察布查尔县扎库齐牛录乡Zhakuqiniulu Town, Qapqal County
2019-06 伊宁YN2 伊宁县英塔木乡Yingtamu Town, Yining County
2019-06 伊宁YN3 伊宁县胡地于孜乡Hudiyuzi Town, Yining County
2019-07 乌鲁木齐URMQ2 乌鲁木齐市萨尔达坂乡Saerdaban Town, Urumqi City
2019-07 乌鲁木齐URMQ3 乌鲁木齐市头屯河区Toutunhe District, Urumqi City
2019-07 乌鲁木齐URMQ4 乌鲁木齐市板房沟乡Banfanggou Town, Urumqi City
2019-07 吉木萨尔JMS 吉木萨尔县泉子街镇Quanzijie Town, Jimusar County

Table 2

The primers ofL. decemlineata for qRT-PCR "

基因 Gene 上游引物序列 Forward primer sequence (5′-3′) 下游引物序列 Reverse primer sequence (5′-3′)
CYP9Ya TGGACCAAAGAGTACCCGAAGGAA TCGACAATTCAGTCCGAGGTACGA
CYP9Yc ATTTGGAAGTGGACCACGCAATTG GCCAAATTCCTTCTCGTCCAGCAAG
CYP9Z25 ACTTGCACACCTTTGAGAGCATCC TTGTCAACTTTCTCATGCCCACCC
CYP4C1 AGCCTGACATTCCACTTC CTGCTCCTCACTAACATCT
CYP9e2 CATCATAGCACAAGCATTCT TTTCCTCCACATATTTCATCAG
CYP305a1 TTCCGAAGAATACGATGGT GCGAAGATGAAGAGTTACAA
RPL4 AAAGAAACGAGCATTGCCCTTCCG TTGTCGCTGACACTGTAGGGTTGA
Ef1α AAGGTTCCTTCAAGTATGCGTGGG GCACAATCAGCTTGCGATGTACCA

Table 3

Susceptibility to thiamethoxam of L. decemlineata 4th instar larvae and adults from Xinjiang "

虫态
Stage 		年份
Year 		种群
Population 		斜率Slope
（b±SE） 		致死中量（95%置信限）
LD50(95% FL) (ng/larva) 		抗性倍数
Resistant ratio (RR)
4龄幼虫
4th instar larva 		2018 QPQL-S 3.456±0.419 6.64 (5.12-8.61) 1.00
YN1 2.588±0.090 12.40 (10.01-15.43) 1.88
TC 3.236±0.211 14.08 (11.53-17.20) 2.14
URMQ1 3.438±0.255 16.04 (13.08-19.67) 2.42
QPQL1 1.255±0.086 27.94 (17.02-45.81) 4.23
2019 URMQ2 10.911±2.538 5.52 (5.21-5.84) 1.00
URMQ3 2.829±0.270 5.85 (4.69-7.29) 1.05
JMS 11.508±3.571 5.93 (5.60-6.28) 1.07
QPQL2 2.514±0.240 9.64 (7.49-12.42) 1.75
URMQ4 2.483±0.205 12.97 (9.62-17.49) 2.36
YN3 2.095±0.293 14.99 (11.38-19.76) 2.73
YN2 2.607±0.105 20.41 (14.76-28.22) 3.71
成虫
Adult 		2018 QPQL-S 1.648±0.098 9.42 (6.73-13.39) 1.00
YN1 2.665±0.075 56.33 (45.14-70.22) 5.99
URMQ1 5.934±0.321 82.76 (74.50-91.94) 8.81
TC 6.857±0.460 102.11 (94.00-110.92) 10.86
QPQL1 1.719±0.085 191.11 (139.32-262.28) 20.33
2019 URMQ2 11.203±1.607 24.69 (22.81-26.72) 1.00
URMQ3 3.707±0.551 37.65 (30.57-46.38) 1.53
URMQ4 3.023±0.406 58.31 (46.96-72.41) 2.36
QPQL2 1.636±0.091 85.25 (61.06-119.00) 3.45
YN3 2.802±0.102 111.19 (89.43-138.25) 4.50
YN2 1.809±0.212 291.97 (161.07-529.24) 11.82
JMS 1.384±0.138 347.01 (204.51-588.80) 14.05

Fig. 1

Changes of detoxification enzyme activities of L. decemlineata adults exposed to LD50 of thiamethoxam for 72 h Data in the figure are mean±SE. Different letters on the bars indicate significant difference atP<0. 05 level. The same as below "

Table 4

Sequencing results of susceptible and resistant adults of L. decemlineata from Xinjiang "

样品
Sample 		原始序列个数
Number of raw sequence 		过滤后的序列个数
Number of filtered sequence 		过滤后的序列长度
Clean bases
碱基错误率
Error of basic group (%) 		Q20 (%) Q30 (%) GC含量GC content (%)
UMRQ3 56872051 55903706 8.39 G 0.03 97.77 93.28 38.95
JMS 62249136 61082076 9.16 G 0.03 97.75 93.25 38.68

Table 5

DEGs between the resistant population and relatively sensitive population"

差异表达基因分类
DEG classification 		所有基因
Whole transcriptome 		上调基因
Up-regulated gene 		下调基因
Down-regulated gene 		显著上调基因Significantly up-regulated gene 显著下调基因Significantly down-regulated gene
细胞色素P450 Cytochrome P450 13 3 10 2 3
谷胱甘肽S-转移酶Glutathione S-transferase 1 0 1 0 0
酯酶Esterase 7 3 4 0 0
尿苷二磷酸-葡萄糖基转移酶UDP-glucuronosyltransferase 9 4 5 1 3
表皮蛋白Cuticular protein 6 3 3 0 0
ABC转运蛋白ABC transporter 12 4 8 3 0
烟碱型乙酰胆碱受体Nicotinic acetylcholine receptor 11 1 3 0 0

Table 6

Up-regulated genes in the resistant population"

基因名称Gene symbol 基因号 Gene ID log2FC P值 Pvalue
CYP4C1类基因 P450 4C1-like 111509985 3.75 9.82E-17
CYP9e2类基因 P450 9e2-like 111511395 2.15 0.001
可能为CYP305a1类基因 Probable P450 305a1 111504977 1.85 0.449
酯酶E4类基因Esterase E4-like 111513709 2.41 0.051
酯酶B1类基因%2C转录本变种X1
Esterase B1-like%2C transcript variant X1 		111502042 1.18 0.190
羧酸酯酶6类基因 Carboxylesterase-6-like 111514530 1.07 0.553
2-羟乙酰鞘氨1-β类半乳糖糖基转移酶基因
2-hydroxyacylsphingosine 1-beta-galactosyltransferase-like 		111516632 1.69 0.444
2-羟乙酰鞘氨1-β类半乳糖糖基转移酶基因
2-hydroxyacylsphingosine 1-beta-galactosyltransferase-like 		111512327 1.90 0.457
未鉴定的LOC111503457 Uncharacterized LOC111503457 111503457 1.52 0.543
尿苷二磷酸-葡萄糖基转移酶2B30类基因
UDP-glucuronosyltransferase 2B30-like 		111513316 2.52 0.023
蛹表皮蛋白36类基因 Pupal cuticle protein 36-like 111501889 3.28 0.073
幼虫表皮蛋白A2B类基因 Larval cuticle protein A2B-like 111503150 1.16 0.173
内表皮结构糖蛋白SgAbd-8类基因
Endocuticle structural glycoprotein SgAbd-8-like 		111517484 3.91 0.173
ABC转运蛋白跨膜区 ABC transporter transmembrane region novel.1120 7.53 6.85E-06
多药耐药相关蛋白1类基因
Multidrug resistance-associated protein 1-like 		111516459 7.98 7.63E-06
ABC转运蛋白 ABC transporter novel.1273 7.35 0.003
ATP-结合盒G亚家族类基因1%2C 转录本变种X1
ATP-binding cassette sub-family G member 1-like%2C transcript variant X1 		111510979 1.79 0.553
烟碱型乙酰胆碱受体α3亚基 α3 111512651 1.00 0.683

Fig. 2

The relative level of three up-regulated P450 genes by qRT-PCR validation"

Fig. 3

Relative expression of P450 genes in the field populations of L. decemlineata 4th instar larvae from Xinjiang in 2018 (A) and 2019 (B) "

Fig. 4

Relative expression of P450 genes in field populations of L. decemlineata adults from Xinjiang in 2018 (A) and 2019 (B) "

Fig. 5

Relative expression of P450 genes in 4th instar larvae and adults of relatively sensitive population of L. decemlineata exposed to thiamethoxam "

Table 7

Correlation analysis between expression of P450 genes and resistance level to thiamethoxam of L. decemlineata from Xinjiang "

采集时间
Sampling time 		基因
Gene 		R 值R value P 值P value
4龄幼虫4th instar larva 成虫Adult 4龄幼虫4th instar larva 成虫Adult
2018 CYP9Ya 0.549 0.548 0.338 0.339
CYP9Yc 0.790 0.487 0.112 0.406
CYP9Z25 0.049 0.309 0.938 0.613
2019 CYP9Ya -0.096 0.810* 0.838 0.027
CYP9Yc -0.101 0.646 0.829 0.117
CYP9Z25 0.270 0.189 0.558 0.685
CYP4C1 0.667 0.679 0.102 0.094
CYP9e2 -0.198 0.426 0.670 0.340
CYP305a1 0.144 0.179 0.758 0.702
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