灰飞虱对毒死蜱和噻嗪酮的抗性机制研究
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摘要
灰飞虱Laodelphax striatellus (Fallen)是我国粮食作物上的一种重要害虫,它不仅刺吸取食禾本科植物造成虫害,还通过传播病毒而引起水稻、玉米、小麦等重要粮食作物的病毒病。2000年以前灰飞虱在我国只是零星发生,长期作为次要害虫对其进行防治。但自从2005年以来,该虫在我国许多地区特别是江苏、山东等省频繁暴发。长期大面积和不合理使用化学药剂导致灰飞虱抗药性的产生,灰飞虱对杀虫剂抗药性的产生是其近年来暴发频繁的主要原因之一。因此,必须加强灰飞虱的抗性治理,以期延缓其抗性进一步发展。明确杀虫剂的抗性机制是害虫抗性治理的前提。本文以灰飞虱室内抗药性筛选为基础,系统地研究了灰飞虱对毒死蜱和噻嗪酮的抗性生化、分子生物学机理。为更好地进行灰飞虱抗性治理和新药开发提供新的依据。
一、灰飞虱抗毒死蜱品系的抗性筛选及生化机理研究
经过对灰飞虱云南敏感品系(YN)连续32代的毒死蜱抗性筛选,与云南品系相比,毒死蜱抗性品系(YN-CPF)的抗药性上升到213.49倍；该抗性品系在连续12代无药剂筛选压力下其抗性衰退为83.08倍,以此作为抗性衰退品系(YN-DPF)。以YN, YN-DPF和YN-CPF品系为试虫,通过解毒代谢酶活力和增效剂生物测定分析,研究了灰飞虱对毒死蜱的抗性生化机理。分别在YN-CPF、YN-DPF和YN品系中测定了PBO、 DEM和TPP对毒死蜱的增效作用。结果显示在抗性和抗性衰退品系中,多功能氧化酶抑制剂PBO分别对毒死蜱有3.77倍和2.28倍的增效作用,谷胱甘肽S-转移酶抑制剂DEM对毒死蜱的增效作用分别为2.82倍和1.79倍,羧酸酯酶抑制剂TPP对毒死蜱的增效作用分别为4.31倍和2.59倍,三种增效剂在敏感品系中均未对毒死蜱表现出显著的增效作用。解毒代谢酶活力测定结果显示抗性品系细胞色素P450单加氧酶活力为敏感品系的0.67倍；谷胱甘肽S-转移酶活力在两品系间无显著差异；酯酶活力在抗性和抗性衰退品系中分别为敏感品系中的4.15倍和1.92倍。此外,抗性品系乙酰胆碱酯酶最大反应速率(Km)是敏感品系的2.56倍,亲和力及氧化毒死蜱抑制中浓度分别为敏感品系的1.81倍(Km-YN-CPF/Km-YN)和5.53倍(I50-YN-CPF/I50-YN)。以上结果说明,酯酶活性提高以及乙酰胆碱酯酶敏感性下降可能参与了毒死蜱的抗性形成,关于细胞色素P450单加氧酶和谷胱甘肽S-转移酶在毒死蜱抗性中的具体作用方式还需进一步研究。
二、灰飞虱抗噻嗪酮品系的抗性筛选及生化机理研究
对灰飞虱YN品系连续41代的噻嗪酮抗性筛选,获得了82.08倍的相对噻嗪酮抗性品系YN-BPF;对南京田间灰飞虱品系(NJ)连续12代的噻嗪酮抗药性筛选,与初始NJ和YN品系相比,获得的南京抗性品系(NJ-BPF)对噻嗪酮的相对抗性分别为4.46倍和96.58倍。以’YN-BPF、NJ-BPF品系和YN品系为试虫,通过解毒代谢酶活力和增效剂生物测定分析,初步研究了灰飞虱对噻嗪酮抗性的生化机理。分别在YN. NJ-BPF和YN-BPF品系中测定了PBO、DEM和TPP对噻嗪酮的增效作用,结果显示,三类增效剂在YN品系中对噻嗪酮都未表现出显著的增效作用。在YN-BPF和NJ-BPF品系中,PBO分别对噻嗪酮有1.77倍和1.69倍的增效作用,细胞色素P450单加氧酶活力也分别比敏感品系中升高了1.39倍和1.89倍； DEM分别对噻嗪酮有1.02倍和1.03倍的增效作用,谷胱甘肽S-转移酶活力在噻嗪酮抗、感品系间也未表现出显著差异；酯酶抑制剂TPP分别对噻嗪酮有1.50倍和1.77倍的增效作用,酯酶活力与YN品系相比分别升高了1.69倍和2.16倍。此外,YN-BPF和NJ-BPF品系中乙酰胆碱酯酶酶活力分别为YN品系的1.79和1.53倍。以上研究结果表明,酯酶及细胞色素P450单加氧酶活力的提高在一定程度上参与了噻嗪酮代谢抗性的形成,而乙酰胆碱酯酶活力升高对噻嗪酮抗性的形成可能也有一定的辅助作用。
三、灰飞虱羧酸酯酶基因序列及表达量分析
以云南敏感品系为材料,运用RT-PCR技术从灰飞虱转录组数据库中成功验证出31条灰飞虱羧酸酯酶基因(暂名为Ls.CarE1-31).分别在毒死蜱抗性和敏感品系中比较了这些基因的表达差异,结果发现：与YN品系相比,Ls. CarE1和Ls.CarE2在YN-CPF品系中分别具有32.6倍和7.52倍的显著过量表达。以YN-DPF品系为实验材料,分析过量表达的羧酸酯酶基因的抗性相关性,结果显示,Ls.CarE1和Ls.CarE2在抗性衰退品系中的表达量分别为敏感品系中的8.6倍和1.09倍。这些结果表明,过量表达的Ls.CarE1与毒死蜱抗性水平密切相关,而在毒死蜱抗性品系中过量表达的Ls.CarE2与抗性水平不存在一致的相关性。此外,毒死蜱抗性和敏感品系中的羧酸酯酶氨基酸序列比较发现,毒死蜱抗性个体中Ls.CarE9、Ls.CarEl6、Ls.CarE24和Ls.CarE25存在相对稳定的点突变。由此推断,不仅过量表达的Ls.CarEl参与了毒死蜱抗性的形成,部分羧酸酯酶点突变也可能是毒死蜱抗性形成的重要因子。
四、灰飞虱细胞色素P450基因序列及表达分析
从灰飞虱转录组数据中筛选出编码细胞色素P450的序列112条(长度从100bp到2000bp以上),去掉较短的及重复测序的序列,RT-PCR共验证出大于279bp的灰飞虱P450基因55条,其中26条具有完整的氨基酸序列编码区。进一步在灰飞虱抗、感噻嗪酮和毒死蜱的品系中分析了这些基因的表达情况。与敏感品系相比,CYP6CW1在噻嗪酮抗性品系中表现出9.75倍的过量表达。此外,3个P450基因(CYP4C,CYP4DE1和CYP6AX)在毒死蜱抗性品系中表达量与敏感品系的相比分别下降了82.01%,89.22%和92.25%。这些结果表明,过量表达的CYP6CW1可能在噻嗪酮抗性中发挥重要作用,减少的毒死蜱活化也有可能参与了毒死蜱抗性的形成。
五、毒死蜱抗性相关的羧酸酯酶基因RNAi功能分析及原核表达
利用cDNA末端快速扩增技术(RACE)克隆了灰飞虱Ls.CarEl的全长cDNA序列。Ls.CarEl全长共1839bp,编码547个氨基酸,5'-UTR为87bp,3'-UTR为111bp。序列分析表明LsCarEl具有羧酸酯酶的基因序列特征,包括三个催化三联体氨基酸残基Ser215、Glu345、His466;氧负离子孔Gly134、Gly135、Ala217;半胱氨酸环残基Cys92、Cys110等编码序列。氨基酸序列比对表明,Ls.CarEl与已报道的褐飞虱羧酸酯酶序列(GenBank:AAG40239.1)同源性达72%。因此推断Ls.CarEl序列为灰飞虱的羧酸酯酶基因序列。接着对其RNAi分析发现,以两个不同浓度(80ng/ul和200ng/ul)的Ls.CarE1-dsRNA连续6天喂养灰飞虱抗毒死蜱品系的一龄若虫后,Ls.CarEl的表达量分别下降62.6%和68.72%。进一步以毒死蜱(800mg/L)对RNA干扰后的抗性品系灰飞虱进行毒力测定,结果显示：与对照相比,死亡率分别由33.7%上升至72.31%(80ng/ul)和31.7%上升至69.56%(200ng/ul).这些结果说明,过量表达的Ls.CarE1在毒死蜱抗性形成中发挥着重要的作用。由于基因表达量增强不一定造成蛋白水平的增加,为此通过原核表达技术成功表达了灰飞虱的Ls.CarE1,为进一步对其进行抗体制备,Western-blot检测毒死蜱抗、感品系间蛋白质量变奠定了基础。
The small brown planthopper Laodelphax striatellus (Fallen) is a kind of pests that bring serious harm to grain crops. It is not only sucking the gramineous plants, but also spreading the virus between crops. This pest broke out only intermittently in China, and it was not an important pest for pest controlling before2000years. Since the early2005, however L. striatellus has reAChEd large number in china, especially in Jiangsu province. Long-term and unreasonable using of chemical insecticides in a wide range of rice-growing areas is the important reason for resistance of L. striatellus to the insecticides, and in recent years, insecticide resistance has been associated with frequent occurrence of the L. striatellus. Therefore, insecticide resistance management strategies must be developed to prevent further increase in resistance of L. striatellus. Lacking of the knowledge of resistance mechanism is the barrier for implementation of resistance management and efficient control. In this paper, efforts have been made to declare its biochemical and molecular mechanism of resistance to two types of synthetic insecticides, chlorpyrifos and buprofezin, which have been frequently used for controlling L. striatellus and other crop insect pests in fields for years, based on the lab-selected resistance strains. The results obtained are summarized as follows.
1. The resistance selection and biochemical mechanism of chlorpyrifos resistance in L. striatellus
Compared with the susceptible strain (YN), the chlorpyrifos resistance strain (YN-CPF) of L. striatellus developed213.49-fold resistance by continuous selection with chlorpyrifos for36generations on the strain YN in the laboratory. The chlorpyrifos resistance recession strain (YN-DPF) of L. striatellus came from the strain YN-CPF and was reared without contacting with any insecticides for12consecutive generations, and the resistance levels of strain YN-DPF recovered to83.08-fold relative to the strain YN. The biochemical mechanisms of chlorpyrifos resistance in L. striatellus were first studied by synergism test and detoxifying enzyme activity. The synergistic effects of PBO, TPP and DEM on chlorpyrifos in strain YN were compared with those in strains YN-CPF and YN-DPF. The resultes indicated that the oxidase inhibitor PBO showed3.77-and2.28-fold synergism with chlorpyrifos in strains YN-CPF and YN-DPF respectively, but no synergism of chlorpyrifos efficacy in strain YN, P450monooxygenase activity in strain YN-CPF was lower (only68%of the YN level) than in strain YN; The glutathione depleter DEM showed2.82-and1.79-fold synergism with chlorpyrifos in strains YN-CPF and YN-DPF respectively, but no synergism of chlorpyrifos efficacy was also found in strain YN, while the glutathione S-transferase activity towards CDNB was not significantly different between the distinct strains; The esterase inhibitor TPP synergized chlorpyrifos both in strains YN-CPF (4.31-fold) and YN-DPF (2.59-fold), but not in strain YN, while esterase activity using α-naphthyl acetate as substrate was significantly higher both in strains YN-CPF (4.15-fold) and YN-DPF (1.92-fold) than in strain YN. In addition, this study also found the maximum reaction rate (Vmax) of acetylcholinesterase (AChE) in strain YN-CPF was2.56-fold higher than that in strain YN. Affinity (Km) and inhibition concentration (Ⅰ10) experiment of AChE on chlorpyrifos-oxon also showed AChE insensitivity in the chlorpyrifos resistance strain. The results revealed that AChE insensitivity and elevated esterase activities may play important roles in conferring chlorpyrifos resistance in L. striatellus, the specific action mechanism of P450monooxygenase and glutathione S-transferase in L. striatellus on chlorpyrifos resistance remained to be further elucidated in future.
2. The resistance selection and biochemical mechanism of buprofezin resistance in L.striatellus
Compared with the strain YN, the buprofezin resistance strain (YN-BPF) of L. striatellus developed82.08-fold resistance by41generations of continuous selection with buprofezin on the strain YN in the laboratory; After12generations of continuous selection with buprofezin on the nanjing field strain (NJ), we obtained another buprofezin resistance strain (NJ-BPF) of L. striatellus which separately showed4.46-and96.58-fold resistance in comparison with the strains NJ and YN. The biochemical mechanisms of buprofezin resistance in L. striatellus were studied by synergism test and detoxifying enzyme activity. The synergistic effects of PBO, TPP and DEM on buprofezin in strain YN were compared with those in strains YN-BPF and NJ-BPF. The results showed that they all had no synergistic effects on strain YN, but the oxidase inhibitor PBO had1.77-and1.69-fold synergism with buprofezin in strains YN-BPF and NJ-BPF respectively, and P450 monooxygenase activity in strains YN-BPF (1.39-fold) and NJ-BPF (1.89-fold) was higher than that in strain YN. The glutathione depleter DEM showed1.02-and1.03-fold synergism with buprofezin in strains YN-BPF and NJ-BPF respectively, and the glutathione S-transferase activity towards CDNB was not significantly different among three strains. The esterase inhibitor TPP synergised buprofezin both in strains YN-BPF (1.50-fold) and NJ-BPF (1.77-fold), while esterase activity using a-naphthyl acetate as substrate was significantly higher in strains YN-BPF (1.69-fold) and NJ-BPF (2.16-fold) than that in strain YN. In addition, this study also found the activity of acetylcholinesterase (AChE) in strains YN-BPF and NJ-BPF were separately1.79-and1.53-fold higher than that in strain YN. The results indicated that enhanced detoxification that was mediated by P450monooxygenase and esterase could contribute to buprofezin resistance to some extent, moreover, the elevated AChE activity as an additional mechanism of buprofezin resistance cannot be ruled out.
3. The sequence identification and expression analysis of carboxylesterase genes in L. striatellus
31carboxylesterase-like genes (CarEs) were identified from the transcriptome database of L striatellus by using RT-PCR technique (tentatively named by Ls.CarEl-Ls.CarE31). Real-time quantitative PCR (qPCR) was performed for the relative expression analysis of31CarEs. Compared with that in strain YN, Ls.CarEl and Ls.CarE2showed significantly overexpression with32.06-and8.52-fold in strain YN-CPF, respectively. Then, qPCR of Ls.CarEl and Ls.CarE2in strain YN-DPF was conducted to verify their correlation with chlorpyrifos resistance. Compared with that in strain YN, the expression levels of Ls.CarEl and Ls.CarE2separately showed8.6-and1.09-fold in strain YN-DPF, which indicated a significant linear relationship between the expression level of Ls.CarEl and the level of phenotypic resistance (LC50), but didn't in the case of Ls.CarE2. In addition, this study also found some amino acid mutations of Ls.CarE9, Ls.CarEl6, Ls.CarE24and Ls.CarE25in YN-CPF individuals. The results indicated that overexpression of Ls.CarEl might play important roles in conferring chlorpyrifos resistance in strain YN-CPF, and the amino acid mutants of carboxylesterase genes as an additional resistance mechanism cannot be ruled out.
4. The sequence identification and expression analysis of P450genes in L. striatellus
A total of112unique sequences annotated as cytochrome P450genes (P450s)(partial or full length cDNA, from100bp to over2000bp) were identified from the transcriptome database of L. striatellus. After the shorter and repeated sequences were deleted, we finally obtained55P450s which ranging from279bp to2001bp in length, of which25P450s had the complete open reading frame (ORF), the55P450s were named by Dr. David Nelson in accordance with the P450nomenclature committee convention (http://drnelson.uthsc.edu/cytochromeP450. html). Then qPCR was used to analyze the relative expression levels of the55P450s among those resistant and susceptible strains of chlorpyrifos and buprofezin. Of these genes, CYP6CW1showed9.72-fold higher expression in strain YN-BPF than in strain YN. Among the55P450s, the expression of CYP4C, CYP4DE1and CYP6AX decreased82.01%,89.22%and92.25%in strain YN-CPF compared with that in strain YN. These results suggested that overexpression of CYP6CW1might play important roles in conferring buprofezin resistances, and chlorpyrifos resistance might be partially achieved through decrease chlorpyrifos activation in L. striatellus.
5. The functional analysis via RNAi and prokaryotic expression of carboxylesterase gene to elucidate the chlorpyrifos resistance in L. striatellus
The Rapid Amplification of cDNA Ends (RACE) technique was employed to clone the full-length sequence of Ls.CarEl from L. striatellus. The results showed that the ORF of Ls.CarEl was1839bp, encoding sequences of474aa in size. The5'and3'untranslated regions (UTR) were87bp and111bp, respectively. Analysis of the Ls.CarEl sequence revealed that it had these characteristics shared in many insect carboxylesterase genes, including the catalytic triads Ser215, Glu345and His466; oxyanion hole Gly134, Gly135and Ala217; the conserved cysteines Cys92and Cys110. Homologous analysis of amino acid sequences indicated that Ls.CarEl shared72%high identity with the carboxylesterase gene of Nilaparvata lugens (GenBank accession no. CAZ65617.1), so we could conclude that the Ls.CarEl was carboxylesterase gene in L. striatellus. Furthermore, Ls.CarEl was chosen for RNA interference (RNAi) followed by chlorpyrifos bioassay. The dsRNA concentrations for RNAi were separately designated as doses of80ng/ul and200ng/μL. qPCR was performed to analyze the relative expression level of Ls.CarEl after ingestion of the dsRNA on the sixth day. The results showed that the transcript level of Ls. CarEl was significantly decreased (60%for80ng/ul and70%for200ng/μL) as compared with those in the controls. At the same time, mortalities of the YN-CPF nymphs by RNAi increased from33.7%to72.31%(for80ng/ul) and31.7%to69.56%(for200ng/μL), respectively. These results provided a believable evidence for the role of Ls.CarEl in the resistance of L. striatellus to chlorpyrifos. Overexpression of gene does not always result in increasing of protein content. Therefore, we obtained the fusion protein of Ls.CarEl through prokaryotic expression technology, which laid a foundation for the following experiment on specific antibody preparation and western-blot to detect the difference of Ls.CarEl quantity between the chlorpyrifos resistance and susceptive strain.
一、灰飞虱抗毒死蜱品系的抗性筛选及生化机理研究
经过对灰飞虱云南敏感品系(YN)连续32代的毒死蜱抗性筛选,与云南品系相比,毒死蜱抗性品系(YN-CPF)的抗药性上升到213.49倍；该抗性品系在连续12代无药剂筛选压力下其抗性衰退为83.08倍,以此作为抗性衰退品系(YN-DPF)。以YN, YN-DPF和YN-CPF品系为试虫,通过解毒代谢酶活力和增效剂生物测定分析,研究了灰飞虱对毒死蜱的抗性生化机理。分别在YN-CPF、YN-DPF和YN品系中测定了PBO、 DEM和TPP对毒死蜱的增效作用。结果显示在抗性和抗性衰退品系中,多功能氧化酶抑制剂PBO分别对毒死蜱有3.77倍和2.28倍的增效作用,谷胱甘肽S-转移酶抑制剂DEM对毒死蜱的增效作用分别为2.82倍和1.79倍,羧酸酯酶抑制剂TPP对毒死蜱的增效作用分别为4.31倍和2.59倍,三种增效剂在敏感品系中均未对毒死蜱表现出显著的增效作用。解毒代谢酶活力测定结果显示抗性品系细胞色素P450单加氧酶活力为敏感品系的0.67倍；谷胱甘肽S-转移酶活力在两品系间无显著差异；酯酶活力在抗性和抗性衰退品系中分别为敏感品系中的4.15倍和1.92倍。此外,抗性品系乙酰胆碱酯酶最大反应速率(Km)是敏感品系的2.56倍,亲和力及氧化毒死蜱抑制中浓度分别为敏感品系的1.81倍(Km-YN-CPF/Km-YN)和5.53倍(I50-YN-CPF/I50-YN)。以上结果说明,酯酶活性提高以及乙酰胆碱酯酶敏感性下降可能参与了毒死蜱的抗性形成,关于细胞色素P450单加氧酶和谷胱甘肽S-转移酶在毒死蜱抗性中的具体作用方式还需进一步研究。
二、灰飞虱抗噻嗪酮品系的抗性筛选及生化机理研究
对灰飞虱YN品系连续41代的噻嗪酮抗性筛选,获得了82.08倍的相对噻嗪酮抗性品系YN-BPF;对南京田间灰飞虱品系(NJ)连续12代的噻嗪酮抗药性筛选,与初始NJ和YN品系相比,获得的南京抗性品系(NJ-BPF)对噻嗪酮的相对抗性分别为4.46倍和96.58倍。以’YN-BPF、NJ-BPF品系和YN品系为试虫,通过解毒代谢酶活力和增效剂生物测定分析,初步研究了灰飞虱对噻嗪酮抗性的生化机理。分别在YN. NJ-BPF和YN-BPF品系中测定了PBO、DEM和TPP对噻嗪酮的增效作用,结果显示,三类增效剂在YN品系中对噻嗪酮都未表现出显著的增效作用。在YN-BPF和NJ-BPF品系中,PBO分别对噻嗪酮有1.77倍和1.69倍的增效作用,细胞色素P450单加氧酶活力也分别比敏感品系中升高了1.39倍和1.89倍； DEM分别对噻嗪酮有1.02倍和1.03倍的增效作用,谷胱甘肽S-转移酶活力在噻嗪酮抗、感品系间也未表现出显著差异；酯酶抑制剂TPP分别对噻嗪酮有1.50倍和1.77倍的增效作用,酯酶活力与YN品系相比分别升高了1.69倍和2.16倍。此外,YN-BPF和NJ-BPF品系中乙酰胆碱酯酶酶活力分别为YN品系的1.79和1.53倍。以上研究结果表明,酯酶及细胞色素P450单加氧酶活力的提高在一定程度上参与了噻嗪酮代谢抗性的形成,而乙酰胆碱酯酶活力升高对噻嗪酮抗性的形成可能也有一定的辅助作用。
三、灰飞虱羧酸酯酶基因序列及表达量分析
以云南敏感品系为材料,运用RT-PCR技术从灰飞虱转录组数据库中成功验证出31条灰飞虱羧酸酯酶基因(暂名为Ls.CarE1-31).分别在毒死蜱抗性和敏感品系中比较了这些基因的表达差异,结果发现：与YN品系相比,Ls. CarE1和Ls.CarE2在YN-CPF品系中分别具有32.6倍和7.52倍的显著过量表达。以YN-DPF品系为实验材料,分析过量表达的羧酸酯酶基因的抗性相关性,结果显示,Ls.CarE1和Ls.CarE2在抗性衰退品系中的表达量分别为敏感品系中的8.6倍和1.09倍。这些结果表明,过量表达的Ls.CarE1与毒死蜱抗性水平密切相关,而在毒死蜱抗性品系中过量表达的Ls.CarE2与抗性水平不存在一致的相关性。此外,毒死蜱抗性和敏感品系中的羧酸酯酶氨基酸序列比较发现,毒死蜱抗性个体中Ls.CarE9、Ls.CarEl6、Ls.CarE24和Ls.CarE25存在相对稳定的点突变。由此推断,不仅过量表达的Ls.CarEl参与了毒死蜱抗性的形成,部分羧酸酯酶点突变也可能是毒死蜱抗性形成的重要因子。
四、灰飞虱细胞色素P450基因序列及表达分析
从灰飞虱转录组数据中筛选出编码细胞色素P450的序列112条(长度从100bp到2000bp以上),去掉较短的及重复测序的序列,RT-PCR共验证出大于279bp的灰飞虱P450基因55条,其中26条具有完整的氨基酸序列编码区。进一步在灰飞虱抗、感噻嗪酮和毒死蜱的品系中分析了这些基因的表达情况。与敏感品系相比,CYP6CW1在噻嗪酮抗性品系中表现出9.75倍的过量表达。此外,3个P450基因(CYP4C,CYP4DE1和CYP6AX)在毒死蜱抗性品系中表达量与敏感品系的相比分别下降了82.01%,89.22%和92.25%。这些结果表明,过量表达的CYP6CW1可能在噻嗪酮抗性中发挥重要作用,减少的毒死蜱活化也有可能参与了毒死蜱抗性的形成。
五、毒死蜱抗性相关的羧酸酯酶基因RNAi功能分析及原核表达
利用cDNA末端快速扩增技术(RACE)克隆了灰飞虱Ls.CarEl的全长cDNA序列。Ls.CarEl全长共1839bp,编码547个氨基酸,5'-UTR为87bp,3'-UTR为111bp。序列分析表明LsCarEl具有羧酸酯酶的基因序列特征,包括三个催化三联体氨基酸残基Ser215、Glu345、His466;氧负离子孔Gly134、Gly135、Ala217;半胱氨酸环残基Cys92、Cys110等编码序列。氨基酸序列比对表明,Ls.CarEl与已报道的褐飞虱羧酸酯酶序列(GenBank:AAG40239.1)同源性达72%。因此推断Ls.CarEl序列为灰飞虱的羧酸酯酶基因序列。接着对其RNAi分析发现,以两个不同浓度(80ng/ul和200ng/ul)的Ls.CarE1-dsRNA连续6天喂养灰飞虱抗毒死蜱品系的一龄若虫后,Ls.CarEl的表达量分别下降62.6%和68.72%。进一步以毒死蜱(800mg/L)对RNA干扰后的抗性品系灰飞虱进行毒力测定,结果显示：与对照相比,死亡率分别由33.7%上升至72.31%(80ng/ul)和31.7%上升至69.56%(200ng/ul).这些结果说明,过量表达的Ls.CarE1在毒死蜱抗性形成中发挥着重要的作用。由于基因表达量增强不一定造成蛋白水平的增加,为此通过原核表达技术成功表达了灰飞虱的Ls.CarE1,为进一步对其进行抗体制备,Western-blot检测毒死蜱抗、感品系间蛋白质量变奠定了基础。
The small brown planthopper Laodelphax striatellus (Fallen) is a kind of pests that bring serious harm to grain crops. It is not only sucking the gramineous plants, but also spreading the virus between crops. This pest broke out only intermittently in China, and it was not an important pest for pest controlling before2000years. Since the early2005, however L. striatellus has reAChEd large number in china, especially in Jiangsu province. Long-term and unreasonable using of chemical insecticides in a wide range of rice-growing areas is the important reason for resistance of L. striatellus to the insecticides, and in recent years, insecticide resistance has been associated with frequent occurrence of the L. striatellus. Therefore, insecticide resistance management strategies must be developed to prevent further increase in resistance of L. striatellus. Lacking of the knowledge of resistance mechanism is the barrier for implementation of resistance management and efficient control. In this paper, efforts have been made to declare its biochemical and molecular mechanism of resistance to two types of synthetic insecticides, chlorpyrifos and buprofezin, which have been frequently used for controlling L. striatellus and other crop insect pests in fields for years, based on the lab-selected resistance strains. The results obtained are summarized as follows.
1. The resistance selection and biochemical mechanism of chlorpyrifos resistance in L. striatellus
Compared with the susceptible strain (YN), the chlorpyrifos resistance strain (YN-CPF) of L. striatellus developed213.49-fold resistance by continuous selection with chlorpyrifos for36generations on the strain YN in the laboratory. The chlorpyrifos resistance recession strain (YN-DPF) of L. striatellus came from the strain YN-CPF and was reared without contacting with any insecticides for12consecutive generations, and the resistance levels of strain YN-DPF recovered to83.08-fold relative to the strain YN. The biochemical mechanisms of chlorpyrifos resistance in L. striatellus were first studied by synergism test and detoxifying enzyme activity. The synergistic effects of PBO, TPP and DEM on chlorpyrifos in strain YN were compared with those in strains YN-CPF and YN-DPF. The resultes indicated that the oxidase inhibitor PBO showed3.77-and2.28-fold synergism with chlorpyrifos in strains YN-CPF and YN-DPF respectively, but no synergism of chlorpyrifos efficacy in strain YN, P450monooxygenase activity in strain YN-CPF was lower (only68%of the YN level) than in strain YN; The glutathione depleter DEM showed2.82-and1.79-fold synergism with chlorpyrifos in strains YN-CPF and YN-DPF respectively, but no synergism of chlorpyrifos efficacy was also found in strain YN, while the glutathione S-transferase activity towards CDNB was not significantly different between the distinct strains; The esterase inhibitor TPP synergized chlorpyrifos both in strains YN-CPF (4.31-fold) and YN-DPF (2.59-fold), but not in strain YN, while esterase activity using α-naphthyl acetate as substrate was significantly higher both in strains YN-CPF (4.15-fold) and YN-DPF (1.92-fold) than in strain YN. In addition, this study also found the maximum reaction rate (Vmax) of acetylcholinesterase (AChE) in strain YN-CPF was2.56-fold higher than that in strain YN. Affinity (Km) and inhibition concentration (Ⅰ10) experiment of AChE on chlorpyrifos-oxon also showed AChE insensitivity in the chlorpyrifos resistance strain. The results revealed that AChE insensitivity and elevated esterase activities may play important roles in conferring chlorpyrifos resistance in L. striatellus, the specific action mechanism of P450monooxygenase and glutathione S-transferase in L. striatellus on chlorpyrifos resistance remained to be further elucidated in future.
2. The resistance selection and biochemical mechanism of buprofezin resistance in L.striatellus
Compared with the strain YN, the buprofezin resistance strain (YN-BPF) of L. striatellus developed82.08-fold resistance by41generations of continuous selection with buprofezin on the strain YN in the laboratory; After12generations of continuous selection with buprofezin on the nanjing field strain (NJ), we obtained another buprofezin resistance strain (NJ-BPF) of L. striatellus which separately showed4.46-and96.58-fold resistance in comparison with the strains NJ and YN. The biochemical mechanisms of buprofezin resistance in L. striatellus were studied by synergism test and detoxifying enzyme activity. The synergistic effects of PBO, TPP and DEM on buprofezin in strain YN were compared with those in strains YN-BPF and NJ-BPF. The results showed that they all had no synergistic effects on strain YN, but the oxidase inhibitor PBO had1.77-and1.69-fold synergism with buprofezin in strains YN-BPF and NJ-BPF respectively, and P450 monooxygenase activity in strains YN-BPF (1.39-fold) and NJ-BPF (1.89-fold) was higher than that in strain YN. The glutathione depleter DEM showed1.02-and1.03-fold synergism with buprofezin in strains YN-BPF and NJ-BPF respectively, and the glutathione S-transferase activity towards CDNB was not significantly different among three strains. The esterase inhibitor TPP synergised buprofezin both in strains YN-BPF (1.50-fold) and NJ-BPF (1.77-fold), while esterase activity using a-naphthyl acetate as substrate was significantly higher in strains YN-BPF (1.69-fold) and NJ-BPF (2.16-fold) than that in strain YN. In addition, this study also found the activity of acetylcholinesterase (AChE) in strains YN-BPF and NJ-BPF were separately1.79-and1.53-fold higher than that in strain YN. The results indicated that enhanced detoxification that was mediated by P450monooxygenase and esterase could contribute to buprofezin resistance to some extent, moreover, the elevated AChE activity as an additional mechanism of buprofezin resistance cannot be ruled out.
3. The sequence identification and expression analysis of carboxylesterase genes in L. striatellus
31carboxylesterase-like genes (CarEs) were identified from the transcriptome database of L striatellus by using RT-PCR technique (tentatively named by Ls.CarEl-Ls.CarE31). Real-time quantitative PCR (qPCR) was performed for the relative expression analysis of31CarEs. Compared with that in strain YN, Ls.CarEl and Ls.CarE2showed significantly overexpression with32.06-and8.52-fold in strain YN-CPF, respectively. Then, qPCR of Ls.CarEl and Ls.CarE2in strain YN-DPF was conducted to verify their correlation with chlorpyrifos resistance. Compared with that in strain YN, the expression levels of Ls.CarEl and Ls.CarE2separately showed8.6-and1.09-fold in strain YN-DPF, which indicated a significant linear relationship between the expression level of Ls.CarEl and the level of phenotypic resistance (LC50), but didn't in the case of Ls.CarE2. In addition, this study also found some amino acid mutations of Ls.CarE9, Ls.CarEl6, Ls.CarE24and Ls.CarE25in YN-CPF individuals. The results indicated that overexpression of Ls.CarEl might play important roles in conferring chlorpyrifos resistance in strain YN-CPF, and the amino acid mutants of carboxylesterase genes as an additional resistance mechanism cannot be ruled out.
4. The sequence identification and expression analysis of P450genes in L. striatellus
A total of112unique sequences annotated as cytochrome P450genes (P450s)(partial or full length cDNA, from100bp to over2000bp) were identified from the transcriptome database of L. striatellus. After the shorter and repeated sequences were deleted, we finally obtained55P450s which ranging from279bp to2001bp in length, of which25P450s had the complete open reading frame (ORF), the55P450s were named by Dr. David Nelson in accordance with the P450nomenclature committee convention (http://drnelson.uthsc.edu/cytochromeP450. html). Then qPCR was used to analyze the relative expression levels of the55P450s among those resistant and susceptible strains of chlorpyrifos and buprofezin. Of these genes, CYP6CW1showed9.72-fold higher expression in strain YN-BPF than in strain YN. Among the55P450s, the expression of CYP4C, CYP4DE1and CYP6AX decreased82.01%,89.22%and92.25%in strain YN-CPF compared with that in strain YN. These results suggested that overexpression of CYP6CW1might play important roles in conferring buprofezin resistances, and chlorpyrifos resistance might be partially achieved through decrease chlorpyrifos activation in L. striatellus.
5. The functional analysis via RNAi and prokaryotic expression of carboxylesterase gene to elucidate the chlorpyrifos resistance in L. striatellus
The Rapid Amplification of cDNA Ends (RACE) technique was employed to clone the full-length sequence of Ls.CarEl from L. striatellus. The results showed that the ORF of Ls.CarEl was1839bp, encoding sequences of474aa in size. The5'and3'untranslated regions (UTR) were87bp and111bp, respectively. Analysis of the Ls.CarEl sequence revealed that it had these characteristics shared in many insect carboxylesterase genes, including the catalytic triads Ser215, Glu345and His466; oxyanion hole Gly134, Gly135and Ala217; the conserved cysteines Cys92and Cys110. Homologous analysis of amino acid sequences indicated that Ls.CarEl shared72%high identity with the carboxylesterase gene of Nilaparvata lugens (GenBank accession no. CAZ65617.1), so we could conclude that the Ls.CarEl was carboxylesterase gene in L. striatellus. Furthermore, Ls.CarEl was chosen for RNA interference (RNAi) followed by chlorpyrifos bioassay. The dsRNA concentrations for RNAi were separately designated as doses of80ng/ul and200ng/μL. qPCR was performed to analyze the relative expression level of Ls.CarEl after ingestion of the dsRNA on the sixth day. The results showed that the transcript level of Ls. CarEl was significantly decreased (60%for80ng/ul and70%for200ng/μL) as compared with those in the controls. At the same time, mortalities of the YN-CPF nymphs by RNAi increased from33.7%to72.31%(for80ng/ul) and31.7%to69.56%(for200ng/μL), respectively. These results provided a believable evidence for the role of Ls.CarEl in the resistance of L. striatellus to chlorpyrifos. Overexpression of gene does not always result in increasing of protein content. Therefore, we obtained the fusion protein of Ls.CarEl through prokaryotic expression technology, which laid a foundation for the following experiment on specific antibody preparation and western-blot to detect the difference of Ls.CarEl quantity between the chlorpyrifos resistance and susceptive strain.
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