梨小食心虫嗅觉相关蛋白基因的分子生物学特性及其原核表达研究
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摘要
昆虫在漫长的进化过程中形成了复杂的嗅觉系统，并以此来感受环境中的信息化学物质，进而做出有利于自身生存和繁衍的行为反应，如寻找食物、求偶交配、定位寄主、躲避天敌等。利用昆虫这种生命活动过程中的特性采取适当的措施进行害虫防治，已成为害虫综合治理的重要手段。梨小食心虫是一种严重危害桃、梨等多种果树的世界性重要害虫，在包括我国在内的许多国家和地区猖獗发生，对果业生产造成了严重危害。目前，生产上主要依靠果实套袋和化学防治，但前者操作费工、费时，且随劳动力价格的上涨已面临严峻的挑战；化学防治则因该虫钻蛀危害，隐蔽性强而效果较差。鉴于此，研发经济高效的梨小食心虫防治新技术已成为生产中亟待解决的问题。深入研究梨小食心虫成虫嗅觉识别系统，阐明梨小食心虫与寄主植物之间信息联系的本质，必将有助于研发梨小食心虫的新型引诱剂和趋避剂，为防治梨小食心虫提供新的思路与途径。
本论文从梨小食心虫成虫感受信息化合物的生理基础入手，系统研究了梨小食心虫成虫的行为习性及其日生理节律，触角感受器的形态、结构和分布；在此基础上研究了梨小食心虫成虫嗅觉识别系统的分子基础——普通气味结合蛋白和化学感受蛋白，取得的主要结果如下。
1、成虫行为节律研究
在人工气候箱（室温23.5～24.5℃、相对湿度60%～80%、光周期15L:9D）条件下，对梨小食心虫成虫羽化、交配及产卵行为及其日节律进行了系统观测。结果表明，梨小食心虫成虫的羽化、交配和产卵节律均具明显时间特点。成虫的羽化主要集中在05:00-10:00，此时成虫的羽化数量达总羽化数量的90%以上，其中以5:00-6:00成虫羽化率最高，显著高于其它时段；雌雄成虫求偶交配多发生在羽化后第3天，雌雄两性呈“一”字形进行交配，单次交配持续时间的平均值为22.07min，交配活动主要集中在17:00-21:00，交配发生率超过90%；雌成虫的产卵时间与雌雄成虫的交配时间基本一致，也主要集中在17:00-21:00，此时雌成虫产卵量达总产卵量的87.43%，显著高于其它时段。
2、成虫触角感器研究
采用扫描电镜对梨小食心虫成虫触角进行观察和研究表明，梨小食心虫成虫触角上共存在7种感器，分别为毛形感器、锥形感器、刺形感器、栓锥形感器、腔锥感器、耳形感器和B hm氏鬃毛。不同触角感器的形态构造和分布特点各异，说明其功能有别。
3、普通气味结合蛋白基因的克隆和表达特性研究
采用反转录多聚酶链式反应（RT-PCR）和cDNA末端快速扩增（RACE）技术，从梨小食心虫雌成虫触角组织克隆到2个编码普通气味结合蛋白（GOBP）的cDNA全长序列GmolGOBP1（Genbank登录号：JN857939）和GmolGOBP2（Genbank登录号：JN857940）。序列分析表明，梨小食心虫的2个GOBP的cDNA序列全长分别为1090bp和637bp，开放性阅读框分别为492bp和483bp，编码164和161个氨基酸残基，预测其N-末端均具由20个氨基酸残基组成的信号肽序列。梨小食心虫的2个普通气味结合蛋白基因推导的氨基酸序列与已知鳞翅目其它昆虫普通气味结合蛋白具很高同源性，但GmolGOBP1和GmolGOBP2之间的同源性仅48%，说明它们归于不同的昆虫普通气味结合蛋白类群。
RT-PCR研究结果显示GmolGOBP1和GmolGOBP2均仅在雌雄成虫触角组织中特异性表达。Real-time PCR研究结果表明，GmolGOBP1在雄成虫触角的表达量较高，而GmolGOBP2在雌成虫触角的表达量较高。另外，研究发现GmolGOBP1在雌雄两性触角及GmolGOBP2在雌虫触角中明显的上调表达均发生在光期的末段及整个暗期，而雄成虫触角中GmolGOBP2在整个光周期各时段表达量相似，据此结果，对GmolGOBP1和GmolGOBP2可能的生理功能进行了探讨。
4、化学感受蛋白基因的克隆及序列分析
采用RT-PCR和RACE技术克隆了梨小食心虫化学感受蛋白基因GmolCSP（GenBank登录号：JQ821389）。GmolCSP开放性阅读框全长384bp，编码127个氨基酸，N-末端含18个氨基酸组成的信号肽序列，成熟蛋白预测分子量为12.80kD，等电点为8.33，且GmolCSP具有4个保守半胱氨酸，符合昆虫化学感受蛋白的一般特征。通过序列相似性及系统发育树分析，GmolCSP与云杉卷蛾Choristoneura fumiferana（CfumCSP3）亲缘关系最近，相似性为73%其次是烟芽夜蛾Heliothis virescens（HvirCSP2），相似性为68%，与其他昆虫仅有34～46%的相似性。RT-PCR研究结果显示，GmolCSP不仅在梨小食心虫触角中表达，在去触角的头，胸、腹、足和翅中均有表达。
5、普通气味结合蛋白2与化学感受蛋白基因的原核表达
在成功克隆梨小食心虫普通气味结合蛋白（GmolGOBPs）和化学感受蛋白（GmolCSP）基因的基础上，将GmolGOBP2和GmolCSP与原核表达载体pET-32a进行重组，在大肠杆菌BL21（DE3）中表达，Western Blots结果显示，大肠杆菌中表达的蛋白正是pET/GmolGOBP2和pET/GmolCSP重组蛋白，从而实现了GmolGOBP2和GmolCSP在大肠杆菌中的表达。异源表达的实现为今后研究蛋白功能及提示梨小食心虫嗅觉识别系统奠定了良好基础。
Throughout evolution, the olfactory system of insect have become highly sensitive,enabling recognize chemical signal from the environment and triggers insect behavioralresponse, such as locating mates, food source, habitat, and ovipositon. Olfactory-basedcontrol strategy has become more and more important in integrated pest management （IPM）.The oriental fruit moth, Grapholita molesta is a severe pest of various fruit crops throughoutworld. Control of G. molesta predominantly relies on chemical pesticides and fruit bagging.However, due to the larvae burrow into fruit and damage only the inner tissues, the chemicalpesticides, which control G. molesta, are not satisfactory. With the increasing prices of laborpower, the fruit bagging is also difficult for orchardists to put it into effect. A strategy forcontrolling adult G. molesta, based on chemical stimuli derived from host plant, is desirableTherefore, it is very important to explore the chemical communication system of G. molesta.With the insights on the chemical communication system, it will be facilitated for design andimplementation of novel monitoring and control strategies against G. molesta.
In this paper, the physiological basis of G. molesta chemical communication system,including adult behavioral rhythm, the morphology, structure and distribution of antennalsensillae, was firstly studied. And then, the chemical communication system of G.molesta wasfurther studied at molecular level. In later part, we studied two functional proteins in insectchemical communication system, general odorant binding proteins （GOBPs） andchemosensory proteins （CSPs）. The main results are as follows:
1. The behavioral rhythms of adult Grapholita molesta
In the laboratory, the Behavioral characteristics of G. molesta，including adult emergence,mating and oviposition behaviors, were investigated under a L15:9D regime at24±0.5℃and70±10%r.h. The results revealed that90%of adults emergence occurred between05:00and10:00, the peak of emergence was between05:00and06:00；the calling behavior of adultscommenced in the3rd days after adult emergence. males and females mated with copulatorypose of “一” type. The mean duration of mating was22.07min. and more than90%ofmating occurred between17:00and21:00；Oviposition in most of females occurred between 17:00and21:00amounting to87.43%of total oviposition.
2. Ultrastructural observation of antennal sensilla of adult Grapholitamolesta
The antennae of G. molesta were observed by scanning electron microscopy. The resultsindicated that the antennae of G. molesta were threadlike and made up of scape, pedicel andflagellum. There were seven kinds of sensillae, including sensilla trichodea, sensillabasiconica, sensilla chaetica, sensilla styloconica, sensilla coeloconica, sensilla auricillica andB hm bristles.
3. Cloning and characterization of GOBP genes from Grapholita molesta
Two new general odorant binding protein （GOBP） genes, GmolGOBP1andGmolGOBP2, were cloned from antennae of female G. molesta by use of RT-PCR and RACE.The GenBank accession numbers are JN857939and JN857940, respectively. The full-lengthcDNA of GmolGOBP1is1090bp with a492bp open reading frame encoding164aminoacids. GmolGOBP2cDNA is637bp in length containing a483bp open reading frameencoding161amino acids. Proteins signature analysis indicated that they contains anN-terminal signal sequence of20amino acids. The two GOBPs from G. molesta show lowsequence identity （48%）, but they are similarity to GOBPs of the same group from otherlepidopteran, suggesting that the two GOBPs belong to different classes of lepidopteranGOBPs.
RT-PCR analysis indicated that GmolGOBP1and GmolGOBP2are only expressed inantennae of both sexes. Real-time PCR analysis further revealed that the transcript level ofGmolGOBP1was higher in males than in females, whereas the transcript level ofGmolGOBP2was higher in females than in males. The high transcript levels of GmolGOBP1in both sex and GmolGOBP2in female were detected at the end of photophase and duringscotophase. The expression of GmolGOBP2in male remained at similar levels during thecomplete photoperiod. Based on these results, the possible physiological functions ofGmolGOBPs are discussed.
4. Cloning and sequence analysis of CSP gene from Grapholita molesta
A novel chemosensory protein gene, GmolCSP, was cloned from antennae of adult G.molesta by use of RT-PCR and RACE. The GenBank accession numbers are JQ821389. Theisolated cDNA encoding GmolCSP contains a384bp open reading frame for a polypeptide of127amino acids. The predicted amino acid sequences contain an N-terminal signal sequence of18amino acids. The mature deduced GmolCSP consist of109amino acids with amolecular mass of12.80kD, and an IP of8.33. after analysis of sequence similarity andphylogenetic tree, it was indicated that GmolCSP share high homology with CfumCSP3（73%）, and then HvirCSP2（68%）, however, GmolCSP share low similarity with otherlepidopteran （34～46%identity）. RT-PCR analysis indicated that GmolCSP expressed in allof the test tissues, including antenna, head, head without antennae, thorax, abdomen, leg andwing.
5. The prokaryotic expression of GOBP2and CSP from Grapholita molesta
Heterologous expression of genes can provide insights to the gene function. Based oncloned GmolGOBP2and GmolCSP information, the GmolGOBP2and GmolCSP wereconstructed into prodaryotic expression vectors pET-32a, and expressed in BL21（DE3）.The results of Western Blot indicated that the recombinant prteins （pET/GmolGOBP2andpET/GmolCSP）were successfully expressed. Our results are not only helpful for the researchof GmolGOBP2and GmolCSP, but also can form a solid basis to explore the chemicalcommunication system of G. molesta.
本论文从梨小食心虫成虫感受信息化合物的生理基础入手，系统研究了梨小食心虫成虫的行为习性及其日生理节律，触角感受器的形态、结构和分布；在此基础上研究了梨小食心虫成虫嗅觉识别系统的分子基础——普通气味结合蛋白和化学感受蛋白，取得的主要结果如下。
1、成虫行为节律研究
在人工气候箱（室温23.5～24.5℃、相对湿度60%～80%、光周期15L:9D）条件下，对梨小食心虫成虫羽化、交配及产卵行为及其日节律进行了系统观测。结果表明，梨小食心虫成虫的羽化、交配和产卵节律均具明显时间特点。成虫的羽化主要集中在05:00-10:00，此时成虫的羽化数量达总羽化数量的90%以上，其中以5:00-6:00成虫羽化率最高，显著高于其它时段；雌雄成虫求偶交配多发生在羽化后第3天，雌雄两性呈“一”字形进行交配，单次交配持续时间的平均值为22.07min，交配活动主要集中在17:00-21:00，交配发生率超过90%；雌成虫的产卵时间与雌雄成虫的交配时间基本一致，也主要集中在17:00-21:00，此时雌成虫产卵量达总产卵量的87.43%，显著高于其它时段。
2、成虫触角感器研究
采用扫描电镜对梨小食心虫成虫触角进行观察和研究表明，梨小食心虫成虫触角上共存在7种感器，分别为毛形感器、锥形感器、刺形感器、栓锥形感器、腔锥感器、耳形感器和B hm氏鬃毛。不同触角感器的形态构造和分布特点各异，说明其功能有别。
3、普通气味结合蛋白基因的克隆和表达特性研究
采用反转录多聚酶链式反应（RT-PCR）和cDNA末端快速扩增（RACE）技术，从梨小食心虫雌成虫触角组织克隆到2个编码普通气味结合蛋白（GOBP）的cDNA全长序列GmolGOBP1（Genbank登录号：JN857939）和GmolGOBP2（Genbank登录号：JN857940）。序列分析表明，梨小食心虫的2个GOBP的cDNA序列全长分别为1090bp和637bp，开放性阅读框分别为492bp和483bp，编码164和161个氨基酸残基，预测其N-末端均具由20个氨基酸残基组成的信号肽序列。梨小食心虫的2个普通气味结合蛋白基因推导的氨基酸序列与已知鳞翅目其它昆虫普通气味结合蛋白具很高同源性，但GmolGOBP1和GmolGOBP2之间的同源性仅48%，说明它们归于不同的昆虫普通气味结合蛋白类群。
RT-PCR研究结果显示GmolGOBP1和GmolGOBP2均仅在雌雄成虫触角组织中特异性表达。Real-time PCR研究结果表明，GmolGOBP1在雄成虫触角的表达量较高，而GmolGOBP2在雌成虫触角的表达量较高。另外，研究发现GmolGOBP1在雌雄两性触角及GmolGOBP2在雌虫触角中明显的上调表达均发生在光期的末段及整个暗期，而雄成虫触角中GmolGOBP2在整个光周期各时段表达量相似，据此结果，对GmolGOBP1和GmolGOBP2可能的生理功能进行了探讨。
4、化学感受蛋白基因的克隆及序列分析
采用RT-PCR和RACE技术克隆了梨小食心虫化学感受蛋白基因GmolCSP（GenBank登录号：JQ821389）。GmolCSP开放性阅读框全长384bp，编码127个氨基酸，N-末端含18个氨基酸组成的信号肽序列，成熟蛋白预测分子量为12.80kD，等电点为8.33，且GmolCSP具有4个保守半胱氨酸，符合昆虫化学感受蛋白的一般特征。通过序列相似性及系统发育树分析，GmolCSP与云杉卷蛾Choristoneura fumiferana（CfumCSP3）亲缘关系最近，相似性为73%其次是烟芽夜蛾Heliothis virescens（HvirCSP2），相似性为68%，与其他昆虫仅有34～46%的相似性。RT-PCR研究结果显示，GmolCSP不仅在梨小食心虫触角中表达，在去触角的头，胸、腹、足和翅中均有表达。
5、普通气味结合蛋白2与化学感受蛋白基因的原核表达
在成功克隆梨小食心虫普通气味结合蛋白（GmolGOBPs）和化学感受蛋白（GmolCSP）基因的基础上，将GmolGOBP2和GmolCSP与原核表达载体pET-32a进行重组，在大肠杆菌BL21（DE3）中表达，Western Blots结果显示，大肠杆菌中表达的蛋白正是pET/GmolGOBP2和pET/GmolCSP重组蛋白，从而实现了GmolGOBP2和GmolCSP在大肠杆菌中的表达。异源表达的实现为今后研究蛋白功能及提示梨小食心虫嗅觉识别系统奠定了良好基础。
Throughout evolution, the olfactory system of insect have become highly sensitive,enabling recognize chemical signal from the environment and triggers insect behavioralresponse, such as locating mates, food source, habitat, and ovipositon. Olfactory-basedcontrol strategy has become more and more important in integrated pest management （IPM）.The oriental fruit moth, Grapholita molesta is a severe pest of various fruit crops throughoutworld. Control of G. molesta predominantly relies on chemical pesticides and fruit bagging.However, due to the larvae burrow into fruit and damage only the inner tissues, the chemicalpesticides, which control G. molesta, are not satisfactory. With the increasing prices of laborpower, the fruit bagging is also difficult for orchardists to put it into effect. A strategy forcontrolling adult G. molesta, based on chemical stimuli derived from host plant, is desirableTherefore, it is very important to explore the chemical communication system of G. molesta.With the insights on the chemical communication system, it will be facilitated for design andimplementation of novel monitoring and control strategies against G. molesta.
In this paper, the physiological basis of G. molesta chemical communication system,including adult behavioral rhythm, the morphology, structure and distribution of antennalsensillae, was firstly studied. And then, the chemical communication system of G.molesta wasfurther studied at molecular level. In later part, we studied two functional proteins in insectchemical communication system, general odorant binding proteins （GOBPs） andchemosensory proteins （CSPs）. The main results are as follows:
1. The behavioral rhythms of adult Grapholita molesta
In the laboratory, the Behavioral characteristics of G. molesta，including adult emergence,mating and oviposition behaviors, were investigated under a L15:9D regime at24±0.5℃and70±10%r.h. The results revealed that90%of adults emergence occurred between05:00and10:00, the peak of emergence was between05:00and06:00；the calling behavior of adultscommenced in the3rd days after adult emergence. males and females mated with copulatorypose of “一” type. The mean duration of mating was22.07min. and more than90%ofmating occurred between17:00and21:00；Oviposition in most of females occurred between 17:00and21:00amounting to87.43%of total oviposition.
2. Ultrastructural observation of antennal sensilla of adult Grapholitamolesta
The antennae of G. molesta were observed by scanning electron microscopy. The resultsindicated that the antennae of G. molesta were threadlike and made up of scape, pedicel andflagellum. There were seven kinds of sensillae, including sensilla trichodea, sensillabasiconica, sensilla chaetica, sensilla styloconica, sensilla coeloconica, sensilla auricillica andB hm bristles.
3. Cloning and characterization of GOBP genes from Grapholita molesta
Two new general odorant binding protein （GOBP） genes, GmolGOBP1andGmolGOBP2, were cloned from antennae of female G. molesta by use of RT-PCR and RACE.The GenBank accession numbers are JN857939and JN857940, respectively. The full-lengthcDNA of GmolGOBP1is1090bp with a492bp open reading frame encoding164aminoacids. GmolGOBP2cDNA is637bp in length containing a483bp open reading frameencoding161amino acids. Proteins signature analysis indicated that they contains anN-terminal signal sequence of20amino acids. The two GOBPs from G. molesta show lowsequence identity （48%）, but they are similarity to GOBPs of the same group from otherlepidopteran, suggesting that the two GOBPs belong to different classes of lepidopteranGOBPs.
RT-PCR analysis indicated that GmolGOBP1and GmolGOBP2are only expressed inantennae of both sexes. Real-time PCR analysis further revealed that the transcript level ofGmolGOBP1was higher in males than in females, whereas the transcript level ofGmolGOBP2was higher in females than in males. The high transcript levels of GmolGOBP1in both sex and GmolGOBP2in female were detected at the end of photophase and duringscotophase. The expression of GmolGOBP2in male remained at similar levels during thecomplete photoperiod. Based on these results, the possible physiological functions ofGmolGOBPs are discussed.
4. Cloning and sequence analysis of CSP gene from Grapholita molesta
A novel chemosensory protein gene, GmolCSP, was cloned from antennae of adult G.molesta by use of RT-PCR and RACE. The GenBank accession numbers are JQ821389. Theisolated cDNA encoding GmolCSP contains a384bp open reading frame for a polypeptide of127amino acids. The predicted amino acid sequences contain an N-terminal signal sequence of18amino acids. The mature deduced GmolCSP consist of109amino acids with amolecular mass of12.80kD, and an IP of8.33. after analysis of sequence similarity andphylogenetic tree, it was indicated that GmolCSP share high homology with CfumCSP3（73%）, and then HvirCSP2（68%）, however, GmolCSP share low similarity with otherlepidopteran （34～46%identity）. RT-PCR analysis indicated that GmolCSP expressed in allof the test tissues, including antenna, head, head without antennae, thorax, abdomen, leg andwing.
5. The prokaryotic expression of GOBP2and CSP from Grapholita molesta
Heterologous expression of genes can provide insights to the gene function. Based oncloned GmolGOBP2and GmolCSP information, the GmolGOBP2and GmolCSP wereconstructed into prodaryotic expression vectors pET-32a, and expressed in BL21（DE3）.The results of Western Blot indicated that the recombinant prteins （pET/GmolGOBP2andpET/GmolCSP）were successfully expressed. Our results are not only helpful for the researchof GmolGOBP2and GmolCSP, but also can form a solid basis to explore the chemicalcommunication system of G. molesta.
引文
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