棉蚜对吡虫啉抗性机理的研究
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摘要
棉蚜Aphis gossypii (Glover)是一种世界性棉花害虫,由于其世代历期短,繁殖力强,加之田间不合理的用药习惯,导致我国田间棉蚜抗药性迅速发展且抗性背景相当复杂,这为该虫的化学防治造成了严重的困难。吡虫啉作为第一个商品化的新烟碱类杀虫剂,自上世纪90年代初开始推广使用,早已成为田间防治棉蚜的骨干药剂。为了延缓棉蚜对吡虫啉的抗性发展,延长其田间使用寿命,本研究通过室内抗性筛选、生物适合度以及交互抗性研究,系统分析了棉蚜对毗虫啉产生高水平抗性的风险；同时以室内筛选的抗性品系和敏感品系棉蚜为研究材料,利用现代分子生物技术,研究分析了棉蚜对吡虫啉产生抗性的生化和分子机制,旨在为该类药剂的科学使用提供指导。研究结果如下：
1、抗吡虫啉棉蚜品系的室内筛选及抗性风险评估
以杀死棉蚜群体60%-70%的剂量对敏感品系棉蚜持续筛选60代后,该品系棉蚜对吡虫啉的抗性达72.8倍,已经产生了高水平的吡虫啉抗性。该棉蚜品系从F0代筛选至F54代,抗性发展趋势较为平稳,抗性增加至47.0倍,达中等抗性水平；但由F54代筛选至F57代,抗性迅速由47.0倍增长至69.5倍,出现抗性突增期；由F57至F60抗性仍有小幅升高,但其发展又趋于缓慢,证明棉蚜对吡虫啉抗性发展趋势呈偏“S”型曲线。该抗性品系对烯啶虫胺(16.0倍)、啶虫脒(12.9倍)、噻虫嗪(11.6倍)、噻虫胺(9.84倍)、呋虫胺(9.50倍)、丁硫克百威(8.38倍)、高效氯氟氰菊酯(6.17倍)、氧乐果(6.13倍)和毒死蜱(5.10倍)均产生了明显的的交互抗性,但对哒螨灵和吡蚜酮的交互抗性水平较低(分别为2.28倍和4.52倍)。吡虫啉抗性和敏感品系生物学特性研究发现,RF60的蜜露分泌量、体重、若蚜存活率、内禀增长率和周限增长率均有所下降,特别是净生殖率,仅为敏感品系的47.7%,且世代周期延长了1.4天左右,相对适合度下降为0.71。
尽管吡虫啉使用中前期棉蚜对其抗性发展比较缓慢,但连续大量使用仍会导致抗性突增,因此尚存在产生高水平抗性的风险。交互抗性问题能够显著影响吡虫啉和大部分常规药剂特别是新烟碱类药剂的防效,在抗性治理中,仅有少数杀虫剂能够作为替代药剂使用。吡虫啉在棉蚜种群上会产生抗性代价,令其生长、发育和繁殖方面均受到一定程度的影响,从而使抗性品系群体增长受到抑制。
2、棉蚜对吡虫啉抗性的生化机理研究
以室内选育的吡虫啉抗性品系(抗性达72.8倍)和敏感品系棉蚜为材料,分别测定了四种解毒酶抑制剂对毗虫啉的增效作用,并且比较了两个品系棉蚜的解毒酶活性。其中SV1、DEM在棉蚜抗吡虫啉品系和敏感品系中均没有表现出明显的增效作用；而TPP和PBO则对吡虫啉起到了明显的增效作用,且在抗性品系中的增效作用显著高于在敏感品系中的增效作用；其中PBO的增效作用最为明显,在抗性品系中的增效比达到了2.97。酶活性测定结果表明,抗吡虫啉棉蚜品系的羧酸酯酶和乙酰胆碱酯酶比活力均高于敏感品系,尤其以羧酸酯酶比活力的提高最明显,而谷胱甘肽-S-转移酶的变化却并不显著。这些结果表明：多功能氧化酶和羧酸酯酶在棉蚜对吡虫啉产生抗性的过程中起到了重要的作用,而乙酰胆碱酯酶也起到了一定的辅助作用。
3、棉蚜对吡虫啉抗性的分子机理研究
以吡虫啉抗性品系和敏感品系棉蚜为材料,分别克隆了一个羧酸酯酶基因,两个P450单加氧酶六家族基因,五个乙酰胆碱受体α亚基和一个β亚基的cDNA序列,所有基因序列经同源序列比对后证实分别为棉蚜各功能基因。抗性和敏感品系棉蚜的羧酸酯酶及P450单加氧酶基因序列比对后并未发现抗性相关突变,但进一步的荧光定量分析发现,CYP6CY3-1基因在抗性品系棉蚜体内过量表达了5.66倍,羧酸酯酶基因过量表达了1.24倍,仅CYP6CY3-2基因的表达量未出现明显变化(1.03倍)。本研究得到的Agα2与Aga4亚基基因序列与NCBI上已登录的棉蚜乙酰胆碱受体α2和β4亚基cDNA序列相比更加完整,包含了翻译氨基酸序列所需的完整开放阅读框。比对各亚基氨基酸序列后发现,在抗性品系棉蚜Agβ1亚基上存在单一的位点突变R81T。
羧酸酯酶与P450单加氧酶基因的过量表达进一步证实了这两个解毒酶系在棉蚜对吡虫啉的抗性产生中起到了重要的作用。而本研究在抗吡虫啉棉蚜中首次发现的R81T氨基酸取代已被证实能够显著降低乙酰胆碱受体与吡虫啉的亲和力,因此,R81T突变直接导致了棉蚜对吡虫啉高水平抗性的产生。
综上所述,本研究通过室内选育明确了棉蚜对吡虫啉的高水平抗性风险,并通过抗性机理分析确定了靶标位点突变是棉蚜对吡虫啉产生高水平抗性的主要原因,同时P450单加氧酶和酯酶活力的升高也是棉蚜对吡虫啉产生抗性的机理之一。显然,本研究结果对建立田间抗性分子监测手段,制定合理的抗性治理策略,延缓田间棉蚜抗药性的发展具有重要指导意义。
The cotton aphid, Aphis gossypii (Glover), is one of the worldwide pests on cotton. Because of the short generation time and the high fecundity of cotton aphid, coupled with the irrational use of pesticides in field, resistance of cotton aphid is complex. So far, serious resistance of A. gossypii to conventional insecticides has resulted in many problems in controlling of this pest in China. Since the early1990s, as the first commercialization product of neonicotinoid insecticides, imidacloprid was extensively used and had become the dominated pesticide to control cotton aphid. To delay the resistance to imidacloprid and prolong its service life in the field, the risk of high level resistance to imidacloprid was studied systematically with the laboratory selected strain. With selected resistant strain and susceptible strain, the biochemical and molecular mechanisms for the resistance were also analyzed. The results are as follows:
1. The selection of imidacloprid-resistant strain of A. gossypii and the research of cross-resistance
The resistance level of A. gossypii to imidacloprid reached to72.8-fold after selection of60generations with the pressure to kill60%to70%individuals of the population. From Fo to F54, the resistance of A. gossypii to imidacloprid developed slowly in the initial and middle stage of resistance selection. However, there was a sudden increase in F57, and the resistance ratio suddenly increased from47.0-fold to69.5-fold. By F57to F60, the resistance was elevated slightly. It proved that the development of resistance to imidacloprid of cotton aphid also showed "S" shaped curve similarly. The cross-resistance phenomena of RF60to nitenpyram (16.0-fold), acetamiprid (12.9-fold), buprofezin (11.6-fold), clothianidin (9.84-fold), dinotefuran (9.50-fold), carbosulfan (8.38-fold), lambda-cyhalothrin (6.17-fold), omethoate (6.13-fold), and chlorpyrifos (5.10-fold) were obviously, while the cross-resistance to pymetrozine and pyridaben at a low level (2.28-and4.52-fold, respectively). Biological research of imidacloprid between resistant and susceptible strains found that the honeydew excretion, boby weight, nymphal survival rate, net reproductive rate and intrinsic rate of natural had declined. In particular, the net reproductive rate of RF60was only47.7%compared with the susceptible strain. At the same time, the mean generation time extended about1.4days and the relative fitness decreased to0.71.
The results of this study showed that the development of resistance to imidacloprid was relatively slow in the early stage, but the resistance of A. gossypii could increase suddenly after persistent imidacloprid selection, so the risk of high-level resistance still existed. Cross-resistance could significantly affect the effect of imidacloprid and most conventional insecticides, and only a small number of novel insecticides could use to be alternative pesticides. Imidacloprid conferred the fitness cost in A. gossypii, affecting its growth, development and reproduction, so the population growth of resistant strain could be inhibited.
2. Studies of biochemical mechanisms of imidacloprid resistance in A. gossypii
The biochemical mechanisms of imdacloprid resistance in A. gossypii were studied by testing the synergism of four enzyme inhibitors and the activity of related enzyme in resistant and susceptible strain of A. gossypii. The results showed that the synergism of PBO and TPP was singnificantly higher in the resistant strain than in the susceptible strain, especially when the synergism ratio of PBO was2.97. The synergism of SV1was relatively low, but DEM did not show any synergism on imidacloprid in both strains. Detoxifieation enzyme activity test in two strains showed that the activity of carboxylesterase (CarE) in resistant strain is much higher than the susceptible strain. However the activity of glutathione-S-transferase (GST) was similar in both strains. Furthermore, the activity of acetylcholinesterase (AChE) in resistant strain was a little higher than the susceptible strain. Thus, it was concluded that the enhanced carboxylesterase and cytochrome P450-monooxygenases detoxifieation might contribute to the high-level of imidacloprid resistance in A.gossypii. Acetylcholinesterase had also played a supporting role in the resistance.
3. Studies of molecular mechanisms of imidacloprid resistance in A. gossypii
We successfully cloned one carboxylesterase gene, two P450monooxygenase genes, five acetylcholine receptor a subunit and one β subunit from both resistant and susceptible strains. All genes we got were confirmed to belong to cotton aphid after homologous sequence alignment respectively. No mutation was found in the carboxylesterase and P450monooxygenase genes in the resistant strain, but the fluorescent quantitative analysis of three genes found that CYP6CY3-1and carboxylesterase gene overexpressed5.66-fold and 1.24-fold in resistant strain compared with the susceptible strain. Nevertheless, expression of CYP6CY3-2gene did not change obviously (only1.03-fold). The Aga2and Aga4subunit gene cDNA sequence we cloned in this study which contained the complete open reading frame were more complete than the A. gossypii nAChR a2and a4subunits cDNA sequences logged on NCBI previously. Comparison of the amino acid sequence of every subunit between the resistant and susceptible strains, a single mutation (R81T) in Agβ1subunit was observed from the resistant strain.
Our results indicated that resistance to imidacloprid in the cotton aphid might be associated with an increase in cytochrome P450monooxygenase and carboxylesterase. The amino acid substitution (R81T) was the first time found in imidacloprid-resistant cotton aphids in this study, and the R81T was proven to significantly reduce the affinity between acetylcholine receptors and imidacloprid. Therefore, the R81T mutation led to the generation of high-level resistance in cotton aphid to imidacloprid directly.
In summary, the risk of high-level imidacloprid-resistance in cotton aphid was determined in this study through laboratory selection. Studies of the resistance mechanisms confirmed that the mutation of target sites was the main reason for the high-level resistance. In addition, the increase of P450monooxygenase and carboxylesterase activity also played a role in the resistance to imidacloprid. Obviously these research results are significant for resistance management.
1、抗吡虫啉棉蚜品系的室内筛选及抗性风险评估
以杀死棉蚜群体60%-70%的剂量对敏感品系棉蚜持续筛选60代后,该品系棉蚜对吡虫啉的抗性达72.8倍,已经产生了高水平的吡虫啉抗性。该棉蚜品系从F0代筛选至F54代,抗性发展趋势较为平稳,抗性增加至47.0倍,达中等抗性水平；但由F54代筛选至F57代,抗性迅速由47.0倍增长至69.5倍,出现抗性突增期；由F57至F60抗性仍有小幅升高,但其发展又趋于缓慢,证明棉蚜对吡虫啉抗性发展趋势呈偏“S”型曲线。该抗性品系对烯啶虫胺(16.0倍)、啶虫脒(12.9倍)、噻虫嗪(11.6倍)、噻虫胺(9.84倍)、呋虫胺(9.50倍)、丁硫克百威(8.38倍)、高效氯氟氰菊酯(6.17倍)、氧乐果(6.13倍)和毒死蜱(5.10倍)均产生了明显的的交互抗性,但对哒螨灵和吡蚜酮的交互抗性水平较低(分别为2.28倍和4.52倍)。吡虫啉抗性和敏感品系生物学特性研究发现,RF60的蜜露分泌量、体重、若蚜存活率、内禀增长率和周限增长率均有所下降,特别是净生殖率,仅为敏感品系的47.7%,且世代周期延长了1.4天左右,相对适合度下降为0.71。
尽管吡虫啉使用中前期棉蚜对其抗性发展比较缓慢,但连续大量使用仍会导致抗性突增,因此尚存在产生高水平抗性的风险。交互抗性问题能够显著影响吡虫啉和大部分常规药剂特别是新烟碱类药剂的防效,在抗性治理中,仅有少数杀虫剂能够作为替代药剂使用。吡虫啉在棉蚜种群上会产生抗性代价,令其生长、发育和繁殖方面均受到一定程度的影响,从而使抗性品系群体增长受到抑制。
2、棉蚜对吡虫啉抗性的生化机理研究
以室内选育的吡虫啉抗性品系(抗性达72.8倍)和敏感品系棉蚜为材料,分别测定了四种解毒酶抑制剂对毗虫啉的增效作用,并且比较了两个品系棉蚜的解毒酶活性。其中SV1、DEM在棉蚜抗吡虫啉品系和敏感品系中均没有表现出明显的增效作用；而TPP和PBO则对吡虫啉起到了明显的增效作用,且在抗性品系中的增效作用显著高于在敏感品系中的增效作用；其中PBO的增效作用最为明显,在抗性品系中的增效比达到了2.97。酶活性测定结果表明,抗吡虫啉棉蚜品系的羧酸酯酶和乙酰胆碱酯酶比活力均高于敏感品系,尤其以羧酸酯酶比活力的提高最明显,而谷胱甘肽-S-转移酶的变化却并不显著。这些结果表明：多功能氧化酶和羧酸酯酶在棉蚜对吡虫啉产生抗性的过程中起到了重要的作用,而乙酰胆碱酯酶也起到了一定的辅助作用。
3、棉蚜对吡虫啉抗性的分子机理研究
以吡虫啉抗性品系和敏感品系棉蚜为材料,分别克隆了一个羧酸酯酶基因,两个P450单加氧酶六家族基因,五个乙酰胆碱受体α亚基和一个β亚基的cDNA序列,所有基因序列经同源序列比对后证实分别为棉蚜各功能基因。抗性和敏感品系棉蚜的羧酸酯酶及P450单加氧酶基因序列比对后并未发现抗性相关突变,但进一步的荧光定量分析发现,CYP6CY3-1基因在抗性品系棉蚜体内过量表达了5.66倍,羧酸酯酶基因过量表达了1.24倍,仅CYP6CY3-2基因的表达量未出现明显变化(1.03倍)。本研究得到的Agα2与Aga4亚基基因序列与NCBI上已登录的棉蚜乙酰胆碱受体α2和β4亚基cDNA序列相比更加完整,包含了翻译氨基酸序列所需的完整开放阅读框。比对各亚基氨基酸序列后发现,在抗性品系棉蚜Agβ1亚基上存在单一的位点突变R81T。
羧酸酯酶与P450单加氧酶基因的过量表达进一步证实了这两个解毒酶系在棉蚜对吡虫啉的抗性产生中起到了重要的作用。而本研究在抗吡虫啉棉蚜中首次发现的R81T氨基酸取代已被证实能够显著降低乙酰胆碱受体与吡虫啉的亲和力,因此,R81T突变直接导致了棉蚜对吡虫啉高水平抗性的产生。
综上所述,本研究通过室内选育明确了棉蚜对吡虫啉的高水平抗性风险,并通过抗性机理分析确定了靶标位点突变是棉蚜对吡虫啉产生高水平抗性的主要原因,同时P450单加氧酶和酯酶活力的升高也是棉蚜对吡虫啉产生抗性的机理之一。显然,本研究结果对建立田间抗性分子监测手段,制定合理的抗性治理策略,延缓田间棉蚜抗药性的发展具有重要指导意义。
The cotton aphid, Aphis gossypii (Glover), is one of the worldwide pests on cotton. Because of the short generation time and the high fecundity of cotton aphid, coupled with the irrational use of pesticides in field, resistance of cotton aphid is complex. So far, serious resistance of A. gossypii to conventional insecticides has resulted in many problems in controlling of this pest in China. Since the early1990s, as the first commercialization product of neonicotinoid insecticides, imidacloprid was extensively used and had become the dominated pesticide to control cotton aphid. To delay the resistance to imidacloprid and prolong its service life in the field, the risk of high level resistance to imidacloprid was studied systematically with the laboratory selected strain. With selected resistant strain and susceptible strain, the biochemical and molecular mechanisms for the resistance were also analyzed. The results are as follows:
1. The selection of imidacloprid-resistant strain of A. gossypii and the research of cross-resistance
The resistance level of A. gossypii to imidacloprid reached to72.8-fold after selection of60generations with the pressure to kill60%to70%individuals of the population. From Fo to F54, the resistance of A. gossypii to imidacloprid developed slowly in the initial and middle stage of resistance selection. However, there was a sudden increase in F57, and the resistance ratio suddenly increased from47.0-fold to69.5-fold. By F57to F60, the resistance was elevated slightly. It proved that the development of resistance to imidacloprid of cotton aphid also showed "S" shaped curve similarly. The cross-resistance phenomena of RF60to nitenpyram (16.0-fold), acetamiprid (12.9-fold), buprofezin (11.6-fold), clothianidin (9.84-fold), dinotefuran (9.50-fold), carbosulfan (8.38-fold), lambda-cyhalothrin (6.17-fold), omethoate (6.13-fold), and chlorpyrifos (5.10-fold) were obviously, while the cross-resistance to pymetrozine and pyridaben at a low level (2.28-and4.52-fold, respectively). Biological research of imidacloprid between resistant and susceptible strains found that the honeydew excretion, boby weight, nymphal survival rate, net reproductive rate and intrinsic rate of natural had declined. In particular, the net reproductive rate of RF60was only47.7%compared with the susceptible strain. At the same time, the mean generation time extended about1.4days and the relative fitness decreased to0.71.
The results of this study showed that the development of resistance to imidacloprid was relatively slow in the early stage, but the resistance of A. gossypii could increase suddenly after persistent imidacloprid selection, so the risk of high-level resistance still existed. Cross-resistance could significantly affect the effect of imidacloprid and most conventional insecticides, and only a small number of novel insecticides could use to be alternative pesticides. Imidacloprid conferred the fitness cost in A. gossypii, affecting its growth, development and reproduction, so the population growth of resistant strain could be inhibited.
2. Studies of biochemical mechanisms of imidacloprid resistance in A. gossypii
The biochemical mechanisms of imdacloprid resistance in A. gossypii were studied by testing the synergism of four enzyme inhibitors and the activity of related enzyme in resistant and susceptible strain of A. gossypii. The results showed that the synergism of PBO and TPP was singnificantly higher in the resistant strain than in the susceptible strain, especially when the synergism ratio of PBO was2.97. The synergism of SV1was relatively low, but DEM did not show any synergism on imidacloprid in both strains. Detoxifieation enzyme activity test in two strains showed that the activity of carboxylesterase (CarE) in resistant strain is much higher than the susceptible strain. However the activity of glutathione-S-transferase (GST) was similar in both strains. Furthermore, the activity of acetylcholinesterase (AChE) in resistant strain was a little higher than the susceptible strain. Thus, it was concluded that the enhanced carboxylesterase and cytochrome P450-monooxygenases detoxifieation might contribute to the high-level of imidacloprid resistance in A.gossypii. Acetylcholinesterase had also played a supporting role in the resistance.
3. Studies of molecular mechanisms of imidacloprid resistance in A. gossypii
We successfully cloned one carboxylesterase gene, two P450monooxygenase genes, five acetylcholine receptor a subunit and one β subunit from both resistant and susceptible strains. All genes we got were confirmed to belong to cotton aphid after homologous sequence alignment respectively. No mutation was found in the carboxylesterase and P450monooxygenase genes in the resistant strain, but the fluorescent quantitative analysis of three genes found that CYP6CY3-1and carboxylesterase gene overexpressed5.66-fold and 1.24-fold in resistant strain compared with the susceptible strain. Nevertheless, expression of CYP6CY3-2gene did not change obviously (only1.03-fold). The Aga2and Aga4subunit gene cDNA sequence we cloned in this study which contained the complete open reading frame were more complete than the A. gossypii nAChR a2and a4subunits cDNA sequences logged on NCBI previously. Comparison of the amino acid sequence of every subunit between the resistant and susceptible strains, a single mutation (R81T) in Agβ1subunit was observed from the resistant strain.
Our results indicated that resistance to imidacloprid in the cotton aphid might be associated with an increase in cytochrome P450monooxygenase and carboxylesterase. The amino acid substitution (R81T) was the first time found in imidacloprid-resistant cotton aphids in this study, and the R81T was proven to significantly reduce the affinity between acetylcholine receptors and imidacloprid. Therefore, the R81T mutation led to the generation of high-level resistance in cotton aphid to imidacloprid directly.
In summary, the risk of high-level imidacloprid-resistance in cotton aphid was determined in this study through laboratory selection. Studies of the resistance mechanisms confirmed that the mutation of target sites was the main reason for the high-level resistance. In addition, the increase of P450monooxygenase and carboxylesterase activity also played a role in the resistance to imidacloprid. Obviously these research results are significant for resistance management.
引文
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