小菜蛾对氯虫苯甲酰胺抗性的分子机制
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摘要
小菜蛾Plutella xylostella (L.)是一种分布广泛的十字花科重要害虫。对小菜蛾的防治长期以化学农药为主,目前小菜蛾已经对92种含有不同活性成分的杀虫剂产生了抗性,成为全世界抗性最严重的害虫之一。氯虫苯甲酰胺是一种以鱼尼丁受体为靶标的具有全新作用机制的双酰胺类杀虫剂,对小菜蛾等鳞翅目害虫具有很好的防治效果。但使用短短几年后,在菲律宾、泰国、巴西和中国等地区均已发现对氯虫苯甲酰胺产生高水平抗性的小菜蛾田间种群。而且对其抗性机制一直不清楚。本文首先明确了低剂量氯虫苯甲酰胺处理对小菜蛾当代及子代的亚致死效应；然后通过对田间高抗小菜蛾种群鱼尼丁受体cDNA全长序列的克隆、分析及时空表达,从分子水平上揭示了小菜蛾对氯虫苯甲酰胺的抗性机制,并建立了小菜蛾田间种群抗性基因快速诊断技术。研究结果对于深入揭示小菜蛾等鳞翅目害虫对双酰胺类杀虫剂抗性的分子机制及田间种群抗性基因频率的快速检测具有重要的理论和实践意义。
本文首先在实验室条件下通过测定LC25剂量的氯虫苯甲酰胺处理小菜蛾后,对亲代和子代小菜蛾发育历期、化蛹率、幼虫体重、产卵量和成活率的影响从而评估了氯虫苯甲酰胺对小菜蛾发育和生殖的影响。当四龄小菜蛾幼虫喂食含有LC25剂量的氯虫苯甲酰胺后,从四龄到蛹的发育历期显著延长(4.27d vs3.34d),蛹重降低(3.58mg vs4.17mg),同时成虫产卵量也下降了42%。小菜蛾子代同样受到药剂的影响,例如发育历期延长,孵化率降低等。种群的生命表参数结果显示种群的净增长率,内禀增长率和周限增长率在处理组明显降低。
利用RT-PCR和RACE的方法,获得一条小菜蛾鱼尼丁受体cDNA全长序列,命名为PxRyRl。该序列全长15753bp,开放阅读框15354bp,编码5117个氨基酸。另一条由于可变剪切形成的基因命名为PxRyR2。PxRyRl与其他昆虫鱼尼丁受体具有77-93%的相似性。实时荧光定量PCR分析发现PxRyR在小菜蛾的二龄幼虫期和成虫期表达量最高,在预蛹和蛹期表达量最低。在幼虫的体壁肌肉组织和头部分布最多(表达量分别是消化道的6.00倍和3.12倍)。蛋白免疫印迹分析发现鱼尼丁受体主要分布在体壁肌肉组织和头部而在血淋巴和消化道中分布较少。
通过检测采自广东地区的四个田间氯虫苯甲酰胺高抗种群,在中国地区首次发现了PxRyR存在G4946E突变位点。更重要的是,通过分析田间小菜蛾抗性水平与G4946E突变频率的关系,发现二者之间呈明显的正相关(R2=0.82,P=0.0003)。配体结合试验结果表明,与敏感种群相比,三个田间高抗种群鱼尼丁受体受体与氯虫苯甲酰胺的结合能力均显著降低,分别比敏感种群低2.41倍、2.54倍和2.60倍。
生测结果显示,采自云南通海地区的小菜蛾种群对氯虫苯甲酰胺具有2128倍的抗性。通过对该种群小菜蛾鱼尼丁受体的全长基因检测,在高度保守区域首次发现了三个新的突变位点,分别为E1338D、Q4594L和I4790M。这三个突变表现出86.7%的高突变频率。更重要的是,通过分析这三个突变及已经报道的G4946E突变位点的连锁关系发现,四个突变通过不同的组合共同导致了小菜蛾对氯虫苯甲酰胺的抗性。
在明确了小菜蛾鱼尼丁受体中的四个突变位点与小菜蛾对氯虫苯甲酰胺的抗性关系后,通过设计等位基因特异性PCR引物,并合理优化等位基因特异性PCR方法(AS-PCR),最终针对E1338D、 Q4594L和G4946E三个突变位点建立了基于AS-PCR的点突变快速检测方法。与测序结果相比,AS-PCR检测方法能够有效区分不同位点的基因型,准确率可达98%。
定量PCR研究发现,PxRyR在所有抗性种群中的表达水平均显著高于敏感种群(2.28-4.14倍)；LC50和LC75的氯虫苯甲酰胺处理同样能诱导小菜蛾PxRyR的表达量增加。利用RNAi技术成功抑制PxRyR表达并没有引起小菜蛾死亡率升高,但是用低剂量氯虫苯甲酰胺(LC25)处理干扰组小菜蛾后,其死亡率显著增加。
The diamondback moth (DBM), Plutella xylostella (L.), is the most widely distributed major pest of crucifers. The annual global costs caused by the DBM have increased from approximately＄1billion in the1990s to＄4-5billion in recent years. However, due to the intensive application of insecticides and the biological characters (such as genetic plasticity, high fecundity and fast cycle) of the DBM, this pest has developed resistance to92compounds and become the most resistant pest insect in the world.
Chlorantraniliprole, a wildly applied diamide insecticide, owns a completely novel mode of action. While high levels of resistance to this insecticide in DBM were reported in Philippines, Thailand, Brazil and China after2-3years of extensive and repetitive application, while its mechanisms of resistance kept unknown. To reveal the molecular mechanisms of resistance to the chlorantraniliprole in DBM, several experiments were conducted, and the results were briefly described as follows:
Chlorantraniliprole showed dramatic sublethal effects on DBM. When4th instar DBM larvae were exposed to LC25of chlorantraniliprole on a cabbage (Brassica oleracea var. capitata L.) leaf for96h, increased developmental time for4th instar larval to pupa period(4.27days vs.3.34days in the control), lower pupal weight (3.58mg vs.4.17mg in the control) and decreased adult fecundity (by42%) were observed. F1generation underwent transgenerational effects, i.e. higher developmental time from egg to pre-pupae and lower egg hatching rate. Demographic growth parameters, such as the net reproductive rate (Ro), the intrinsic rate of increase (rm), and the finite rate of increase (λ) were significantly lower for the LC25chlorantraniliprole treated group than for the untreated control.
A full-length cDNA sequence of RyR was cloned from DBM through RT-PCR and rapid amplification of cDNA ends (RACE). The gene (named PxRyRl) is15,753bp long, with an open reading frame of15,354bp, encoding a predicted RyR of5117amino acids. An alternative splicing of the PxRyRl was also cloned and named PxRyR2. The PxRyRl shares77-93%identity with other insect RyRs. Quantitative real-time PCR analysis showed that the PxRyR was expressed at a high level in second-instar larvae and adults, at a low level in prepupae and pupae and abundantly in the body wall muscle and head (respectively6.00and3.12times of the expression in the gut). Western blot analysis with anti-RyR antibodies showed that the RyR was mainly present in the body wall muscle and head, but barely present in the haemocyte and gut.
In the four field chlorantraniliprole resistant populations collected in Guangdong province, we identified a point mutation (G4946E) in PxRyR. Most importantly, the frequency of the G4946E mutation is significantly correlated to the chlorantraniliprole resistance ratios in P. xylostella (R2=0.82,.P=0.0003). Ligand binding assays showed that the binding affinities of the PxRyR to chlorantraniliprole in three field resistant populations were2.41-,2.54-and2.60-times lower than that in the susceptible one. These results showed that the point mutation G4946E confered high chlorantraniliprole resistance in field DBM populations from Guangdong province.
Later, a field population was collected from Tonghai,Yunnan province, which showed2128-fold resistance to chlorantraniliprole. When examined the frequency of G4946E, only20%individuals were found mutant at position4946as heterozygous genotype. Then the full length of RyR was screened for other possible mutations, and three novel mutations, including a glutamic acid to valine substitution (E1338D), a glutamine to leucine substitution (Q4594L) and an isoleucine to methionine substitution (I4790M) were identified in highly conserved regions, and each mutation showed a high frequency of86.7%. More importantly, the co-existence of the three new mutations together with the previously reported G4946E were all involved in the chlorantraniliprole resistance through different combinations.
After definiting the role of four mutationsin in resistance to chlorantraniliprole, an allele-specific PCR (AS-PCR) based method was established for the diagnosis of the three mutations (E1338D, Q4594L and G4946E), which could efficiently detect these mutations with a98%accuracy.
Besides the four point muations, overexpression of PxRyR was also involved in chorantraniliprole resistance in DBM. qRT-PCR showed that the expression levels of PxRyR in several high resistant populations were2.28-4.14folds higher than that of the susceptible one. When the expression of PxRyR was successfully suppressed in both resistant and susceptible populations by injection of corresponding dsRNA,there showed no difference in mortality. However, when both resistant and susceptible populations were treated with LC25of chlorantraniliprole after dsRNA injection, the resistant population showed a significantly higher mortality than the susceptible one.
本文首先在实验室条件下通过测定LC25剂量的氯虫苯甲酰胺处理小菜蛾后,对亲代和子代小菜蛾发育历期、化蛹率、幼虫体重、产卵量和成活率的影响从而评估了氯虫苯甲酰胺对小菜蛾发育和生殖的影响。当四龄小菜蛾幼虫喂食含有LC25剂量的氯虫苯甲酰胺后,从四龄到蛹的发育历期显著延长(4.27d vs3.34d),蛹重降低(3.58mg vs4.17mg),同时成虫产卵量也下降了42%。小菜蛾子代同样受到药剂的影响,例如发育历期延长,孵化率降低等。种群的生命表参数结果显示种群的净增长率,内禀增长率和周限增长率在处理组明显降低。
利用RT-PCR和RACE的方法,获得一条小菜蛾鱼尼丁受体cDNA全长序列,命名为PxRyRl。该序列全长15753bp,开放阅读框15354bp,编码5117个氨基酸。另一条由于可变剪切形成的基因命名为PxRyR2。PxRyRl与其他昆虫鱼尼丁受体具有77-93%的相似性。实时荧光定量PCR分析发现PxRyR在小菜蛾的二龄幼虫期和成虫期表达量最高,在预蛹和蛹期表达量最低。在幼虫的体壁肌肉组织和头部分布最多(表达量分别是消化道的6.00倍和3.12倍)。蛋白免疫印迹分析发现鱼尼丁受体主要分布在体壁肌肉组织和头部而在血淋巴和消化道中分布较少。
通过检测采自广东地区的四个田间氯虫苯甲酰胺高抗种群,在中国地区首次发现了PxRyR存在G4946E突变位点。更重要的是,通过分析田间小菜蛾抗性水平与G4946E突变频率的关系,发现二者之间呈明显的正相关(R2=0.82,P=0.0003)。配体结合试验结果表明,与敏感种群相比,三个田间高抗种群鱼尼丁受体受体与氯虫苯甲酰胺的结合能力均显著降低,分别比敏感种群低2.41倍、2.54倍和2.60倍。
生测结果显示,采自云南通海地区的小菜蛾种群对氯虫苯甲酰胺具有2128倍的抗性。通过对该种群小菜蛾鱼尼丁受体的全长基因检测,在高度保守区域首次发现了三个新的突变位点,分别为E1338D、Q4594L和I4790M。这三个突变表现出86.7%的高突变频率。更重要的是,通过分析这三个突变及已经报道的G4946E突变位点的连锁关系发现,四个突变通过不同的组合共同导致了小菜蛾对氯虫苯甲酰胺的抗性。
在明确了小菜蛾鱼尼丁受体中的四个突变位点与小菜蛾对氯虫苯甲酰胺的抗性关系后,通过设计等位基因特异性PCR引物,并合理优化等位基因特异性PCR方法(AS-PCR),最终针对E1338D、 Q4594L和G4946E三个突变位点建立了基于AS-PCR的点突变快速检测方法。与测序结果相比,AS-PCR检测方法能够有效区分不同位点的基因型,准确率可达98%。
定量PCR研究发现,PxRyR在所有抗性种群中的表达水平均显著高于敏感种群(2.28-4.14倍)；LC50和LC75的氯虫苯甲酰胺处理同样能诱导小菜蛾PxRyR的表达量增加。利用RNAi技术成功抑制PxRyR表达并没有引起小菜蛾死亡率升高,但是用低剂量氯虫苯甲酰胺(LC25)处理干扰组小菜蛾后,其死亡率显著增加。
The diamondback moth (DBM), Plutella xylostella (L.), is the most widely distributed major pest of crucifers. The annual global costs caused by the DBM have increased from approximately＄1billion in the1990s to＄4-5billion in recent years. However, due to the intensive application of insecticides and the biological characters (such as genetic plasticity, high fecundity and fast cycle) of the DBM, this pest has developed resistance to92compounds and become the most resistant pest insect in the world.
Chlorantraniliprole, a wildly applied diamide insecticide, owns a completely novel mode of action. While high levels of resistance to this insecticide in DBM were reported in Philippines, Thailand, Brazil and China after2-3years of extensive and repetitive application, while its mechanisms of resistance kept unknown. To reveal the molecular mechanisms of resistance to the chlorantraniliprole in DBM, several experiments were conducted, and the results were briefly described as follows:
Chlorantraniliprole showed dramatic sublethal effects on DBM. When4th instar DBM larvae were exposed to LC25of chlorantraniliprole on a cabbage (Brassica oleracea var. capitata L.) leaf for96h, increased developmental time for4th instar larval to pupa period(4.27days vs.3.34days in the control), lower pupal weight (3.58mg vs.4.17mg in the control) and decreased adult fecundity (by42%) were observed. F1generation underwent transgenerational effects, i.e. higher developmental time from egg to pre-pupae and lower egg hatching rate. Demographic growth parameters, such as the net reproductive rate (Ro), the intrinsic rate of increase (rm), and the finite rate of increase (λ) were significantly lower for the LC25chlorantraniliprole treated group than for the untreated control.
A full-length cDNA sequence of RyR was cloned from DBM through RT-PCR and rapid amplification of cDNA ends (RACE). The gene (named PxRyRl) is15,753bp long, with an open reading frame of15,354bp, encoding a predicted RyR of5117amino acids. An alternative splicing of the PxRyRl was also cloned and named PxRyR2. The PxRyRl shares77-93%identity with other insect RyRs. Quantitative real-time PCR analysis showed that the PxRyR was expressed at a high level in second-instar larvae and adults, at a low level in prepupae and pupae and abundantly in the body wall muscle and head (respectively6.00and3.12times of the expression in the gut). Western blot analysis with anti-RyR antibodies showed that the RyR was mainly present in the body wall muscle and head, but barely present in the haemocyte and gut.
In the four field chlorantraniliprole resistant populations collected in Guangdong province, we identified a point mutation (G4946E) in PxRyR. Most importantly, the frequency of the G4946E mutation is significantly correlated to the chlorantraniliprole resistance ratios in P. xylostella (R2=0.82,.P=0.0003). Ligand binding assays showed that the binding affinities of the PxRyR to chlorantraniliprole in three field resistant populations were2.41-,2.54-and2.60-times lower than that in the susceptible one. These results showed that the point mutation G4946E confered high chlorantraniliprole resistance in field DBM populations from Guangdong province.
Later, a field population was collected from Tonghai,Yunnan province, which showed2128-fold resistance to chlorantraniliprole. When examined the frequency of G4946E, only20%individuals were found mutant at position4946as heterozygous genotype. Then the full length of RyR was screened for other possible mutations, and three novel mutations, including a glutamic acid to valine substitution (E1338D), a glutamine to leucine substitution (Q4594L) and an isoleucine to methionine substitution (I4790M) were identified in highly conserved regions, and each mutation showed a high frequency of86.7%. More importantly, the co-existence of the three new mutations together with the previously reported G4946E were all involved in the chlorantraniliprole resistance through different combinations.
After definiting the role of four mutationsin in resistance to chlorantraniliprole, an allele-specific PCR (AS-PCR) based method was established for the diagnosis of the three mutations (E1338D, Q4594L and G4946E), which could efficiently detect these mutations with a98%accuracy.
Besides the four point muations, overexpression of PxRyR was also involved in chorantraniliprole resistance in DBM. qRT-PCR showed that the expression levels of PxRyR in several high resistant populations were2.28-4.14folds higher than that of the susceptible one. When the expression of PxRyR was successfully suppressed in both resistant and susceptible populations by injection of corresponding dsRNA,there showed no difference in mortality. However, when both resistant and susceptible populations were treated with LC25of chlorantraniliprole after dsRNA injection, the resistant population showed a significantly higher mortality than the susceptible one.
引文
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