新疆马铃薯甲虫对噻虫嗪的抗性监测及其细胞色素P450基因表达分析

doi:10.3864/j.issn.0578-1752.2021.14.007

中国农业科学 ›› 2021, Vol. 54 ›› Issue (14): 3004-3016.doi: 10.3864/j.issn.0578-1752.2021.14.007

新疆马铃薯甲虫对噻虫嗪的抗性监测及其细胞色素P450基因表达分析

石鑫¹(),李莎¹,王志敏¹,付开赟²,付文君³,姜卫华¹()

¹南京农业大学植物保护学院,南京 210095
²新疆农业科学院植物保护研究所/农业农村部西北荒漠绿洲作物有害生物综合治理重点实验室,乌鲁木齐 830091
³新疆伊犁州农业技术推广总站,新疆伊宁 835000

收稿日期:2020-10-30 接受日期:2020-11-21 出版日期:2021-07-16 发布日期:2021-07-26
通讯作者: 姜卫华
作者简介:石鑫,E-mail： 907094441@qq.com。
基金资助:
国家重点研发计划(2018YFD0200802)

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()

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

摘要/Abstract

摘要：

【目的】以世界性害虫马铃薯甲虫（Leptinotarsa decemlineata）为研究对象,筛选其参与噻虫嗪解毒的细胞色素P450主效基因。【方法】于2018、2019年利用点滴法监测新疆察布查尔县、伊宁县、塔城市、乌鲁木齐市和吉木萨尔县11个马铃薯甲虫田间种群对噻虫嗪的抗性水平,并测定分析噻虫嗪LD₅₀处理72 h后成虫中3种主要解毒酶细胞色素P450酶（P450）、谷胱甘肽S-转移酶（GST）和酯酶（EST）的活性变化。利用Illumina HiSeq^TM 2500 高通量测序技术进行转录组测序,获得抗性和敏感种群之间的差异表达基因（DEG）,运用实时荧光定量PCR（qRT-PCR）技术验证3个P450基因并分析6个P450基因（CYP4C1、CYP9e2、CYP305a1、CYP9Z25、CYP9Ya和CYP9Yc）在不同种群及噻虫嗪处理后的表达情况。【结果】抗性监测发现,2018年的YN1、URMQ1、TC和QPQL1以及2019年的YN2和JMS种群成虫对噻虫嗪抗性倍数（RR）分别达到5.99、8.81、10.86和20.33倍和11.82、14.05倍,为低至中水平抗性。解毒酶活性测定结果表明,2个敏感种群URMQ2、URMQ3以及2个抗性种群YN2、JMS成虫分别经噻虫嗪LD₅₀处理72 h后其P450活性均显著增加,分别为对照的1.76、2.75、1.91和1.66倍。另外,URMQ3种群的GST（CDNB和DCNB为底物）及URMQ2、YN2种群的EST活性显著升高,分别为对照的1.19、2.10倍和1.35、1.91倍。转录组分析表明,通过合并组装分别获得噻虫嗪敏感和抗性种群样品56 872 051和62 249 136个原始序列数据以及55 903 706和61 082 076个过滤后的序列数据,过滤后的序列长度分别为8.39和9.16 G,碱基错误率均为0.03%。抗性种群中差异表达的P450基因13个,其中2个基因显著上调。3个上调的P450基因CYP4C1、CYP9e2和CYP305a1的qRT-PCR检测结果与转录组测序结果基本一致,qRT-PCR分析还发现CYP9Ya、CYP9Yc、CYP4C1、CYP305a1和CYP9Z25在抗性种群成虫中表达量显著增加,噻虫嗪LD₅₀处理均可引起URMQ2种群4龄幼虫和成虫CYP9Ya、CYP9Yc表达量显著上调。相关性分析发现成虫对噻虫嗪的抗性水平与CYP9Ya表达量呈显著正相关。【结论】CYP9Ya可能在马铃薯甲虫中对噻虫嗪具有重要的解毒作用,其他基因的作用也不能排除。

关键词: 马铃薯甲虫, 噻虫嗪, 抗药性, 细胞色素P450, 基因表达

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 HiSeq^TM 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

石鑫,李莎,王志敏,付开赟,付文君,姜卫华. 新疆马铃薯甲虫对噻虫嗪的抗性监测及其细胞色素P450基因表达分析[J]. 中国农业科学, 2021, 54(14): 3004-3016.

SHI Xin,LI Sha,WANG ZhiMin,FU KaiYun,FU WenJun,JIANG WeiHua. Resistance Monitoring to Thiamethoxam and Expression Analysis of Cytochrome P450 Genes in Leptinotarsa decemlineata from Xinjiang[J]. Scientia Agricultura Sinica, 2021, 54(14): 3004-3016.

0
/ / 推荐

导出引用管理器 EndNote|Reference Manager|ProCite|BibTeX|RefWorks

链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2021.14.007

https://www.chinaagrisci.com/CN/Y2021/V54/I14/3004

图/表 12

表1

表2

表3

图1

表4

表5

表6

图2

图3

图4

图5

表7

参考文献 26

[1]	ALYOKHIN A. Colorado potato beetle management on potatoes: Current challenges and future prospects//Fruit, Vegetable and Cereal Science and Biotechnology, 2009, 3(1):10-19.
[2]	ALYOKHIN A, BAKER M, MOTA-SANCHEZ D, DIVELY G, GRAFIUS E. Colorado potato beetle resistance to insecticides. American Journal of Potato Research, 2008, 85:395-413. doi: 10.1007/s12230-008-9052-0
[3]	郭文超, 吐尔逊, 许建军, 刘建, 何江, 李晶, 马德成, 王俊. 马铃薯甲虫识别及其在新疆的分布、传播和危害. 新疆农业科学, 2010, 47(5):906-909.
	GUO W C, TU E R, XU J J, LIU J, HE J, LI J, MA D C, WANG J. Research on the identification of Colorado potato beetle and its distribution, dispersal and damage in Xinjiang. Xinjiang Agricultural Sciences, 2010, 47(5):906-909. (in Chinese)
[4]	须志平. 新烟碱类杀虫剂在作物保护方面的应用. 世界农药, 2009, 31(1):18-21.
	XU Z P. Application of neonicotinoids insecticides in crop protection. World Pesticides, 2009, 31(1):18-21. (in Chinese)
[5]	王彦华, 王鸣华. 害虫对噻虫嗪抗药性及其治理. 世界农药, 2008, 30(4):42-45.
	WANG Y H, WANG M H. Pest resistance to thiamethoxam and its management. World Pesticides, 2008, 30(4):42-45. (in Chinese)
[6]	ZHAO J Z, BISHOP B A, GRAFIUS E J. Inheritance and synergism of resistance to imidacloprid in the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 2000, 93(5):1508-1514. doi: 10.1603/0022-0493-93.5.1508
[7]	MOTA-SANCHEZ D, HOLLINGWORTH R M, GRAFIUS E J, MOYER D D. Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Management Science, 2006, 62(1):30-37. doi: 10.1002/(ISSN)1526-4998
[8]	王志田, 姜卫华, 李国清. 新疆北疆马铃薯甲虫成虫抗药性水平监测. 农药, 2010, 49(3):206-208.
	WANG Z T, JIANG W H, LI G Q. Insecticide resistance in adult of the Colorado potato beetle among north Xinjiang Uygur autonomous region. Agrochemicals, 2010, 49(3):206-208. (in Chinese)
[9]	刘萍, 姜卫华, 卢伟平, 李国清. 新疆北疆马铃薯甲虫成虫对新烟碱类杀虫剂的敏感性变化. 农药学学报, 2011, 13(3):271-275.
	LIU P, JIANG W H, LU W P, LI G Q. Susceptibility of Colorado potato beetle Leptinotarsa decemlineata adults from northern Xinjiang Uygur autonomous region to 4 neonicotinoids . Chinese Journal of Pesticide Science, 2011, 13(3):271-275. (in Chinese)
[10]	KAPLANOGLU E, CHAPMAN P, SCOTT I M, DONLY C. Overexpression of a cytochrome P450 and UDP-glycosyltransferase is associated with imidacloprid resistance in the Colorado potato beetle, Leptinotarsa decemlineata. Scientific Reports, 2017, 7:1762. doi: 10.1038/s41598-017-01961-4
[11]	CLEMENTS J, SCHOVILLE S, PETERSON N, LAN Q, GROVES R L. Characterizing molecular mechanisms of imidacloprid resistance in select populations of Leptinotarsa decemlineata in the central sands region of Wisconsin. PLoS ONE, 2016, 11(1):e0147844. doi: 10.1371/journal.pone.0147844
[12]	CLEMENTS J, SCHOVILLE S, PETERSON N, HUSETH A S, LAN Q, GROVES R L. RNA interference of three up-regulated transcripts associated with insecticide resistance in an imidacloprid resistant population of Leptinotarsa decemlineata. Pesticide Biochemistry and Physiology, 2017, 135:35-40. doi: 10.1016/j.pestbp.2016.07.001
[13]	CLEMENTS J, OLSON J M, SANCHEZ-SEDILLO B, BRADFORD B, GROVES R L. Changes in emergence phenology, fatty acid composition, and xenobiotic-metabolizing enzyme expression is associated with increased insecticide resistance in the Colorado potato beetle. Archives of Insect Biochemistry and Physiology, 2020, 103(3):e21630.
[14]	卢伟平, 刘萍, 姜卫华, 李国清. 4种新烟碱类杀虫剂对马铃薯甲虫的触杀毒力比较. 农药, 2011, 50(2):137-140.
	LU W P, LIU P, JIANG W H, LI G Q. Comparison of contact toxicities of 4 neonicotinoids against Leptinotarsa decemlineata . Agrochemicals, 2011, 50(2):137-140. (in Chinese)
[15]	BRADFORD M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 1976, 72:248-254. doi: 10.1016/0003-2697(76)90527-3
[16]	祝海栋, 李瑞琳, 何小雨, 赵丹, 韩鑫胤, 牛北方. 六倍体小麦基因组注释流程构建与优化. 计算机系统应用, 2019, 28(8):222-228.
	ZHU H D, LI R L, HE X Y, ZHAO D, HAN X Y, NIU B F. Construction and optimization of hexaploid wheat genome annotation process. Computer Systems and Applications, 2019, 28(8):222-228. (in Chinese)
[17]	LANGMEAD B, TRAPNELL C, POP M, SALZBERG S L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 2009, 10(3):R25. doi: 10.1186/gb-2009-10-3-r25
[18]	ZHU F, MOURAL T W, NELSON D R, PALLI S R. A specialist herbivore pest adaptation to xenobiotics through up-regulation of multiple cytochrome P450s. Scientific Reports, 2016, 6:20421. doi: 10.1038/srep20421
[19]	王彦华, 陈进, 沈晋良, 高聪芬, 黄悦, 张久双, 李文红, 周威君. 防治褐飞虱的高毒农药替代药剂的室内筛选及交互抗性研究. 中国水稻科学, 2008, 22(5):519-526.
	WANG Y H, CHEN J, SHEN J L, GAO C F, HUANG Y, ZHANG J S, LI W H, ZHOU W J. Laboratory screening and cross-resistance analysis of alternative insecticides for highly-toxic pesticides for controlling brown planthopper, Nilaparvata lugens . Chinese Journal of Rice Science, 2008, 22(5):519-526. (in Chinese)
[20]	LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔCT method. Methods, 2001, 25(4):402-408. doi: 10.1006/meth.2001.1262
[21]	MOTA-SANCHEZ D, WHALON M, GRAFIUS E, HOLLINGWOETH R. Resistance of Colorado potato beetle to imidacloprid. Resistant Pest Management, 2000, 11(1):31-34.
[22]	张钰明, 向兴, 王学贵. 噻虫嗪对褐飞虱的毒力及解毒代谢酶活性的影响. 华南农业大学学报, 2020, 41(3):80-85.
	ZHANG Y M, XIANG X, WANG X G. Effects of thiamethoxam on toxicity and detoxification metabolic enzyme activity of Nilaparvata lugens . Journal of South China Agricultural University, 2020, 41(3):80-85. (in Chinese)
[23]	CLEMENTS J, SANCHEZ-SEDILLO B, BRADFIELD C A, GROVES R L. Transcriptomic analysis reveals similarities in genetic activation of detoxification mechanisms resulting from imidacloprid and chlorothalonil exposure. PLoS ONE, 2018, 13(10):e0205881. doi: 10.1371/journal.pone.0205881
[24]	WU M C, CHANG Y W, LU K H, YANG E C. Gene expression changes in honey bees induced by sublethal imidacloprid exposure during the larval stage. Insect Biochemistry and Molecular Biology, 2017, 88:12-20. doi: 10.1016/j.ibmb.2017.06.016
[25]	刘昌燕, 曾凡荣. 大草蛉P450基因cDNA片段的克隆及吡虫啉诱导表达. 中国生物防治学报, 2014, 30(3):427-433.
	LIU C Y, ZENG F R. Cloning of Chrysopa pallens P450 cDNA fragment and the expression induced by imidacloprid . Chinese Journal of Biological Control, 2014, 30(3):427-433. (in Chinese)
[26]	ZHANG Y X, YANG Y X, SUN H H, LIU Z W. Metabolic imidacloprid resistance in the brown planthopper, Nilaparvata lugens, relies on multiple P450 enzymes. Insect Biochemistry and Molecular Biology, 2016, 79:50-56. doi: 10.1016/j.ibmb.2016.10.009

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

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

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

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

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

新疆马铃薯甲虫对噻虫嗪的抗性监测及其细胞色素P450基因表达分析

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

RichHTML

PDF

赞

可视化

摘要/Abstract

引用本文

使用本文

图/表 12

参考文献 26

相关文章 15

Metrics

本文评价

推荐阅读 0

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

采集时间 Sampling time	基因 Gene	R 值R value		P 值P value
采集时间 Sampling time	基因 Gene	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

[1]	张克坤,陈可钦,李婉平,乔浩蓉,张俊霞,刘凤之,房玉林,王海波. 灌水量对限根栽培‘阳光玫瑰’葡萄果实发育与香气物质积累的影响[J]. 中国农业科学, 2023, 56(1): 129-143.
[2]	古丽旦,刘洋,李方向,成卫宁. 小麦吸浆虫小热激蛋白基因Hsp21.9的克隆及在滞育过程与温度胁迫下的表达特性[J]. 中国农业科学, 2023, 56(1): 79-89.
[3]	束婧婷,单艳菊,姬改革,章明,屠云洁,刘一帆,巨晓军,盛中伟,唐燕飞,李华,邹剑敏. 广西麻鸡m6A甲基转移酶基因表达与肌纤维类型及成肌分化的关系[J]. 中国农业科学, 2022, 55(3): 589-601.
[4]	李志玲,李香菊,崔海兰,于海燕,陈景超. 牛筋草EPSPS酶联免疫试剂盒的研发及应用[J]. 中国农业科学, 2022, 55(24): 4851-4862.
[5]	郭绍雷,许建兰,王晓俊,宿子文,张斌斌,马瑞娟,俞明亮. 桃XTH家族基因鉴定及其在桃果实贮藏过程中的表达特性[J]. 中国农业科学, 2022, 55(23): 4702-4716.
[6]	郝艳,李晓颍,叶茂,刘亚婷,王天宇,王海静,张立彬,肖啸,武军凯. ‘21世纪’桃与‘久脆’桃及其杂交后代果实挥发性成分特征分析[J]. 中国农业科学, 2022, 55(22): 4487-4499.
[7]	王帅宇,张子腾,谢爱婷,董杰,杨建国,张爱环. 我国草地贪夜蛾种群杀虫剂靶标基因突变分析[J]. 中国农业科学, 2022, 55(20): 3948-3959.
[8]	康忱,赵雪芳,李亚栋,田哲娟,王鹏,吴志明. 黄瓜CC-NBS-LRR家族基因鉴定及在霜霉病和白粉病胁迫下的表达分析[J]. 中国农业科学, 2022, 55(19): 3751-3766.
[9]	温玉霞,张坚,王琴,王靖,裴悦宏,田绍锐,樊光进,马小舟,孙现超. 本氏烟NbMBF1c的克隆、表达及在TMV侵染过程中的功能[J]. 中国农业科学, 2022, 55(18): 3543-3555.
[10]	尹飞,李振宇,SAMINA Shabbir,林庆胜. P450基因在氯虫苯甲酰胺不同抗性品系小菜蛾中的表达及功能分析[J]. 中国农业科学, 2022, 55(13): 2562-2571.
[11]	金梦娇,刘博,王抗抗,张广忠,钱万强,万方浩. 薇甘菊光能利用及叶绿素合成在不同光照强度下的响应[J]. 中国农业科学, 2022, 55(12): 2347-2359.
[12]	袁景丽,郑红丽,梁先利,梅俊,余东亮,孙玉强,柯丽萍. 花青素代谢对陆地棉叶片和纤维色泽呈现的影响[J]. 中国农业科学, 2021, 54(9): 1846-1855.
[13]	束婧婷,姬改革,单艳菊,章明,巨晓军,刘一帆,屠云洁,盛中伟,唐燕飞,蒋华莲,邹剑敏. IGF1-PI3K-Akt信号通路相关基因在黄羽肉鸡肌肉和肝脏中的表达[J]. 中国农业科学, 2021, 54(9): 2027-2038.
[14]	赵珂,郑林,杜美霞,龙俊宏,何永睿,陈善春,邹修平. 柑橘SAR及其信号转导基因CsSABP2在黄龙病菌侵染中的响应特征[J]. 中国农业科学, 2021, 54(8): 1638-1652.
[15]	郑海霞,高玉林,张方梅,杨超霞,蒋健,朱勋,张云慧,李祥瑞. 马铃薯甲虫热激蛋白基因Ld-hsp70的克隆及温度胁迫下的表达特性[J]. 中国农业科学, 2021, 54(6): 1163-1175.