苏云金杆菌Cry毒素对褐飞虱无毒原因分析及对褐飞虱有效新型Bt Cry毒素的改造
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摘要
苏云金杆菌（Bacillus thuringiensis, Bt），是目前应用最为广泛的微生物杀虫剂，在Bt所产生的多种杀虫毒素中，Cry毒素是当前研究最为深入且应用最为广泛的一种，cry基因也已经被广泛应用与转基因作物中，成为农业生产中防治鳞翅目、鞘翅目、双翅目、线虫等Bt Cry毒素靶标昆虫的一种有效的途径，从而减少了对环境有负作用的化学农药的使用。
然而，Cry毒素蛋白的杀虫谱仅局限于鳞翅目、鞘翅目、双翅目等特定靶标昆虫，对于半翅目刺吸式口器的蚜虫、飞虱、叶蝉等昆虫暂时还没有有效Cry毒素的报道。随着能够表达Cry毒素的转基因作物的大量种植及Bt制剂在农田中的广泛使用，鳞翅目、鞘翅目、双翅目等Cry靶标昆虫能够得到有效控制，而飞虱、叶蝉、蚜虫等半翅目非Bt靶标昆虫则依旧需要使用化学农药进行防治，甚至有大爆发的可能。因此，急需寻找或开发一种能够对此类半翅目害虫具有毒性作用的新型Cry毒素。
本研究首先克隆、表达并制备了可溶的Cry1Ab毒素蛋白，利用获得的Cry1Ab蛋白，制备了高效价的兔抗Cry1Ab的多克隆抗血清。而后，利用膜饲喂法测定了Cry1Ab蛋白对重要水稻害虫褐飞虱（Nilaparvata lugens）的毒性作用。并结合体外水解与Pull-down技术，利用免疫印迹法分析了Cry1Ab毒素对褐飞虱只有低毒作用的原因进行了分析，发现Cry1Ab毒素能够在褐飞虱中肠内被水解且能够与褐飞虱中肠刷状缘膜囊泡（brash border membrane vesicle, BBMV）结合。因此，推断Cry1Ab毒素对褐飞虱鲜有毒性作用的原因是其无法与正确的受体蛋白结合所致。
另一方面，本研究利用蚜虫中肠内膜结合短肽对Cry1Ab毒素domainⅡ中决定受体识别的3个loop进行逐一替换，并测定了替换loop后的三株Cry蛋白对鳞翅目小菜蛾幼虫的毒性作用。研究发现，在Cry1Ab domainⅡ中决定受体识别的3个loop分别被替换后，Cry1Ab毒素对小菜蛾的毒性作用受到不同程度的影响，其中loop2被替换后，Cry1Ab对小菜蛾的毒性作用下降最为明显，LC50达到32.25μg/mL。由此可以推断，对于Cry1A毒素而言，在受体识别功能作用上domainⅡ中的loop2起到的作用最大。
为了获得对褐飞虱具有较好毒性作用的新型Cry毒素，本研究利用噬菌体短肽文库展示技术筛选出了能够与水稻褐飞虱中肠内膜结合的短肽P2S。通过将P2S与加强绿色荧光蛋白（enhanced green fluorescent protein, EGFP）基因的融合，制备了P2S-EGFP融合蛋白，利用Pull-down技术及荧光显微镜观察，验证了P2S与褐飞虱中肠内膜及BBMV较强的结合能力。随后，本研究利用分子区域替换技术，使用能够与褐飞虱中肠内膜结合的短肽P2S及本实验室早先筛选出的能够与褐飞虱中肠BBMV结合的短肽P1Z分别对Cry1Ab决定受体识别的3个loop分别进行了替换获得了六株新型的cry基因，并对六株新型Cry蛋白进行了原核表达及纯化。通过体外水解、Pull-down体外结合及膜饲喂法生测，筛选出一株在褐飞虱中肠中最稳定，与褐飞虱中肠BBMV结合能力最强且对褐飞虱毒性作用最好的新型Cry毒素Cry1Ab-2S。该毒素将Cry1Ab对褐飞虱的毒性作用提高了近13倍。而后，本研究还利用透射电镜对取食了Cry1Ab-2S的褐飞虱中肠超微组织进行观察，发现其中肠内膜细胞有明显被消解的现象，证明了Cry1Ab-2S对褐飞虱的良好毒性作用。本研究为利用基因工程定向改造Cry毒素，为发展针对特定害虫作用的Cry毒素研究提供了可行的途径；为Cry毒素及其他昆虫毒素在昆虫体内受体的研究提供了新的思路；为应用分子工程手段发展新型害虫毒素提供理论和应用基础；为Cry和其它昆虫毒素的毒理机制研究提供新的手段。
本研究的特色与创新点主要包括：
1.分析了Cry毒素对半翅目褐飞虱等刺吸式口器害虫无法产生良好毒性作用的原因；
2.证明了domainⅡ三个受体识别loop对Cry1Ab毒性影响的重要性；
3.将噬菌体短肽文库展示技术与膜饲喂法相结合，成功筛选出能够穿透围食膜与褐飞虱中肠内膜结合的短肽；
4.通过定向改造、筛选，获得了能够对非Bt靶标的半翅目刺吸式口器害虫褐飞虱产生较好毒性作用的新型Cry毒素。
Cry toxins are the most important toxin extracted from Bacillus thuringiensis (Bt),which have been widely used in the management of lepidopteran, coleopteran,dipteran pests and nematode. Alone with the widely planting of transgenic cropscarrying Bt cry genes, target pest which is susceptive to Cry toxins will be effectivelycontrolled and the use of classical chemical pesticides which may cause risks to theenvironment will be decreased。
However, insecticidal spectrum of Cry toxins are limited. Only Lepidoptera,Coleoptera, Diptera are susceptible to Cry toxins. Currently, seldom reports concernedto the toxicity from Cry toxins against hemipteran pests such as aphids, planhoppersand leafhoppers. As a result, after the planting of Bt transgenic crops and widely usedof Bt insecticide, lepidopteran, coleopteran, dipteran pests will be efficientlycontrolled, but hemipteran pests with sucking and piercing mouth part like aphids,planthoppers and leafhoppers will only be managed by the use of traditional chemicalpesticides. The deterioration of these Bt nontarget pests will increase and even lead toan explosion. Thus, it is emergency to search or create a novel Cry toxin that showsconsiderable toxicity against these hemipteran pests.
Our research, firstly, prepared purified and soluble Cry1Ab pro-toxin. ThenCry1Ab antiserum was produced by immuning Cry1Ab pro-toxin to Newzealandwhite rabbit.The reason of low toxicity from Cry1Ab against N. lugens, an importantpest in rice production, was analyzed by the use of membrane feeding, pull-downtechnology and in vitro hydrolysis. Results showed that Cry1Ab pro-toxin can beefficiently activated into~60kDa peptide by proteaeses exist in N. lugens gut andthese activated mature peptide can bind to N. lugens BBMV (brash border membranevesicle). According to the reported mechanism of Cry1Ab toxin, activated protein cannot bind to proper receotros is the most likely reason for the low toxicity of Cry1Abagainst N. lugens.
On the other hand, three receptor binding loops in domainⅡ of Cry1Ab toxinwas replaced by an aphid gut inner membrane binding peptide GBP3.1respectively.To find out which loop is the most important receptor binding site, LC50of three modified Cry toxin, with each loop be substituded by GBP3.1, against diamond backmoth (Plutella xylostella) was tested. Results showed that toxicity of Cry1Ab toxindroped sharply when loop2was replaced, indicating that loop2is more importantthan loop1and loop3in receptor binding and toxicity excerting.
To develop a novel Cry toxin which will show toxicity to N. lugens, our researchscreened a peptide which could bind to N. lugens gut inner membrane. After fusingP2S with egfp (enhanced green fluorescent protein) gene, P2S-EGFP fusion proteinwas prepared to confirm the binding acitivy between P2S and N. lugens gut BBMV orgut inner membrane. After that, three receptor binding loops of Cry1Ab domainⅡwas replaced by P2S or P1Z (a peptide screened from N. lugens BBMV bindingphage) respectively to produce six novel Cry proteins. With the use of in vitrohydrolysis, pull-down technology and membrane feeding, one novel Cry toxinCry1Ab-2S with loop2be replaced by P2S was selected. Cry1Ab-2S was the moststable novel toxin after the treatment by N. lugens gut proteases and had the strongestbinding activity to N. lugens BBMV. Bioassay results demonstrated that toxicity ofCry1Ab-2S against N. lugens nymphs were nearly13folds more than Cry1Ab toxin.By observing gut ultrastructure of N. lugens though electron microscope, gutmicrovilli of N. lugens fed by Cry1Ab-2S was obviously hydrolyzed.
This research provides a new method for molecular modification of Cry toxinstarget on specific pests. Furthermore, result of this research will help theunderstanding of mechanism of Cry toxins in hemipteran insects. In summary, thisresearch work was focused on the following:
1. Analyzed the probable reseaon of low toxicity of Cry toxin against N. lugens andother hemipteran pest with sucking and piercing mouth part;
2. Determined the importance of three loops in domainⅡ in excerting toxicity ofCry1Ab toxin;
3. Screened a peptide which can bind to N. lugens gut inner membrane by phagedisplay library;
4. Obtained a novel Cry toxin showed high toxicity against N. lugens by directedmodification.
然而，Cry毒素蛋白的杀虫谱仅局限于鳞翅目、鞘翅目、双翅目等特定靶标昆虫，对于半翅目刺吸式口器的蚜虫、飞虱、叶蝉等昆虫暂时还没有有效Cry毒素的报道。随着能够表达Cry毒素的转基因作物的大量种植及Bt制剂在农田中的广泛使用，鳞翅目、鞘翅目、双翅目等Cry靶标昆虫能够得到有效控制，而飞虱、叶蝉、蚜虫等半翅目非Bt靶标昆虫则依旧需要使用化学农药进行防治，甚至有大爆发的可能。因此，急需寻找或开发一种能够对此类半翅目害虫具有毒性作用的新型Cry毒素。
本研究首先克隆、表达并制备了可溶的Cry1Ab毒素蛋白，利用获得的Cry1Ab蛋白，制备了高效价的兔抗Cry1Ab的多克隆抗血清。而后，利用膜饲喂法测定了Cry1Ab蛋白对重要水稻害虫褐飞虱（Nilaparvata lugens）的毒性作用。并结合体外水解与Pull-down技术，利用免疫印迹法分析了Cry1Ab毒素对褐飞虱只有低毒作用的原因进行了分析，发现Cry1Ab毒素能够在褐飞虱中肠内被水解且能够与褐飞虱中肠刷状缘膜囊泡（brash border membrane vesicle, BBMV）结合。因此，推断Cry1Ab毒素对褐飞虱鲜有毒性作用的原因是其无法与正确的受体蛋白结合所致。
另一方面，本研究利用蚜虫中肠内膜结合短肽对Cry1Ab毒素domainⅡ中决定受体识别的3个loop进行逐一替换，并测定了替换loop后的三株Cry蛋白对鳞翅目小菜蛾幼虫的毒性作用。研究发现，在Cry1Ab domainⅡ中决定受体识别的3个loop分别被替换后，Cry1Ab毒素对小菜蛾的毒性作用受到不同程度的影响，其中loop2被替换后，Cry1Ab对小菜蛾的毒性作用下降最为明显，LC50达到32.25μg/mL。由此可以推断，对于Cry1A毒素而言，在受体识别功能作用上domainⅡ中的loop2起到的作用最大。
为了获得对褐飞虱具有较好毒性作用的新型Cry毒素，本研究利用噬菌体短肽文库展示技术筛选出了能够与水稻褐飞虱中肠内膜结合的短肽P2S。通过将P2S与加强绿色荧光蛋白（enhanced green fluorescent protein, EGFP）基因的融合，制备了P2S-EGFP融合蛋白，利用Pull-down技术及荧光显微镜观察，验证了P2S与褐飞虱中肠内膜及BBMV较强的结合能力。随后，本研究利用分子区域替换技术，使用能够与褐飞虱中肠内膜结合的短肽P2S及本实验室早先筛选出的能够与褐飞虱中肠BBMV结合的短肽P1Z分别对Cry1Ab决定受体识别的3个loop分别进行了替换获得了六株新型的cry基因，并对六株新型Cry蛋白进行了原核表达及纯化。通过体外水解、Pull-down体外结合及膜饲喂法生测，筛选出一株在褐飞虱中肠中最稳定，与褐飞虱中肠BBMV结合能力最强且对褐飞虱毒性作用最好的新型Cry毒素Cry1Ab-2S。该毒素将Cry1Ab对褐飞虱的毒性作用提高了近13倍。而后，本研究还利用透射电镜对取食了Cry1Ab-2S的褐飞虱中肠超微组织进行观察，发现其中肠内膜细胞有明显被消解的现象，证明了Cry1Ab-2S对褐飞虱的良好毒性作用。本研究为利用基因工程定向改造Cry毒素，为发展针对特定害虫作用的Cry毒素研究提供了可行的途径；为Cry毒素及其他昆虫毒素在昆虫体内受体的研究提供了新的思路；为应用分子工程手段发展新型害虫毒素提供理论和应用基础；为Cry和其它昆虫毒素的毒理机制研究提供新的手段。
本研究的特色与创新点主要包括：
1.分析了Cry毒素对半翅目褐飞虱等刺吸式口器害虫无法产生良好毒性作用的原因；
2.证明了domainⅡ三个受体识别loop对Cry1Ab毒性影响的重要性；
3.将噬菌体短肽文库展示技术与膜饲喂法相结合，成功筛选出能够穿透围食膜与褐飞虱中肠内膜结合的短肽；
4.通过定向改造、筛选，获得了能够对非Bt靶标的半翅目刺吸式口器害虫褐飞虱产生较好毒性作用的新型Cry毒素。
Cry toxins are the most important toxin extracted from Bacillus thuringiensis (Bt),which have been widely used in the management of lepidopteran, coleopteran,dipteran pests and nematode. Alone with the widely planting of transgenic cropscarrying Bt cry genes, target pest which is susceptive to Cry toxins will be effectivelycontrolled and the use of classical chemical pesticides which may cause risks to theenvironment will be decreased。
However, insecticidal spectrum of Cry toxins are limited. Only Lepidoptera,Coleoptera, Diptera are susceptible to Cry toxins. Currently, seldom reports concernedto the toxicity from Cry toxins against hemipteran pests such as aphids, planhoppersand leafhoppers. As a result, after the planting of Bt transgenic crops and widely usedof Bt insecticide, lepidopteran, coleopteran, dipteran pests will be efficientlycontrolled, but hemipteran pests with sucking and piercing mouth part like aphids,planthoppers and leafhoppers will only be managed by the use of traditional chemicalpesticides. The deterioration of these Bt nontarget pests will increase and even lead toan explosion. Thus, it is emergency to search or create a novel Cry toxin that showsconsiderable toxicity against these hemipteran pests.
Our research, firstly, prepared purified and soluble Cry1Ab pro-toxin. ThenCry1Ab antiserum was produced by immuning Cry1Ab pro-toxin to Newzealandwhite rabbit.The reason of low toxicity from Cry1Ab against N. lugens, an importantpest in rice production, was analyzed by the use of membrane feeding, pull-downtechnology and in vitro hydrolysis. Results showed that Cry1Ab pro-toxin can beefficiently activated into~60kDa peptide by proteaeses exist in N. lugens gut andthese activated mature peptide can bind to N. lugens BBMV (brash border membranevesicle). According to the reported mechanism of Cry1Ab toxin, activated protein cannot bind to proper receotros is the most likely reason for the low toxicity of Cry1Abagainst N. lugens.
On the other hand, three receptor binding loops in domainⅡ of Cry1Ab toxinwas replaced by an aphid gut inner membrane binding peptide GBP3.1respectively.To find out which loop is the most important receptor binding site, LC50of three modified Cry toxin, with each loop be substituded by GBP3.1, against diamond backmoth (Plutella xylostella) was tested. Results showed that toxicity of Cry1Ab toxindroped sharply when loop2was replaced, indicating that loop2is more importantthan loop1and loop3in receptor binding and toxicity excerting.
To develop a novel Cry toxin which will show toxicity to N. lugens, our researchscreened a peptide which could bind to N. lugens gut inner membrane. After fusingP2S with egfp (enhanced green fluorescent protein) gene, P2S-EGFP fusion proteinwas prepared to confirm the binding acitivy between P2S and N. lugens gut BBMV orgut inner membrane. After that, three receptor binding loops of Cry1Ab domainⅡwas replaced by P2S or P1Z (a peptide screened from N. lugens BBMV bindingphage) respectively to produce six novel Cry proteins. With the use of in vitrohydrolysis, pull-down technology and membrane feeding, one novel Cry toxinCry1Ab-2S with loop2be replaced by P2S was selected. Cry1Ab-2S was the moststable novel toxin after the treatment by N. lugens gut proteases and had the strongestbinding activity to N. lugens BBMV. Bioassay results demonstrated that toxicity ofCry1Ab-2S against N. lugens nymphs were nearly13folds more than Cry1Ab toxin.By observing gut ultrastructure of N. lugens though electron microscope, gutmicrovilli of N. lugens fed by Cry1Ab-2S was obviously hydrolyzed.
This research provides a new method for molecular modification of Cry toxinstarget on specific pests. Furthermore, result of this research will help theunderstanding of mechanism of Cry toxins in hemipteran insects. In summary, thisresearch work was focused on the following:
1. Analyzed the probable reseaon of low toxicity of Cry toxin against N. lugens andother hemipteran pest with sucking and piercing mouth part;
2. Determined the importance of three loops in domainⅡ in excerting toxicity ofCry1Ab toxin;
3. Screened a peptide which can bind to N. lugens gut inner membrane by phagedisplay library;
4. Obtained a novel Cry toxin showed high toxicity against N. lugens by directedmodification.
引文
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