小菜蛾对多杀霉素和氯虫苯甲酰胺抗性的特征及机理
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摘要
小菜蛾Plutella xylostella (Lepidoptera:Yponomeutidae)属于鳞翅目菜蛾科,是世界范围内的一种重要害虫,每年造成的经济损失达40～50亿美元。小菜蛾寄主植物种类达40多种,主要为害十字花科蔬菜。由于生活周期短、繁殖能力强、世代重叠严重及田间不合理用药,使小菜蛾几乎对所有的防控用药(至少涉及84种杀虫剂)产生了不同程度的抗性。小菜蛾抗药性问题给十字花科蔬菜生产带来严重威胁和巨大挑战,抗性治理形势严峻。
多杀霉素是一种作用于烟碱型乙酰胆碱受体的抗生素类药剂,氯虫苯甲酰胺是作用于昆虫鱼尼丁受体的二酰胺类杀虫剂。这两种新型杀虫剂均对鳞翅目等靶标害虫具有优异的防治效果,并具备良好的环境安全性。本文系统研究了小菜蛾对多杀霉素和氯虫苯甲酰胺抗性的特征(包括抗性筛选、抗性稳定性、交互抗性谱及抗性遗传方式等)以及抗性机理,研究结果对于了解小菜蛾对新型杀虫剂抗性演化的分子机理及制订抗性治理对策具有重要意义。
1.小菜蛾对多杀霉素抗性特征的分析
利用浸叶法对小菜蛾SZ-Spin56品系进行26代连续筛选,获得多杀霉素高抗品系SZ-Spin83。与室内敏感品系Roth和室内对照品系SZ相比,SZ-Spin83品系对多杀霉素的抗性分别达到10,000倍和4,000倍。对该高抗品系用多杀霉素继续筛选或停止筛选,抗性均无显著变化,表明小菜蛾SZ-Spin83品系对多杀霉素抗性稳定(抗性基因已经纯合)。交互抗性测定结果显示,SZ-Spin83品系对阿维菌素和乙基多杀菌素存在高水平交互抗性(交互抗性分别为468倍和2396倍),对茚虫威、高效氯氰菊酯、氟虫腈、溴虫腈、巴丹、啶虫隆、丁醚脲、虫酰肼、氰氟虫腙和氯虫苯甲酰胺均没有明显交互抗性。抗性遗传方式分析表明,小菜蛾SZ-Spin83品系对多杀霉素的抗性受位于常染色体、共显性遗传的两个或两个以上基因控制。
2.小菜蛾对多杀霉素的抗性机制
三种解毒酶抑制剂(PBO、DEM和DEF)在室内敏感品系Roth、室内对照品系SZ和抗性品系SZ-Spin83中对多杀霉素均不存在显著的增效作用(增效比<2倍)。SZ-Spin83品系多功能氧化酶、酯酶和谷胱甘肽S-转移酶活性相对于敏感品系Roth有所升高(<2倍),但与其初始种群SZ品系水平相当(<1.2倍)。因此,代谢酶介导的解毒作用与SZ-Spin83品系对多杀霉素的抗性关系不大,其主导抗性机理可能为靶标变异。通过RT-PCR和RACE技术克隆了小菜蛾烟碱型乙酰胆碱受体Pxa2基因,该基因在多杀霉素抗性品系和敏感品系间不存在保守的氨基酸突变位点,并且该基因mRNA表达水平在抗性品系SZ-Spin83与其初始种群SZ之间没有显著差异。另外,对已报道的多杀霉素抗性基因Pxa6进行了研究。通过对敏感品系Roth55个和抗性品系SZ-Spin8358个阳性克隆的测序,检测到Pxa6亚基的6种转录本,其中3种类型为本研究首次发现。Pxa6基因在抗性和敏感品系间不存在保守的氨基酸突变位点,同时SZ-Spin83品系与其初始种群SZ相比,Pxa6的mRNA表达量没有差异。因此,我们认为小菜蛾对多杀霉素的抗性机理以靶标抗性为主,但与烟碱型乙酰胆碱受体a6亚基(Pxa6)和α2亚基(Pxa2)无关,或为nAChR其它亚基突变所致,亦不排除其它靶标基因参与抗性演化的可能性。
3.小菜蛾对氯虫苯甲酰胺的敏感毒力基线和抗性监测
利用浸叶法测定了2007-2009年间采集自我国11个地区的16个田间种群和7个室内饲养品系对氯虫苯甲酰胺的敏感性。16个田间种群的LC50值介于0.221-1.104mg/L之间,敏感性波动幅度在5倍以内；7个室内饲养品系基于LC50值的敏感性波动范围小于10倍。同时,利用16个田间种群的毒理学数据确定了15mg/L的诊断剂量,7个室内品系和5个田间小菜蛾种群在该剂量下的平均死亡率为99.75%(98%-100%)。该结果表明我国小菜蛾田间种群对尚未用于蔬菜害虫防控的氯虫苯甲酰胺具有较高的敏感性。本研究建立的小菜蛾对氯虫苯甲酰胺敏感毒力基线对于抗性监测与预警具有重要价值。
在2010-2011年间,监测了我国12个地点采集的20个小菜蛾种群对氯虫苯甲酰胺敏感性的变化。结果表明,采自北部地区的14个田间种群对氯虫苯甲酰胺仍然敏感,LC50值在0.226-0.71mg/L,波动范围仅3倍。采自广东省的6个田间种群对该药剂的抗性水平差异很大,LC50值在0.343-256.2mg/L之间,波动幅度达770倍。与敏感品系Roth相比,广东珠海(ZH)和增城(ZC)种群分别具有150倍和2,140倍的抗性。该结果表明,必须合理使用氯虫苯甲酰胺防治小菜蛾以延缓抗性；同时,加强小菜蛾对氯虫苯甲酰胺抗性的监测,在高抗地区必须停止使用氯虫苯甲酰胺。
4.小菜蛾对氯虫苯甲酰胺抗性特征的分析
2011年秋季采集的对氯虫苯甲酰胺具有抗性的PY、ZH和ZC种群(F3测定抗性倍数为18-1,150倍),对氟虫双酰胺表现出相近的抗性水平(15-800倍),说明二酰胺类的两种药剂之间存在着交互抗性。药剂选择压力移除以后,ZC种群对氯虫苯甲酰胺的抗性表现出不稳定性,由2,040倍下降至25倍仅用6代时间。抗性遗传方式分析表明,小菜蛾ZC高抗种群对氯虫苯甲酰胺的抗性为常染色体、不完全隐性遗传。由ZC分离一部分建立ZC-R品系,对其进行的增效实验表明PBO、DEF和DEM对氯虫苯甲酰胺毒力具微弱的增效作用(增效比为2.2～2.9),表明代谢酶介导的解毒作用在氯虫苯甲酰胺的抗性形成中作用有限,靶标抗性可能为小菜蛾对氯虫苯甲酰胺抗性的主要机理。
5.小菜蛾鱼尼丁受体的变异与氯虫苯甲酰胺抗性的关系
昆虫鱼尼丁受体是二酰胺类杀虫剂的作用靶标。我们克隆了小菜蛾的鱼尼丁受体基因(PxRyR)cDNA全长,从而为研究靶标抗性奠定基础。PxRyR由15,495bp的ORF框、267bp的5'-UTR区和351bp的3'-UTR区组成,编码5164个氨基酸,分子量约为583.7KDao PxRyR具备鱼尼丁受体的普遍特征：保守的羧基端结构,此区域含6个跨膜结构域可形成功能性的Ca2+通道,胞浆区为大的氧基端结构域。PxRyR与昆虫RyR在氨基酸水平上的一致性很高,为78%-80%. PxRyR全长cDNA存在10个缺失多态性位点,说明单个PxRyR基因可以产生多种类型的转录本。同时,PxRyR基因在小菜蛾卵期、幼虫期和成虫期mRNA表达量分别是蛹期的1.36、2.47和1.40倍,幼虫期表达量显著高于蛹期；在幼虫不同组织部位中的表达量相对一致,没有显著差异。
分别以氯虫苯甲酰胺抗性小菜蛾品系ZC-R和室内敏感品系Roth为材料,利用PxRyR碱基13,349位存在的保守替换位点作为抗性、敏感个体的分子标记,通过遗传分析发现氯虫苯甲酰胺抗性与PxRyR基因连锁。对抗性和敏感品系PxRyR基因羧基端1691个氨基酸序列进行了比对分析,发现抗性品系ZC-R在氨基酸4790(I到K)和4946(G到E)位存在50%和41%的突变频率,遗传分析结果表明G4946E点突变与氯虫苯甲酰胺抗性具有相关性。以β-actin和EF-1α基因为内参的定量PCR分析表明,ZC-R品系PxRyR基因mRNA表达量仅为室内敏感品系Roth和室内对照品系SZ的41-46%。上述研究结果表明,小菜蛾对氯虫苯甲酰胺的抗性与鱼尼丁受体基因连锁,该基因可能通过氨基酸点突变、mRNA表达下调或两者协同作用导致高水平抗性的形成。
The diamondback moth, Plutella xylostella (L.)(Lepidoptera:Plutellidae), is one of the most damaging, cosmopolitan economic pests of cruciferous vegetables, especially in the tropical and subtropical areas. A conservative estimate of total costs associated with its management is about US$4-5billion every year. Its short generation time, high fecundity, and extensive selection pressure in the field, have resulted in rapid evolution of resistance to various classes of insecticides (including84kinds of active ingredients). P. xylostella has become one of the most difficult pests to control in cruciferous vegetables.
Spinosad is the first commercialized member of spinosyn class of insecticides, which primarily attacks the nicotinic acetylcholine receptor. Chlorantraniliprole is the first commercial insecticide from a novel class of chemistry, the anthranilic diamides, which selectively binds to insect ryanodine receptors (RyRs). Both insecticides have high insecticidal potency and good mammalian safety. In the present study, we investigated the characteristics (including resistance selection, stability, cross-resistance and mode of inheritance) and mechanisms for resistance to spinosad and chlorantraniliprole in P. xylostella. The information from our research will be valuable in understanding resistance mechanisms at molecular level and in developing rational resistance management strategies.
1. Characterization of spinosad resistance in the SZ-Spin83strain of P. xylostella
The SZ-Spin83strain developed4,000-fold and10,000-fold resistance to spinosad under laboratory selection when compared with SZ (the progenitor strain of SZ-Spin83) and Roth (the susceptible strain) respectively. With or without continuous selection by spinosad, resistance in SZ-Spin83was stable with no significant change. Compared with the SZ strain, the SZ-Spin83strain showed high levels of cross-resistance to abamectin (468-fold) and spinetoram (2396-fold), no obvious cross-resistance to indoxacarb, beta-cypermethrin, fipronil, chlorfenapyr, cartap, chlorfluazuron, diafenthiuron, tebufenozide, metaflumizone and chlorantraniliprole. Inheritance analysis results showed that spinosad resistance in SZ-Spin83strain of P. xylostella was autosomal, co-dominant, and polygenic.
2. Mechanisms of spinosad resistance in the SZ-Spin83strain of P. xylostella
The synergistic effects of PBO, DEM and DEF on spinosad were determined in the Roth, SZ and SZ-Spin83strains, and the results showed that the three inhibitors did not significantly synergize spinosad against the three strains (SR<2-fold). In order to evaluate the role of metabolic detoxification mechanisms in spinosad resistance, the activities of P450monooxygenases, esterases and glutathione S-transferases were measured in the three strains. Metabolic enzyme activities in SZ-Spin83were0.68～1.81-fold compared with the Roth strain, and there was no significant difference in activities between SZ-Spin83and SZ strains. Enzyme activity results were consistent with those of the synergism experiments, supporting that metabolic detoxification was not involved in spinosad resistance in SZ-Spin83, and taget-site resistance may be the the major resistance mechanism. To investigate possible target site resistance mechanisms, a nAChR subunit gene (Pxa2) was cloned and characterized from SZ-Spin83and Roth strains. There was no conservative difference at amino acid level among the Roth, SZ and SZ-Spin83strains. Pxa2mRNA expression, quantified by real-time PCR, was no significantly different between SZ-Spin83and SZ strains. Recent studies reported that Pxa6gene mutation was associated with spinosad resistance in a strain of P. xylostella. To determine if SZ-Spin83resistance was due to the same mutation,55from Roth and58from SZ-Spin83of Pxa.6transcripts were sequenced and analyzed. Six isoforms of Pxa6were detected, three of which are novel isoforms. However, our results showed no evidence of a selective sweep associated with the Pxa6in the resistant SZ-Spin83strain, and the mRNA expression levels were similar among the resistant and susceptible strains. Our work suggested neither Pxa2nor Pxa6was associated with spinosad resistance in SZ-Spin83. It is suggested that other nAChR subunits or other receptor genes other than nAChR could be responsible for spinosad resistance in SZ-Spin83.
3. Baseline susceptibility and resistance monitoring of P. xylostella to chlorantraniliprole
The susceptibility of16field populations and seven laboratory maintained strains of P. xylostella to chlorantraniliprole were determined through leaf dip bioassay during2008-2009. The susceptibility variation among16field populations was low (5-fold), with median lethal concentrations (LC50values) varying from0.221to1.104mg/liter. However, wider ranges of variation in LC50s (10-fold) were observed among seven laboratory strains. A discriminating concentration (15mg/liter) was calibrated from pooled toxicological data of the16field populations, seven laboratory strains and five field populations showed an average mortality of99.75%(from98to100%). The results indicated field P. xylostella populations were sensitive to this chemical, will also be useful in resistance monitoring and early warning.
20field populations of P. xylostella sampled in2010-2011from China were tested with laboratory bioassays to determine if susceptibility to chlorantraniliprole had changed in the field. The LC50s was about three fold (from0.226to0.71mg/liter) among the14field populations from northern China, but reached as high as770-fold (from0.343to265.2mg/liter) among the six field populations from southern China (Guangdong Province). Among the six populations, very high levels of resistance were detected in Zhuhai (ZH)(150-fold) and Zengcheng (ZC)(2140-fold). The present work suggests that we should rational use chlorantraniliprole, inorder to extend the useful life of this compound. Meanwhile, we urge to stop use of chlorantraniliprole in somewhere if high level of resistance had evolved in field.
4. Characterization of field-evolved resistance to chlorantraniliprole in P. xylostella
Three field populations of P. xylostella collected from southern China in2011showed parallel resistance levels to chlorantraniliprole (from18-to1150-fold) and flubendiamide (from15-fold to800-fold), indicating strong cross-resistance between these two diamide insecticides. In the absence of selection pressure, resistance to chlorantraniliprole in ZC population declined from2040-fold (Gi) to25-fold (G7). Genetic analysis showed that chlorantraniliprole resistance in the ZC population was autosomal and incompletely recessive. The ZC-R strain (derived from ZC) had670-fold resistance to chlorantraniliprole. Synergist bioassays performed on ZC-R showed chlorantraniliprole toxicity was synergized by PBO, DEM and DEF at low levels. This work showed metabolic detoxification was involved in chlorantraniliprole resistance in the ZC-R strain to some extent, and target-site resistance may be the major mechanism.
5. Relationship between variations of the ryanodine receptor of P. xylostella and chlorantraniliprole resistance
The full-length cDNA of a ryanodine receptor gene (PxRyR) was cloned and characterized from P. xylostella by RNA-Seq, RT-PCR and RACE technologies. The cDNAs of PxRyR contain a15,495-bp open reading frame,267-bp5'untranslated region (UTR) and a3'-UTR of351-bp. The predicted mature protein consists of5164amino acids with a predicted molecular weight of583.7-kDa. PxRyR shares common structural features with known RyRs:the well-conserved COOH-terminal domain, which forms a functional Ca2+channel, and a large hydrophilic NH2-terminal domain. PxRyR shows a high level of amino acid sequence identity (78-80%) to the insect RyR isoforms. Ten deletion polymorphism sites were detected in PxRyR cDNAs, suggesting a single PxRyR can produce many polymorphic transcripts. Although the highest mRNA expression level was observed in larva and the lowest in pupa, there was a relatively stable expression during the developmental period from egg to adult. The relative mRNA expression levels of PxRyR were similar among the head, thorax, and abdomen of the fourth-instar larva body.
We used the A/C polymorphism at the site13,349bp as a molecular marker of PxRyR cDNA to test the linkage between PxRyR locus and chlorantraniliprole resistance in the ZC-R strain. Backcross analysis results showed that chlorantraniliprole resistance was genetically linked with PxRyR in ZC-R. We sequenced a cDNA fragment encoding1691amino acids in the COOH-terminal domain of PxRyR. Two point mutations (I4790K, G4946E) were existed in resistant ZC-R strain, but only G4946E was associated with resistance to some extent. PxRyR mRNA expression levels in the resistant ZC-R strain, quantified by real-time PCR, was reduced to41～46%of the Roth and SZ strains. It was concluded that chlorantraniliprole resistance was linked with the PxRyR locus, and both amino acid mutations and reduced mRNA expression of PxRyR could be involved in resistance.
多杀霉素是一种作用于烟碱型乙酰胆碱受体的抗生素类药剂,氯虫苯甲酰胺是作用于昆虫鱼尼丁受体的二酰胺类杀虫剂。这两种新型杀虫剂均对鳞翅目等靶标害虫具有优异的防治效果,并具备良好的环境安全性。本文系统研究了小菜蛾对多杀霉素和氯虫苯甲酰胺抗性的特征(包括抗性筛选、抗性稳定性、交互抗性谱及抗性遗传方式等)以及抗性机理,研究结果对于了解小菜蛾对新型杀虫剂抗性演化的分子机理及制订抗性治理对策具有重要意义。
1.小菜蛾对多杀霉素抗性特征的分析
利用浸叶法对小菜蛾SZ-Spin56品系进行26代连续筛选,获得多杀霉素高抗品系SZ-Spin83。与室内敏感品系Roth和室内对照品系SZ相比,SZ-Spin83品系对多杀霉素的抗性分别达到10,000倍和4,000倍。对该高抗品系用多杀霉素继续筛选或停止筛选,抗性均无显著变化,表明小菜蛾SZ-Spin83品系对多杀霉素抗性稳定(抗性基因已经纯合)。交互抗性测定结果显示,SZ-Spin83品系对阿维菌素和乙基多杀菌素存在高水平交互抗性(交互抗性分别为468倍和2396倍),对茚虫威、高效氯氰菊酯、氟虫腈、溴虫腈、巴丹、啶虫隆、丁醚脲、虫酰肼、氰氟虫腙和氯虫苯甲酰胺均没有明显交互抗性。抗性遗传方式分析表明,小菜蛾SZ-Spin83品系对多杀霉素的抗性受位于常染色体、共显性遗传的两个或两个以上基因控制。
2.小菜蛾对多杀霉素的抗性机制
三种解毒酶抑制剂(PBO、DEM和DEF)在室内敏感品系Roth、室内对照品系SZ和抗性品系SZ-Spin83中对多杀霉素均不存在显著的增效作用(增效比<2倍)。SZ-Spin83品系多功能氧化酶、酯酶和谷胱甘肽S-转移酶活性相对于敏感品系Roth有所升高(<2倍),但与其初始种群SZ品系水平相当(<1.2倍)。因此,代谢酶介导的解毒作用与SZ-Spin83品系对多杀霉素的抗性关系不大,其主导抗性机理可能为靶标变异。通过RT-PCR和RACE技术克隆了小菜蛾烟碱型乙酰胆碱受体Pxa2基因,该基因在多杀霉素抗性品系和敏感品系间不存在保守的氨基酸突变位点,并且该基因mRNA表达水平在抗性品系SZ-Spin83与其初始种群SZ之间没有显著差异。另外,对已报道的多杀霉素抗性基因Pxa6进行了研究。通过对敏感品系Roth55个和抗性品系SZ-Spin8358个阳性克隆的测序,检测到Pxa6亚基的6种转录本,其中3种类型为本研究首次发现。Pxa6基因在抗性和敏感品系间不存在保守的氨基酸突变位点,同时SZ-Spin83品系与其初始种群SZ相比,Pxa6的mRNA表达量没有差异。因此,我们认为小菜蛾对多杀霉素的抗性机理以靶标抗性为主,但与烟碱型乙酰胆碱受体a6亚基(Pxa6)和α2亚基(Pxa2)无关,或为nAChR其它亚基突变所致,亦不排除其它靶标基因参与抗性演化的可能性。
3.小菜蛾对氯虫苯甲酰胺的敏感毒力基线和抗性监测
利用浸叶法测定了2007-2009年间采集自我国11个地区的16个田间种群和7个室内饲养品系对氯虫苯甲酰胺的敏感性。16个田间种群的LC50值介于0.221-1.104mg/L之间,敏感性波动幅度在5倍以内；7个室内饲养品系基于LC50值的敏感性波动范围小于10倍。同时,利用16个田间种群的毒理学数据确定了15mg/L的诊断剂量,7个室内品系和5个田间小菜蛾种群在该剂量下的平均死亡率为99.75%(98%-100%)。该结果表明我国小菜蛾田间种群对尚未用于蔬菜害虫防控的氯虫苯甲酰胺具有较高的敏感性。本研究建立的小菜蛾对氯虫苯甲酰胺敏感毒力基线对于抗性监测与预警具有重要价值。
在2010-2011年间,监测了我国12个地点采集的20个小菜蛾种群对氯虫苯甲酰胺敏感性的变化。结果表明,采自北部地区的14个田间种群对氯虫苯甲酰胺仍然敏感,LC50值在0.226-0.71mg/L,波动范围仅3倍。采自广东省的6个田间种群对该药剂的抗性水平差异很大,LC50值在0.343-256.2mg/L之间,波动幅度达770倍。与敏感品系Roth相比,广东珠海(ZH)和增城(ZC)种群分别具有150倍和2,140倍的抗性。该结果表明,必须合理使用氯虫苯甲酰胺防治小菜蛾以延缓抗性；同时,加强小菜蛾对氯虫苯甲酰胺抗性的监测,在高抗地区必须停止使用氯虫苯甲酰胺。
4.小菜蛾对氯虫苯甲酰胺抗性特征的分析
2011年秋季采集的对氯虫苯甲酰胺具有抗性的PY、ZH和ZC种群(F3测定抗性倍数为18-1,150倍),对氟虫双酰胺表现出相近的抗性水平(15-800倍),说明二酰胺类的两种药剂之间存在着交互抗性。药剂选择压力移除以后,ZC种群对氯虫苯甲酰胺的抗性表现出不稳定性,由2,040倍下降至25倍仅用6代时间。抗性遗传方式分析表明,小菜蛾ZC高抗种群对氯虫苯甲酰胺的抗性为常染色体、不完全隐性遗传。由ZC分离一部分建立ZC-R品系,对其进行的增效实验表明PBO、DEF和DEM对氯虫苯甲酰胺毒力具微弱的增效作用(增效比为2.2～2.9),表明代谢酶介导的解毒作用在氯虫苯甲酰胺的抗性形成中作用有限,靶标抗性可能为小菜蛾对氯虫苯甲酰胺抗性的主要机理。
5.小菜蛾鱼尼丁受体的变异与氯虫苯甲酰胺抗性的关系
昆虫鱼尼丁受体是二酰胺类杀虫剂的作用靶标。我们克隆了小菜蛾的鱼尼丁受体基因(PxRyR)cDNA全长,从而为研究靶标抗性奠定基础。PxRyR由15,495bp的ORF框、267bp的5'-UTR区和351bp的3'-UTR区组成,编码5164个氨基酸,分子量约为583.7KDao PxRyR具备鱼尼丁受体的普遍特征：保守的羧基端结构,此区域含6个跨膜结构域可形成功能性的Ca2+通道,胞浆区为大的氧基端结构域。PxRyR与昆虫RyR在氨基酸水平上的一致性很高,为78%-80%. PxRyR全长cDNA存在10个缺失多态性位点,说明单个PxRyR基因可以产生多种类型的转录本。同时,PxRyR基因在小菜蛾卵期、幼虫期和成虫期mRNA表达量分别是蛹期的1.36、2.47和1.40倍,幼虫期表达量显著高于蛹期；在幼虫不同组织部位中的表达量相对一致,没有显著差异。
分别以氯虫苯甲酰胺抗性小菜蛾品系ZC-R和室内敏感品系Roth为材料,利用PxRyR碱基13,349位存在的保守替换位点作为抗性、敏感个体的分子标记,通过遗传分析发现氯虫苯甲酰胺抗性与PxRyR基因连锁。对抗性和敏感品系PxRyR基因羧基端1691个氨基酸序列进行了比对分析,发现抗性品系ZC-R在氨基酸4790(I到K)和4946(G到E)位存在50%和41%的突变频率,遗传分析结果表明G4946E点突变与氯虫苯甲酰胺抗性具有相关性。以β-actin和EF-1α基因为内参的定量PCR分析表明,ZC-R品系PxRyR基因mRNA表达量仅为室内敏感品系Roth和室内对照品系SZ的41-46%。上述研究结果表明,小菜蛾对氯虫苯甲酰胺的抗性与鱼尼丁受体基因连锁,该基因可能通过氨基酸点突变、mRNA表达下调或两者协同作用导致高水平抗性的形成。
The diamondback moth, Plutella xylostella (L.)(Lepidoptera:Plutellidae), is one of the most damaging, cosmopolitan economic pests of cruciferous vegetables, especially in the tropical and subtropical areas. A conservative estimate of total costs associated with its management is about US$4-5billion every year. Its short generation time, high fecundity, and extensive selection pressure in the field, have resulted in rapid evolution of resistance to various classes of insecticides (including84kinds of active ingredients). P. xylostella has become one of the most difficult pests to control in cruciferous vegetables.
Spinosad is the first commercialized member of spinosyn class of insecticides, which primarily attacks the nicotinic acetylcholine receptor. Chlorantraniliprole is the first commercial insecticide from a novel class of chemistry, the anthranilic diamides, which selectively binds to insect ryanodine receptors (RyRs). Both insecticides have high insecticidal potency and good mammalian safety. In the present study, we investigated the characteristics (including resistance selection, stability, cross-resistance and mode of inheritance) and mechanisms for resistance to spinosad and chlorantraniliprole in P. xylostella. The information from our research will be valuable in understanding resistance mechanisms at molecular level and in developing rational resistance management strategies.
1. Characterization of spinosad resistance in the SZ-Spin83strain of P. xylostella
The SZ-Spin83strain developed4,000-fold and10,000-fold resistance to spinosad under laboratory selection when compared with SZ (the progenitor strain of SZ-Spin83) and Roth (the susceptible strain) respectively. With or without continuous selection by spinosad, resistance in SZ-Spin83was stable with no significant change. Compared with the SZ strain, the SZ-Spin83strain showed high levels of cross-resistance to abamectin (468-fold) and spinetoram (2396-fold), no obvious cross-resistance to indoxacarb, beta-cypermethrin, fipronil, chlorfenapyr, cartap, chlorfluazuron, diafenthiuron, tebufenozide, metaflumizone and chlorantraniliprole. Inheritance analysis results showed that spinosad resistance in SZ-Spin83strain of P. xylostella was autosomal, co-dominant, and polygenic.
2. Mechanisms of spinosad resistance in the SZ-Spin83strain of P. xylostella
The synergistic effects of PBO, DEM and DEF on spinosad were determined in the Roth, SZ and SZ-Spin83strains, and the results showed that the three inhibitors did not significantly synergize spinosad against the three strains (SR<2-fold). In order to evaluate the role of metabolic detoxification mechanisms in spinosad resistance, the activities of P450monooxygenases, esterases and glutathione S-transferases were measured in the three strains. Metabolic enzyme activities in SZ-Spin83were0.68～1.81-fold compared with the Roth strain, and there was no significant difference in activities between SZ-Spin83and SZ strains. Enzyme activity results were consistent with those of the synergism experiments, supporting that metabolic detoxification was not involved in spinosad resistance in SZ-Spin83, and taget-site resistance may be the the major resistance mechanism. To investigate possible target site resistance mechanisms, a nAChR subunit gene (Pxa2) was cloned and characterized from SZ-Spin83and Roth strains. There was no conservative difference at amino acid level among the Roth, SZ and SZ-Spin83strains. Pxa2mRNA expression, quantified by real-time PCR, was no significantly different between SZ-Spin83and SZ strains. Recent studies reported that Pxa6gene mutation was associated with spinosad resistance in a strain of P. xylostella. To determine if SZ-Spin83resistance was due to the same mutation,55from Roth and58from SZ-Spin83of Pxa.6transcripts were sequenced and analyzed. Six isoforms of Pxa6were detected, three of which are novel isoforms. However, our results showed no evidence of a selective sweep associated with the Pxa6in the resistant SZ-Spin83strain, and the mRNA expression levels were similar among the resistant and susceptible strains. Our work suggested neither Pxa2nor Pxa6was associated with spinosad resistance in SZ-Spin83. It is suggested that other nAChR subunits or other receptor genes other than nAChR could be responsible for spinosad resistance in SZ-Spin83.
3. Baseline susceptibility and resistance monitoring of P. xylostella to chlorantraniliprole
The susceptibility of16field populations and seven laboratory maintained strains of P. xylostella to chlorantraniliprole were determined through leaf dip bioassay during2008-2009. The susceptibility variation among16field populations was low (5-fold), with median lethal concentrations (LC50values) varying from0.221to1.104mg/liter. However, wider ranges of variation in LC50s (10-fold) were observed among seven laboratory strains. A discriminating concentration (15mg/liter) was calibrated from pooled toxicological data of the16field populations, seven laboratory strains and five field populations showed an average mortality of99.75%(from98to100%). The results indicated field P. xylostella populations were sensitive to this chemical, will also be useful in resistance monitoring and early warning.
20field populations of P. xylostella sampled in2010-2011from China were tested with laboratory bioassays to determine if susceptibility to chlorantraniliprole had changed in the field. The LC50s was about three fold (from0.226to0.71mg/liter) among the14field populations from northern China, but reached as high as770-fold (from0.343to265.2mg/liter) among the six field populations from southern China (Guangdong Province). Among the six populations, very high levels of resistance were detected in Zhuhai (ZH)(150-fold) and Zengcheng (ZC)(2140-fold). The present work suggests that we should rational use chlorantraniliprole, inorder to extend the useful life of this compound. Meanwhile, we urge to stop use of chlorantraniliprole in somewhere if high level of resistance had evolved in field.
4. Characterization of field-evolved resistance to chlorantraniliprole in P. xylostella
Three field populations of P. xylostella collected from southern China in2011showed parallel resistance levels to chlorantraniliprole (from18-to1150-fold) and flubendiamide (from15-fold to800-fold), indicating strong cross-resistance between these two diamide insecticides. In the absence of selection pressure, resistance to chlorantraniliprole in ZC population declined from2040-fold (Gi) to25-fold (G7). Genetic analysis showed that chlorantraniliprole resistance in the ZC population was autosomal and incompletely recessive. The ZC-R strain (derived from ZC) had670-fold resistance to chlorantraniliprole. Synergist bioassays performed on ZC-R showed chlorantraniliprole toxicity was synergized by PBO, DEM and DEF at low levels. This work showed metabolic detoxification was involved in chlorantraniliprole resistance in the ZC-R strain to some extent, and target-site resistance may be the major mechanism.
5. Relationship between variations of the ryanodine receptor of P. xylostella and chlorantraniliprole resistance
The full-length cDNA of a ryanodine receptor gene (PxRyR) was cloned and characterized from P. xylostella by RNA-Seq, RT-PCR and RACE technologies. The cDNAs of PxRyR contain a15,495-bp open reading frame,267-bp5'untranslated region (UTR) and a3'-UTR of351-bp. The predicted mature protein consists of5164amino acids with a predicted molecular weight of583.7-kDa. PxRyR shares common structural features with known RyRs:the well-conserved COOH-terminal domain, which forms a functional Ca2+channel, and a large hydrophilic NH2-terminal domain. PxRyR shows a high level of amino acid sequence identity (78-80%) to the insect RyR isoforms. Ten deletion polymorphism sites were detected in PxRyR cDNAs, suggesting a single PxRyR can produce many polymorphic transcripts. Although the highest mRNA expression level was observed in larva and the lowest in pupa, there was a relatively stable expression during the developmental period from egg to adult. The relative mRNA expression levels of PxRyR were similar among the head, thorax, and abdomen of the fourth-instar larva body.
We used the A/C polymorphism at the site13,349bp as a molecular marker of PxRyR cDNA to test the linkage between PxRyR locus and chlorantraniliprole resistance in the ZC-R strain. Backcross analysis results showed that chlorantraniliprole resistance was genetically linked with PxRyR in ZC-R. We sequenced a cDNA fragment encoding1691amino acids in the COOH-terminal domain of PxRyR. Two point mutations (I4790K, G4946E) were existed in resistant ZC-R strain, but only G4946E was associated with resistance to some extent. PxRyR mRNA expression levels in the resistant ZC-R strain, quantified by real-time PCR, was reduced to41～46%of the Roth and SZ strains. It was concluded that chlorantraniliprole resistance was linked with the PxRyR locus, and both amino acid mutations and reduced mRNA expression of PxRyR could be involved in resistance.
引文
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