蝶蛹金小蜂毒液分子特性及其调控寄主分子机理的研究
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摘要
寄生蜂携带毒液、多分DNA病毒、类病毒颗粒、畸形细胞等寄生因子，以抑制寄主细胞或体液免疫，以及调控寄主生长发育来保证其后代在寄主体内或体外成功发育。这些寄生因子因具有特殊的生理功能，若能结合现代生物技术，以这些活性物质为资源研制新型生防制剂或转基因作物，将为害虫生物防治开辟新的途径。为此，寄生蜂与寄主相互作用关系的研究一直以来是昆虫生理生化和生物防治领域的研究热点。这些研究旨在揭示寄生蜂寄生因子的本质及其调控寄主的机制，为这些资源的利用奠定基础。目前，对多分DNA病毒和类病毒颗粒生化与分子特性的研究已相当多，如近10种寄生蜂携带的多分DNA病毒已得到全基因组测序，从中获得了众多基因资源。然而，就毒液而言，现仅有为数不多的组分被鉴定。在寄生蜂调控寄主的机制方面，很大程度上仅是生理生化层面的研究，很少有寄生蜂调控寄主分子机制的研究。此外，在寄生蜂与寄主相互作用关系的研究中，涉及的寄生蜂主要限于茧蜂科Braconidae和姬蜂科Ichneumonidae，且多限于卵-幼虫期或幼虫期寄生蜂。有鉴于此，本研究以菜粉蝶Pieris rapae(鳞翅目Lepidoptera：粉蝶科Pieridae)的蛹期优势内寄生蜂蝶蛹金小蜂Pteromalus puparum(膜翅目Hymenoptera：金小蜂科Pteromalidae)(仅携带毒液一种寄生因子)为研究对象，在本实验室对蝶蛹金小蜂毒液生化特性及其调控寄主生理生化机制有过较详细研究的基础上，开展了蝶蛹金小蜂毒液分子特性及其调控寄主分子机理的研究。
1蝶蛹金小蜂毒液分子特性
(1)蝶蛹金小蜂毒器官形态结构。利用光镜和电镜技术研究了蝶蛹金小蜂毒器官形态结构，并利用电泳和免疫组化技术研究了毒液在毒器官中的合成。蝶蛹金小蜂毒器官由毒腺和毒囊构成，并附着有杜氏腺。毒腺由基膜层、分泌细胞层、导管细胞层和内膜层组成。基膜层和内膜层，薄而光滑。分泌细胞层，毒腺组织的主要部分，分泌细胞内含粗糙型内质网、分泌囊泡、末端附器、分泌颗粒、液泡等细胞器，其末端附器有导管和毒腺腔体连通，用于收集毒腺分泌物。导管细胞层，导管细胞内细胞器种类较少，仅有分泌囊泡，细胞核比分泌细胞的细胞核小了很多。毒囊由肌肉鞘层、上皮细胞层和内膜层由外向内依次排列组成。肌肉鞘层，肌纤丝纵向有序排列，不交错。上皮细胞层，其细胞核大而长形。内膜层，薄，均匀而光滑。电泳和免疫组化结果表明，和毒囊一样，毒腺中也存在毒液蛋白，毒液主要在毒腺中合成，最后贮存在毒囊中。
(2)蝶蛹金小蜂毒液蛋白质组学分析。双向电泳结果显示，蝶蛹金小蜂毒液中主要有55个蛋白质点，等电点集中在4-7之间，分子量主要在25-66．2 kDa之间。所有蛋白质点经质谱鉴定，获得了钙网蛋白、精氨酸激酶、丝氨酸蛋白酶、热激蛋白70等4个毒液蛋白。
(3)蝶蛹金小蜂毒器官cDNA文库的构建及EST序列分析。文库原始滴度为1．6×10~6cfu，重组率为90．65％，外源插入片段在0．5-2．5 kb之间。对文库进行小规模随机测序，共得到256条高质量序列，其中仅有72条序列得到基因注释，说明蝶蛹金小蜂毒器官中的大部分基因为新基因。经EST分析，获得了蝶蛹金小蜂毒液酸性磷酸酶和丝氨酸蛋白酶的部分基因序列。另外，还获得一个病毒结构蛋白基因，开放阅读框(ORF)为2619 bp，编码873 aa，预测分子量为97．6 kDa，由分子量为28 kDa、31 kDa、28 kDa和9．6 kDa的4个衣壳蛋白组成。系统进化分析表明，该病毒与Black queen cell virus的进化程度最近，属于具致病性的双顺反子病毒科Dicistroviridae，蟋蟀麻痹病毒属Cripavirus。
(4)蝶蛹金小蜂毒液钙网蛋白基因的克隆及分析。该毒液蛋白基因全长为1685 bp，ORF为1212 bp，编码404 aa，预测分子量为42．57 kDa，pI为4．31，与菜粉蝶微红盘绒茧蜂Cotesia rubecula毒液钙网蛋白的相似性为69％。
(5)蝶蛹金小蜂毒液精氨酸激酶基因的克隆及表达。该毒液蛋白基因全长为1828 bp，ORF为1068 bp，编码356 aa，预测分子量为39．9 kDa，pI为8．89，与背湾沟蛛蜂Cyphononyxdorsalis毒液精氨酸激酶的相似性高达92％。利用pET-32a表达载体，成功对该毒液蛋白基因进行了原核表达。
(6)蝶蛹金小蜂毒液酸性磷酸酶基因的克隆及分析。克隆到该蜂毒液酸性磷酸酶基因全长为1378 bp，ORF为1215 bp，编码405 aa，预测分子量为39．9 kDa，pI为8．89，与丽蝇蛹集金小蜂Nasoniavitripennis、意大利蜜蜂Apis mellifera、赤拟谷盗Tribolium castaneum、埃及伊蚊Aedes aegypti和黑腹果蝇Drosophila melanogaster的酸性磷酸酶相似性分别为88％、41％、31％、30％和29％。以p-NPP(p-pnitrophenyl phosphate，p-NPP)为底物分析蝶蛹金小蜂毒液酸性磷酸酶生化特性，明确其最适pH和温度分别为4．8和45℃，酶活性能被NaF抑制。在毒腺分泌细胞中，酸性磷酸酶分布在细胞核和分泌囊泡上。RT-PCR分析表明，蝶蛹金小蜂毒液酸性磷酸酶基因在毒器官中的转录具有时相性。该毒液蛋白在毒器官内的含量也随发育时间变化而改变，并与其基因转录模式一致。
(7)蝶蛹金小蜂毒液碱性磷酸酶基因的克隆及分析。利用5-溴-4-氯-3-吲哚基-磷酸盐和氮蓝四唑染色方法，在蝶蛹金小蜂毒器官中发现有碱性磷酸酶存在。超微结构研究也发现碱性磷酸酶分布在毒腺分泌细胞的细胞核和分泌囊泡上。以p-NPP(p-pnitrophenylphosphate，p-NPP)为底物分析蝶蛹金小蜂毒液碱性磷酸酶生化特性，发现温度和二价金属离子都能影响其酶活性。克隆得到蝶蛹金小蜂毒液碱性磷酸酶基因全长为2645 bp，ORF为1623 bp，编码541 aa，预测分子量为59．83 kDa，pI为6．98，与丽蛹集金小蜂、意大利蜜蜂、赤拟谷盗、埃及伊蚊和黑腹果蝇碱性磷酸酶的相似性分别为91％、66％、48％、48％和46％。RT-PCR分析表明，蝶蛹金小蜂毒液酸性磷酸酶在毒器官中的转录具有时相性。该毒液蛋白在毒器官内的含量也随发育时间变化而改变，并与与其基因转录模式一致。2蝶蛹金小蜂调控寄主菜粉蝶的分子机理
(1)蝶蛹金小蜂寄生对菜粉蝶血浆蛋白质组分的影响。通过双向电泳研究发现，菜粉蝶蛹被蝶蛹金小蜂寄生24 h后，其血浆中7个蛋白质点发生了差异表达，这些差异蛋白质点经质谱鉴定，为类似丝氨酸蛋白酶同源蛋白、烯醇化酶、成虫盘生长因子、胆素结合蛋白、鸟氨酸脱羧酶、维甲酸结合蛋白以及一未知功能蛋白，它们为与免疫、细胞骨架、解毒和能量代谢相关蛋白。依据质谱获得的肽段序列，设计简并引物，并结合RACE技术，克隆获得了类似丝氨酸蛋白酶同源蛋白、烯醇化酶和胆素结合蛋白的全长基因。RT-PCR分析表明，蝶蛹金小蜂寄生能导致菜粉蝶类似丝氨酸蛋白酶同源蛋白和胆素结合蛋白基因在蛹脂肪体中的转录水平升高，而对烯醇化酶和成虫盘生长因子蛹脂肪体中的转录水平无影响。
(2)蝶蛹金小蜂寄生对菜粉蝶贮藏蛋白基因的转录调控。克隆了菜粉蝶贮藏蛋白基因，并研究了蝶蛹金小蜂寄生对其转录水平的影响。菜粉蝶贮藏蛋白基因全长为2270 bp，ORF为2121 bp，编码707 aa，预测分子量约83 kDa，pI 6．13。推导的氨基酸序列中有一16 aa的信号肽，2个保守的贮藏蛋白家族结构域。分子进化分析表明，克隆到的菜粉蝶贮藏蛋白基因属芳基贮藏蛋白。依据氨基酸组成，克隆到的菜粉蝶贮藏蛋白甲硫氨酸和芳香族氨基酸的含量分别为1．42％和18．82％，属芳基贮藏蛋白的范围。RT-PCR分析表明，蝶蛹金小蜂寄生能引起菜粉蝶芳基贮藏蛋白基因在蛹脂肪体中的转录水平升高。
(3)蝶蛹金小蜂寄生对菜粉蝶钙网蛋白基因的转录调控。克隆了菜粉蝶钙网蛋白基因，并研究了蝶蛹金小蜂寄生对其转录水平的影响。菜粉蝶钙网蛋白基因全长1816 bp，ORF为1194 bp，编码398 aa，预测分子量为45．75 kDa，pI 4．4。推导的氨基酸序列，可分为N、P、C 3个区域，3个区域的特性与其它物种钙网蛋白相似，与意大利蜜蜂、冈比亚按蚊Anopheles gambiae和黑腹果蝇的相似性分别为74％、70％和69％。RT-PCR分析表明，蝶蛹金蜂寄生能抑制钙网蛋白基因在菜粉蝶蛹血细胞中的转录水平。
(4)蝶蛹金小蜂寄生对菜粉蝶血细胞骨架相关蛋白基因的转录调控。克隆了菜粉蝶肌动蛋白、肌动蛋白解聚因子及微管蛋白基因，并研究了蝶蛹金小蜂寄生对其转录水平的影响。菜粉蝶肌动蛋白基因ORF为1131 bp，编码377 aa，预测分子量为41．78 kDa，pI为5．29，与其它昆虫肌动蛋白的相似性非常高，在90％以上。氨基酸组成特点和系统进化分析表明，克隆到的菜粉蝶肌动蛋白基因属细胞质型肌动蛋白。菜粉蝶肌动蛋白解聚因子基因全长为1243 bp，ORF为447 bp，编码149 aa，预测分子量为16．97 kDa，pI为7．11，与家蚕Bombyx mori、赤拟谷盗、意大利蜜蜂和桑粉介壳虫Maconellicoccus hirsutus肌动蛋白解聚因子的相似性分别为97％、87％、89％和72％。菜粉蝶微管蛋白基因全长为1757bp，ORF为1344 bp，编码448 aa，预测分子量为50．38 kDa，pI为4．86，与家蚕β型微管蛋白1、2、3和4的相似性分别为97％、97％、87％和93％。系统进化分析表明，克隆到的菜粉蝶微管蛋白基因属β型微管蛋白。RT-PCR分析表明，蝶蛹金蜂寄生能抑制肌动蛋白、肌动蛋白解聚因子及微管蛋白基因在菜粉蝶蛹血细胞中的转录水平。
(5)蝶蛹金小蜂毒液对寄主菜粉蝶内分泌激素的影响。结合寄生和毒液离体注射的方法，以未寄生和注射PBS为对照，测定菜粉蝶蛹血淋巴内保幼激素滴度、保幼激素酯酶活性和蜕皮激素滴度在处理后72 h内的变化。结果显示，寄生或注射毒液寄主蛹血淋巴的保幼激素(仅检测到Ⅲ型)滴度在24-72 h内显著高于对照组，且在处理12 h后保幼激素滴度激急上升；保幼激素酯酶活性在未寄生或注射PBS的蛹血淋巴中分别于6-48 h和12-36 h显著高于处理组，且其活性分别在12 h和24 h达到最大值；与处理组相比，蜕皮激素滴度在未寄生或注射PBS的蛹血淋巴中，12-36 h之间快速上升，在36 h达到峰值，然后下降，但48 h以前其滴度均高于处理组，并在24-48 h与处理组呈显著差异。研究结果表明，蝶蛹金小蜂毒液能够扰乱其寄主菜粉蝶蛹的激素分泌系统。
(6)蝶蛹金小蜂寄生对柑桔凤蝶血浆蛋白质组分的影响。通过双向电泳研究发现，柑桔凤蝶蛹被蝶蛹金小蜂寄生24 h后，其血浆中有16个蛋白质点发生了差异表达。其中8个蛋白点表达量上调，5个蛋白点表达量下降，1个蛋白质点消失，2个蛋白质点新出现。这些差异表达蛋白质点经质谱鉴定，为与细胞或体液免疫、解毒及能量代谢相关的蛋白。
通过较系统的研究，本论文取得了下列创新性成果：明确了蝶蛹金小蜂毒器官的显微和超微形态结构，鉴定出蛹期或金小蜂科寄生蜂毒液中有钙网蛋白、精氨酸激酶、丝氨酸蛋白酶、热激蛋白70、酸性磷酸酶和碱性磷酸酶等组分，克隆了钙网蛋白精氨酸激酶、酸性磷酸酶和碱性磷酸酶等4个毒液蛋白基因，并明确了酸性和碱性磷酸酶基因的组织定位、生化特性和表达时相；在寄生蜂毒器官中发现了1种致病性微小RNA新病毒；发现以毒液为单一寄生因子的寄生蜂寄生能引起寄主免疫、解毒和能量代谢的相关蛋白差异表达，其中与营养代谢相关的芳基贮藏蛋白基因的转录水平上升，而与细胞免疫相关的钙网蛋白、肌动蛋白、肌动蛋白解聚因子及微管蛋白的转录水平下降；发现寄生蜂毒液能扰乱寄主的内分泌系统。这些结果在很大程度上揭示了寄生蜂与寄主互作的分子机制，对开辟利用寄生蜂毒液控制害虫的新途径有指导意义。
Parasitoids associated diversified range of virulence parasitic factors such as venom,polydnaviruse(PDV),virus-like particle(VLP),and teratocyte appear to interfere with host'simmune response or to disrupt host's development to insure the successful development of theiroffspring in the hemocoel or at the external surface of host insects.Given the specialphysiological functions,these parasitic factors would be potentially valuable resources ofnatural substance in developing new environmentally safe insect control agents or transgeneticcrops with modem biotechnologies.As a consequence,parasitoid-host interaction is a focalresearch point in the entomological physiology and biochemistry and biological control area,which aims to explore the nature of the parasitic factors and the mechanisms of parasitoidmanipulation of host that helpful to gain insights into the potential properties of the parasiticfactors for future practical use.Up to date,the biochemical and molecular basis of PDV andVLP have been well documented.The genome of PDV from near 10 parasitoids has beencompletely sequenced and lots of gene resources from them are available.Howeverover,onlylittle is known so far on the biochemical and molecular basis of venom.Regarding to themechanisms of parasitoid-host interactions,mostly investigations carried out at thephysiological and biochemical levels,but molecular dissection of parasitoid-host interactions isstill little known.In addition,in terms of parasitoid-host systems,the investigated parasitoids aremostly limited to ichneumonid and braconid,and are of egg-larval or larval stage specificparasitism.By consideration the historical perspective on previous issues on parasitoid-hostinteractions and on the basis of detailed biochemical characters and physiological functions ofvenom from Pteromalus puparum(Hymenoptera:Pteromalidae)(no other parasitoid associatedfactors other than venom are found in the female reproductive organ),a predominate pupalendoparasitoid of Pieris rapae(Lepidoptera:Pieridae),been well investigated in our laboratory,we here report on the outcomes of molecular characterization of venom from P.puparum andmolecular mechanism of this parasitoid manipulation to the host.
1 Molecular characterization of venom from P.puparum
(1)Morphology and ultrastructure of P.puparum venom apparatus.The venomapparatus of P.puparum was studied with light and electron microscope and was subjected tothe electrophoretic and immunohistochemical analyses.Typically its venom apparatus consistsof a venom gland and a venom reservoir,which is associated with a Dufour gland.The venomgland consists of four layers of basement membrane layer,secretory cell layer,duct cell layer and inner intima layer.Basement membrane and inner intima layers have evenly thickenedorganization.Secretory cells in the venom gland are characterized by extensive roughendoplasmic reticulum and numerous secretory vesicles,which is associated with an endapparatus to collect its secretions into the venom gland lumen.They also exhibit severalsecretory granules and vacuoles.Duct cells in the venom gland lack numerous cellularorganelles except secretory vesicles and their nucleus becomes smaller as compared to thenucleus in the secretory cell.The venom reservoir presents three distinct regions:an externallayer,composed by numerous fine muscle fibers;an internal layer,represented by epithelial cellwith large nucleus;and an intima portion,represented by thin and uniform organization.Theelectrophoretic and immunohistochemical results reveal that the rich proteinaceous componentsare present in the venom gland as that in venom reservoir.The venom proteins are firstly mainlyproduced in the venom gland,then drained to the lumen through the end apparatus,and arefinally collected and stored in the venom reservoir.
(2)Proteomic analysis of P.puparum venom.Two-dimensional gel electrophoresisclearly defined 55 spots showing a major protein region(25-66.2 kDa,pI 4-7)were observed.All the venom protein spots were analyzed by mass spectrometry.Four venom components wereidentified:calreticulin,arginine kinase,serine protease and heat shock protein 70.
(3)cDNA library construction and EST analysis of P.puparum venom apparatus.Theoriginal titration of library was 1.6×10~6 cfu with recombinant rate of 90.65%.The averagelength of insert cDNA fragment was between 0.5 kb and 2.5 kb.265 ESTs from the cDNAlibrary were obtained.After annotation,the results revealed that only 72 ESTs showedsignificant similarity to known genes from other organisms,and the other had no match to anydatabase sequence,indicating that mostly venom genes of P.puparum are new genes.Thevenom acid phospoatase and serine protease genes were obtained.A few contigs with homologyto virus structural protein were observed.Its open reading frame(ORF)was 2619 bp encoding873 amino acid residues with estimated molecular weight of 97.6 kDa.Its mature protein waswith three major capsid polyproteins(28,31 and 28 kDa)and a minor one(9.6 kDa).
Phylogenetic evolution analysis exhibited that this virus belonged to the Cripavirus genus ofpathogenetic dicistroviruse and fell into same clade with Black queen cell virus.
(4)Cloning and sequence analysis of cDNA encoding venom calreticulin gene of P.puparum.The 1722 bp full-length sequence had an open reading frame of 1212 bp encoding aprotein of 404 amino acids.The calculated molecular mass of the mature protein was 42.57 kDawith an estimated pI of 4.31.Sequence comparison showed that this venom protein has anoverall similarity of 69% to venom calreticulin of Cotesia rubecula.
(5)Cloning and expression of venom arginine kinase gene of P.puparum.Thecomplete cDNA consisted of 1828 bp and contained an open reading frame of 1068 bp thatencoded 356 amino acid residues and had a predicted molecular weight of 39.9 kDa and pI 8.89.Sequence comparison showed that this venom protein has a highly similarity of 92% to venomarginine kinase of Cyphononyx dorsalis.This gene was expressed as a fusion protein usingpET-32a vector in Escherichia coli.
(6)Molecular cloning and characterization of acid phosphatase in venom of P.puparum.The cDNA consisted of 1378 bp with 1215 bp open reading frame and encoded asequence of 405 amino acids.By multiple sequence alignment,the deduced amino acidsequence shared 88%,41%,31%,30% and 29% identity to its counterparts from Nasoniavitripennis,Apis mellifera,Tribolium castaneum,Aedes aegypti and Drosophila melanogaster.Using p-nitrophenyl phosphate(p-NPP)as substrate,the optimal pH and temperature for thisenzyme activity was measured to be 4.8 and 45℃,respectively.And NaF treatment waseffective way to inhibit the activity if this venom enzyme.Ultracytochemical analyses furtherrevealed that strong enzyme activity was located in the nuclei and secretory vesicles of thevenom gland secretory cells.Expression of the acid phosphatase gene was observed to beregulated at different developmental stages by RT-PCR analysis.Compared to the mRNAexpression,a time-course related enzyme activity in an individual venom apparatus was alsofound.
(7)Molecular cloning and characterization of alkaline phosphatase in venom of P.puparum.Using chromogenic substrates 5-bromo-4-chloro-3'-indolyl phosphate(BCIP)andnitro blue tetrazolium(NBT),alkaline phosphatase was histochemically detected in the venomapparatus of P.puparum.Ultrastructural observations also demonstrated its presence in thesecretory vesicles and nuclei of the venom gland secretory cells.Using p-nitrophenyl phosphate(p-NPP)as substrate to measure the enzyme activity,this venom alkaline phosphatase wasfound to be temperature dependent and with bivalent cations effects.The full-length eDNAsequence of alkaline phosphatase was 2645 bp with 1623 bp open reading frame covered 541deduced amino acids with predicted molecular mass of 59.83 kDa and pI of 6.98.By multiplesequence alignment,the deduced amino acid sequence shared 91%,66%,48%,48% and 46%identity to its counterparts from N.vitripennis,A.mellifera,T.castaneum,A.aegypti and D.melanogaster.The transcript of alkaline phosphatase gene was detected by RT-PCR in venomapparatus with development related expression after adult wasp emergence.Compared to themRNA expression,a time-course related enzyme activity in an individual venom apparatus wasalso found.
2 Molecular mechanism of P.puparum manipulation of P.rapae
(1)Proteome changes in the plasma ofP.rapae induced by P.puparum parasitization.By examining the differential expression of plasma proteins in the parasitized and unparasitizedhosts pupae after 24 h by two-dimensional electrophoresis,7 proteins were found to vary inrelation to parasitization compared to unparasitized control samples.All of them were submittedto identification by mass spectrometry coupled with a database search.Six were identified asmasquerade-like serine proteinase homolog(MasSPH),enolase(ENO),imaginal disc growthfactor(IDGF),bilin-binding protein(BBP),ornithine decarboxylase(ODC)and cellular retinoicacid binding protein(CRABP).Next to known function proteins,one was identified asunannotated proteins.The modulated proteins were found to fall into the following functionalgroups:humoral or cellular immunity,detoxification,energy metabolism,and others.Degenerate primers designed based on peptides obtained from mass spectral analysis were usedfor PCR amplification of the fragment of the differential expressed proteins.And their fulllength eDNA were derived from RACE amplification.The gene of MasSPH,ENO and BBPwere cloned and sequenced.RT-PCR analysis indicated that parasitization by P.puparuminduced increased transcripts of MasSPH and BBP,and had no apparent impact on the level ofIDGF and ENO transcripts in the fat body of P.rapae pupae.
(2)cDNA of an arylphorin-type storage protein from P.rapae with parasitisminducible expression by P.puparum.The cDNA of a storage protein,PraAry,from P.rapaewas cloned and its expression regulated by parasitization of P.puparum was investigated.Thefull-length cDNA of PraAry was 2270 nucleotides and contains a 2121 bp open reading frameencoding 707 amino acids with calculated molecular weights of approximately 83 kDa.Analysisof the primary protein sequence revealed that it possesses a signal peptide of 16 amino acids atthe N-terminus and contains two highly conserved storage protein signature motifs.Accordingto both phylogenetic analysis and the criteria for amino acid composition,PraAry belongs to thesubfamily of arylphorin-type storage protein(1.42% methionine and 18.82% aromatic aminoacids).RT-PCR analysis indicated that the transcriptional level of PraAry mRNA in P.rapaepupae fat body is inducible upregulation in response to parasitization by P.puparum.
(3)Transcriptional changes of calreticulin from P.rapae after parasitization by P.puparum.The cDNA of calreticulin from P.rapae was cloned and its expression regulated byparasitization of P.puparum was investigated.Sequence analysis showed that P.rapaecalreticulin was of 1816 bp in full length contained an 1194 bp open reading frame whichpredicted a 398 amino acid protein.The calculated molecular mass and pI were 45.75 kDa and4.4,respectively.The deduced amino acid sequence contained N,P and C domains with special characters similar to that of other species,sharing 74%,70% and 69% homology with thecounterparts of A.mellifera,Anopheles gambiae and D.melanogaster.Expression analyses ofthe calreticulin gene in the haemocyte of P.rapae pupae parasitized and unparasitized by P.puparum were performed by RT-PCR,which indicated down regulated transcription underparasitization.
(4)Transcriptional changes of cytoskeleton related proteins of P.rapae afterparasitization by the endoparasitoid wasp P.puparum.The cDNA of actin,actindepolymerisation factor and tubulin from P.rapae was cloned and their expression regulated byparasitization of P.puparum was investigated.P.rapae actin contained an open reading frameof 1131 bp encoding for 377 amino acid residues with predicted molecular mass and pI of 41.78kDa and 5.29,respectively.The homology of P.rapae actin with other insect actin genes wasgreater than 90% in amino acids.P.rapae actin was classified as a cytoplasmic type by absenceof muscle-specific amino acids and phylogenetic tree analysis.The 1243 bp cDNA sequence ofP.rapae actin depolymerisation factor contained an open reading frame of 447 bp encoding anneutral(pI 7.11)protein of 149 amino acids predicted molecular mass of 16.97 kDa,sharing97%,87%,89% and 72% homology with the counterparts of Bombyx mori,T.castaneum,A.mellifera and Maconellicoccus hirsutus.Nucleotide sequence analysis of P.rapae tubulinshowed full length cDNA of 1757 bp with open reading frames of 1344 bp encoding proteins of448 amino acids with a predicted molecular weight and pI of 50.38 kDa and 4.86,respectively.The cDNA-deduced amino acid sequence of P.rapae tubulin showed 97%,97%,87% and 93%homology with that of B.mori beta-tubulin 1,2,3 and 4.P.rapae tubulin was classified as betatype by phylogenetic evolution analysis.RT-PCR analysis showed that P.rapae actin,actindepolymerisation factor and tubulin gene were affected by P.puparum parasitization indicatingdecreased expression.
(5)Endocrine changes in the hemolymph ofP.rapae indiced by venom of P.puparum.The changes of hemolymph juvenile hormone(JH)(only JHⅢdetected),ecdysteroid andjuvenile hormone esterase activity(JHE)over 72 h in parasitized and venom microinjected P.rapae pupae were monitored.Non-parasisized and PBS microinjected P.rapae served ascontrols.Results showed that JH titers were significant higher in parasitized and venommicroinjected pupae than that in control pupae during 24 to 72 h.After 12 h,JH titers weresignificantly promoted by parasitization and venom microinjection.JHE activities ofnon-parasitized and PBS microinjected pupae were significant higher than that of parasitizedand venom microinjected which was with a peak at 12 h(parasitized pupae)or 24 h(venommicroinjected pupae)during 6 to 48 and 12 to 36 h respectively.The hemolymph titers of ecdysteroid in non-parasitized and PBS microinjected pupae increased rapidly during 12 to 36 hwith a peak at 36 h,and were higher than treatments before 48 h,while presenting significantdifference at 24 to 48 h between the treatments and controls.The results demonstrate that venomalone of this parasitoid wasp can disrupt its host's endocrine system.
(6)Proteome changes in the plasma of Papilio xuthus induced by P.puparumparasitization.By examining the differential expression of plasma proteins in the parasitizedand non-parasitized hosts pupae after 24 h by two-dimensional electrophoresis,16 proteins werefound to vary in relation to parasitization compared to unparasitized control samples.Among ofthem,8 proteins were elevated,5 showed decreased expression,and 1 disappeared,and 2 newlyoccurred after parasitization.All of them were submitted to identification by mass spectrometrycoupled with a database search.The modulated proteins were found to fall into the followingfunctional groups:humoral or cellular immunity,detoxification,energy metabolism,and others.
In this paper,the microstructure and ultrastructure of venom apparatus of P.puparum wasclearly defined.The venom proteins of calreticulin,arginine kinase,serine protease,heat shockprotein 70,acid phosphatase and alkaline phosphatase were firtly identified from the venom ofpupal stage specific parasitoid or parasitoid belonging to Pteromalidae.The cDNA encodingvenom calreticulin,arginine kinase,acid phosphatase and alkaline phosphatase genes werecloned and sequenced,and the tissue location,biochemical characters and time-course relatedgene expression of acid and alkaline phosphatase were defined,which provided the firstevidence for the detail investigation of parasitoid venom acid and alkaline phosphatase.A novelpathogenic small RNA virus belonged to the Cripavirus genus of Dicistroviridae was reportedfrom the parasitoid.The results first revealed that the parasitization by the parasitoid onlyassociated with venom induced the proteins in the host plasma related to humoral or cellularimmunity,detoxification,energy metabolism differentially expressed,the the transcription ofnutrition metabolism related arylphorin-type storage protein gene up regulated,and thetranscription of cellular immune related calreticulin,actin,actin depolymerisation factor andtubulin genes decreased.In addition,the results firstly demonstrated that venom alone ofparasitoid can disrupted its host's endocrine system.These results not only revealed themolecular mechanisms of the interaction between parasitoid and host to a large extent,but alsomade a great contribution to gain insights into exploiting parasitoid venom for insect control.
1蝶蛹金小蜂毒液分子特性
(1)蝶蛹金小蜂毒器官形态结构。利用光镜和电镜技术研究了蝶蛹金小蜂毒器官形态结构，并利用电泳和免疫组化技术研究了毒液在毒器官中的合成。蝶蛹金小蜂毒器官由毒腺和毒囊构成，并附着有杜氏腺。毒腺由基膜层、分泌细胞层、导管细胞层和内膜层组成。基膜层和内膜层，薄而光滑。分泌细胞层，毒腺组织的主要部分，分泌细胞内含粗糙型内质网、分泌囊泡、末端附器、分泌颗粒、液泡等细胞器，其末端附器有导管和毒腺腔体连通，用于收集毒腺分泌物。导管细胞层，导管细胞内细胞器种类较少，仅有分泌囊泡，细胞核比分泌细胞的细胞核小了很多。毒囊由肌肉鞘层、上皮细胞层和内膜层由外向内依次排列组成。肌肉鞘层，肌纤丝纵向有序排列，不交错。上皮细胞层，其细胞核大而长形。内膜层，薄，均匀而光滑。电泳和免疫组化结果表明，和毒囊一样，毒腺中也存在毒液蛋白，毒液主要在毒腺中合成，最后贮存在毒囊中。
(2)蝶蛹金小蜂毒液蛋白质组学分析。双向电泳结果显示，蝶蛹金小蜂毒液中主要有55个蛋白质点，等电点集中在4-7之间，分子量主要在25-66．2 kDa之间。所有蛋白质点经质谱鉴定，获得了钙网蛋白、精氨酸激酶、丝氨酸蛋白酶、热激蛋白70等4个毒液蛋白。
(3)蝶蛹金小蜂毒器官cDNA文库的构建及EST序列分析。文库原始滴度为1．6×10~6cfu，重组率为90．65％，外源插入片段在0．5-2．5 kb之间。对文库进行小规模随机测序，共得到256条高质量序列，其中仅有72条序列得到基因注释，说明蝶蛹金小蜂毒器官中的大部分基因为新基因。经EST分析，获得了蝶蛹金小蜂毒液酸性磷酸酶和丝氨酸蛋白酶的部分基因序列。另外，还获得一个病毒结构蛋白基因，开放阅读框(ORF)为2619 bp，编码873 aa，预测分子量为97．6 kDa，由分子量为28 kDa、31 kDa、28 kDa和9．6 kDa的4个衣壳蛋白组成。系统进化分析表明，该病毒与Black queen cell virus的进化程度最近，属于具致病性的双顺反子病毒科Dicistroviridae，蟋蟀麻痹病毒属Cripavirus。
(4)蝶蛹金小蜂毒液钙网蛋白基因的克隆及分析。该毒液蛋白基因全长为1685 bp，ORF为1212 bp，编码404 aa，预测分子量为42．57 kDa，pI为4．31，与菜粉蝶微红盘绒茧蜂Cotesia rubecula毒液钙网蛋白的相似性为69％。
(5)蝶蛹金小蜂毒液精氨酸激酶基因的克隆及表达。该毒液蛋白基因全长为1828 bp，ORF为1068 bp，编码356 aa，预测分子量为39．9 kDa，pI为8．89，与背湾沟蛛蜂Cyphononyxdorsalis毒液精氨酸激酶的相似性高达92％。利用pET-32a表达载体，成功对该毒液蛋白基因进行了原核表达。
(6)蝶蛹金小蜂毒液酸性磷酸酶基因的克隆及分析。克隆到该蜂毒液酸性磷酸酶基因全长为1378 bp，ORF为1215 bp，编码405 aa，预测分子量为39．9 kDa，pI为8．89，与丽蝇蛹集金小蜂Nasoniavitripennis、意大利蜜蜂Apis mellifera、赤拟谷盗Tribolium castaneum、埃及伊蚊Aedes aegypti和黑腹果蝇Drosophila melanogaster的酸性磷酸酶相似性分别为88％、41％、31％、30％和29％。以p-NPP(p-pnitrophenyl phosphate，p-NPP)为底物分析蝶蛹金小蜂毒液酸性磷酸酶生化特性，明确其最适pH和温度分别为4．8和45℃，酶活性能被NaF抑制。在毒腺分泌细胞中，酸性磷酸酶分布在细胞核和分泌囊泡上。RT-PCR分析表明，蝶蛹金小蜂毒液酸性磷酸酶基因在毒器官中的转录具有时相性。该毒液蛋白在毒器官内的含量也随发育时间变化而改变，并与其基因转录模式一致。
(7)蝶蛹金小蜂毒液碱性磷酸酶基因的克隆及分析。利用5-溴-4-氯-3-吲哚基-磷酸盐和氮蓝四唑染色方法，在蝶蛹金小蜂毒器官中发现有碱性磷酸酶存在。超微结构研究也发现碱性磷酸酶分布在毒腺分泌细胞的细胞核和分泌囊泡上。以p-NPP(p-pnitrophenylphosphate，p-NPP)为底物分析蝶蛹金小蜂毒液碱性磷酸酶生化特性，发现温度和二价金属离子都能影响其酶活性。克隆得到蝶蛹金小蜂毒液碱性磷酸酶基因全长为2645 bp，ORF为1623 bp，编码541 aa，预测分子量为59．83 kDa，pI为6．98，与丽蛹集金小蜂、意大利蜜蜂、赤拟谷盗、埃及伊蚊和黑腹果蝇碱性磷酸酶的相似性分别为91％、66％、48％、48％和46％。RT-PCR分析表明，蝶蛹金小蜂毒液酸性磷酸酶在毒器官中的转录具有时相性。该毒液蛋白在毒器官内的含量也随发育时间变化而改变，并与与其基因转录模式一致。2蝶蛹金小蜂调控寄主菜粉蝶的分子机理
(1)蝶蛹金小蜂寄生对菜粉蝶血浆蛋白质组分的影响。通过双向电泳研究发现，菜粉蝶蛹被蝶蛹金小蜂寄生24 h后，其血浆中7个蛋白质点发生了差异表达，这些差异蛋白质点经质谱鉴定，为类似丝氨酸蛋白酶同源蛋白、烯醇化酶、成虫盘生长因子、胆素结合蛋白、鸟氨酸脱羧酶、维甲酸结合蛋白以及一未知功能蛋白，它们为与免疫、细胞骨架、解毒和能量代谢相关蛋白。依据质谱获得的肽段序列，设计简并引物，并结合RACE技术，克隆获得了类似丝氨酸蛋白酶同源蛋白、烯醇化酶和胆素结合蛋白的全长基因。RT-PCR分析表明，蝶蛹金小蜂寄生能导致菜粉蝶类似丝氨酸蛋白酶同源蛋白和胆素结合蛋白基因在蛹脂肪体中的转录水平升高，而对烯醇化酶和成虫盘生长因子蛹脂肪体中的转录水平无影响。
(2)蝶蛹金小蜂寄生对菜粉蝶贮藏蛋白基因的转录调控。克隆了菜粉蝶贮藏蛋白基因，并研究了蝶蛹金小蜂寄生对其转录水平的影响。菜粉蝶贮藏蛋白基因全长为2270 bp，ORF为2121 bp，编码707 aa，预测分子量约83 kDa，pI 6．13。推导的氨基酸序列中有一16 aa的信号肽，2个保守的贮藏蛋白家族结构域。分子进化分析表明，克隆到的菜粉蝶贮藏蛋白基因属芳基贮藏蛋白。依据氨基酸组成，克隆到的菜粉蝶贮藏蛋白甲硫氨酸和芳香族氨基酸的含量分别为1．42％和18．82％，属芳基贮藏蛋白的范围。RT-PCR分析表明，蝶蛹金小蜂寄生能引起菜粉蝶芳基贮藏蛋白基因在蛹脂肪体中的转录水平升高。
(3)蝶蛹金小蜂寄生对菜粉蝶钙网蛋白基因的转录调控。克隆了菜粉蝶钙网蛋白基因，并研究了蝶蛹金小蜂寄生对其转录水平的影响。菜粉蝶钙网蛋白基因全长1816 bp，ORF为1194 bp，编码398 aa，预测分子量为45．75 kDa，pI 4．4。推导的氨基酸序列，可分为N、P、C 3个区域，3个区域的特性与其它物种钙网蛋白相似，与意大利蜜蜂、冈比亚按蚊Anopheles gambiae和黑腹果蝇的相似性分别为74％、70％和69％。RT-PCR分析表明，蝶蛹金蜂寄生能抑制钙网蛋白基因在菜粉蝶蛹血细胞中的转录水平。
(4)蝶蛹金小蜂寄生对菜粉蝶血细胞骨架相关蛋白基因的转录调控。克隆了菜粉蝶肌动蛋白、肌动蛋白解聚因子及微管蛋白基因，并研究了蝶蛹金小蜂寄生对其转录水平的影响。菜粉蝶肌动蛋白基因ORF为1131 bp，编码377 aa，预测分子量为41．78 kDa，pI为5．29，与其它昆虫肌动蛋白的相似性非常高，在90％以上。氨基酸组成特点和系统进化分析表明，克隆到的菜粉蝶肌动蛋白基因属细胞质型肌动蛋白。菜粉蝶肌动蛋白解聚因子基因全长为1243 bp，ORF为447 bp，编码149 aa，预测分子量为16．97 kDa，pI为7．11，与家蚕Bombyx mori、赤拟谷盗、意大利蜜蜂和桑粉介壳虫Maconellicoccus hirsutus肌动蛋白解聚因子的相似性分别为97％、87％、89％和72％。菜粉蝶微管蛋白基因全长为1757bp，ORF为1344 bp，编码448 aa，预测分子量为50．38 kDa，pI为4．86，与家蚕β型微管蛋白1、2、3和4的相似性分别为97％、97％、87％和93％。系统进化分析表明，克隆到的菜粉蝶微管蛋白基因属β型微管蛋白。RT-PCR分析表明，蝶蛹金蜂寄生能抑制肌动蛋白、肌动蛋白解聚因子及微管蛋白基因在菜粉蝶蛹血细胞中的转录水平。
(5)蝶蛹金小蜂毒液对寄主菜粉蝶内分泌激素的影响。结合寄生和毒液离体注射的方法，以未寄生和注射PBS为对照，测定菜粉蝶蛹血淋巴内保幼激素滴度、保幼激素酯酶活性和蜕皮激素滴度在处理后72 h内的变化。结果显示，寄生或注射毒液寄主蛹血淋巴的保幼激素(仅检测到Ⅲ型)滴度在24-72 h内显著高于对照组，且在处理12 h后保幼激素滴度激急上升；保幼激素酯酶活性在未寄生或注射PBS的蛹血淋巴中分别于6-48 h和12-36 h显著高于处理组，且其活性分别在12 h和24 h达到最大值；与处理组相比，蜕皮激素滴度在未寄生或注射PBS的蛹血淋巴中，12-36 h之间快速上升，在36 h达到峰值，然后下降，但48 h以前其滴度均高于处理组，并在24-48 h与处理组呈显著差异。研究结果表明，蝶蛹金小蜂毒液能够扰乱其寄主菜粉蝶蛹的激素分泌系统。
(6)蝶蛹金小蜂寄生对柑桔凤蝶血浆蛋白质组分的影响。通过双向电泳研究发现，柑桔凤蝶蛹被蝶蛹金小蜂寄生24 h后，其血浆中有16个蛋白质点发生了差异表达。其中8个蛋白点表达量上调，5个蛋白点表达量下降，1个蛋白质点消失，2个蛋白质点新出现。这些差异表达蛋白质点经质谱鉴定，为与细胞或体液免疫、解毒及能量代谢相关的蛋白。
通过较系统的研究，本论文取得了下列创新性成果：明确了蝶蛹金小蜂毒器官的显微和超微形态结构，鉴定出蛹期或金小蜂科寄生蜂毒液中有钙网蛋白、精氨酸激酶、丝氨酸蛋白酶、热激蛋白70、酸性磷酸酶和碱性磷酸酶等组分，克隆了钙网蛋白精氨酸激酶、酸性磷酸酶和碱性磷酸酶等4个毒液蛋白基因，并明确了酸性和碱性磷酸酶基因的组织定位、生化特性和表达时相；在寄生蜂毒器官中发现了1种致病性微小RNA新病毒；发现以毒液为单一寄生因子的寄生蜂寄生能引起寄主免疫、解毒和能量代谢的相关蛋白差异表达，其中与营养代谢相关的芳基贮藏蛋白基因的转录水平上升，而与细胞免疫相关的钙网蛋白、肌动蛋白、肌动蛋白解聚因子及微管蛋白的转录水平下降；发现寄生蜂毒液能扰乱寄主的内分泌系统。这些结果在很大程度上揭示了寄生蜂与寄主互作的分子机制，对开辟利用寄生蜂毒液控制害虫的新途径有指导意义。
Parasitoids associated diversified range of virulence parasitic factors such as venom,polydnaviruse(PDV),virus-like particle(VLP),and teratocyte appear to interfere with host'simmune response or to disrupt host's development to insure the successful development of theiroffspring in the hemocoel or at the external surface of host insects.Given the specialphysiological functions,these parasitic factors would be potentially valuable resources ofnatural substance in developing new environmentally safe insect control agents or transgeneticcrops with modem biotechnologies.As a consequence,parasitoid-host interaction is a focalresearch point in the entomological physiology and biochemistry and biological control area,which aims to explore the nature of the parasitic factors and the mechanisms of parasitoidmanipulation of host that helpful to gain insights into the potential properties of the parasiticfactors for future practical use.Up to date,the biochemical and molecular basis of PDV andVLP have been well documented.The genome of PDV from near 10 parasitoids has beencompletely sequenced and lots of gene resources from them are available.Howeverover,onlylittle is known so far on the biochemical and molecular basis of venom.Regarding to themechanisms of parasitoid-host interactions,mostly investigations carried out at thephysiological and biochemical levels,but molecular dissection of parasitoid-host interactions isstill little known.In addition,in terms of parasitoid-host systems,the investigated parasitoids aremostly limited to ichneumonid and braconid,and are of egg-larval or larval stage specificparasitism.By consideration the historical perspective on previous issues on parasitoid-hostinteractions and on the basis of detailed biochemical characters and physiological functions ofvenom from Pteromalus puparum(Hymenoptera:Pteromalidae)(no other parasitoid associatedfactors other than venom are found in the female reproductive organ),a predominate pupalendoparasitoid of Pieris rapae(Lepidoptera:Pieridae),been well investigated in our laboratory,we here report on the outcomes of molecular characterization of venom from P.puparum andmolecular mechanism of this parasitoid manipulation to the host.
1 Molecular characterization of venom from P.puparum
(1)Morphology and ultrastructure of P.puparum venom apparatus.The venomapparatus of P.puparum was studied with light and electron microscope and was subjected tothe electrophoretic and immunohistochemical analyses.Typically its venom apparatus consistsof a venom gland and a venom reservoir,which is associated with a Dufour gland.The venomgland consists of four layers of basement membrane layer,secretory cell layer,duct cell layer and inner intima layer.Basement membrane and inner intima layers have evenly thickenedorganization.Secretory cells in the venom gland are characterized by extensive roughendoplasmic reticulum and numerous secretory vesicles,which is associated with an endapparatus to collect its secretions into the venom gland lumen.They also exhibit severalsecretory granules and vacuoles.Duct cells in the venom gland lack numerous cellularorganelles except secretory vesicles and their nucleus becomes smaller as compared to thenucleus in the secretory cell.The venom reservoir presents three distinct regions:an externallayer,composed by numerous fine muscle fibers;an internal layer,represented by epithelial cellwith large nucleus;and an intima portion,represented by thin and uniform organization.Theelectrophoretic and immunohistochemical results reveal that the rich proteinaceous componentsare present in the venom gland as that in venom reservoir.The venom proteins are firstly mainlyproduced in the venom gland,then drained to the lumen through the end apparatus,and arefinally collected and stored in the venom reservoir.
(2)Proteomic analysis of P.puparum venom.Two-dimensional gel electrophoresisclearly defined 55 spots showing a major protein region(25-66.2 kDa,pI 4-7)were observed.All the venom protein spots were analyzed by mass spectrometry.Four venom components wereidentified:calreticulin,arginine kinase,serine protease and heat shock protein 70.
(3)cDNA library construction and EST analysis of P.puparum venom apparatus.Theoriginal titration of library was 1.6×10~6 cfu with recombinant rate of 90.65%.The averagelength of insert cDNA fragment was between 0.5 kb and 2.5 kb.265 ESTs from the cDNAlibrary were obtained.After annotation,the results revealed that only 72 ESTs showedsignificant similarity to known genes from other organisms,and the other had no match to anydatabase sequence,indicating that mostly venom genes of P.puparum are new genes.Thevenom acid phospoatase and serine protease genes were obtained.A few contigs with homologyto virus structural protein were observed.Its open reading frame(ORF)was 2619 bp encoding873 amino acid residues with estimated molecular weight of 97.6 kDa.Its mature protein waswith three major capsid polyproteins(28,31 and 28 kDa)and a minor one(9.6 kDa).
Phylogenetic evolution analysis exhibited that this virus belonged to the Cripavirus genus ofpathogenetic dicistroviruse and fell into same clade with Black queen cell virus.
(4)Cloning and sequence analysis of cDNA encoding venom calreticulin gene of P.puparum.The 1722 bp full-length sequence had an open reading frame of 1212 bp encoding aprotein of 404 amino acids.The calculated molecular mass of the mature protein was 42.57 kDawith an estimated pI of 4.31.Sequence comparison showed that this venom protein has anoverall similarity of 69% to venom calreticulin of Cotesia rubecula.
(5)Cloning and expression of venom arginine kinase gene of P.puparum.Thecomplete cDNA consisted of 1828 bp and contained an open reading frame of 1068 bp thatencoded 356 amino acid residues and had a predicted molecular weight of 39.9 kDa and pI 8.89.Sequence comparison showed that this venom protein has a highly similarity of 92% to venomarginine kinase of Cyphononyx dorsalis.This gene was expressed as a fusion protein usingpET-32a vector in Escherichia coli.
(6)Molecular cloning and characterization of acid phosphatase in venom of P.puparum.The cDNA consisted of 1378 bp with 1215 bp open reading frame and encoded asequence of 405 amino acids.By multiple sequence alignment,the deduced amino acidsequence shared 88%,41%,31%,30% and 29% identity to its counterparts from Nasoniavitripennis,Apis mellifera,Tribolium castaneum,Aedes aegypti and Drosophila melanogaster.Using p-nitrophenyl phosphate(p-NPP)as substrate,the optimal pH and temperature for thisenzyme activity was measured to be 4.8 and 45℃,respectively.And NaF treatment waseffective way to inhibit the activity if this venom enzyme.Ultracytochemical analyses furtherrevealed that strong enzyme activity was located in the nuclei and secretory vesicles of thevenom gland secretory cells.Expression of the acid phosphatase gene was observed to beregulated at different developmental stages by RT-PCR analysis.Compared to the mRNAexpression,a time-course related enzyme activity in an individual venom apparatus was alsofound.
(7)Molecular cloning and characterization of alkaline phosphatase in venom of P.puparum.Using chromogenic substrates 5-bromo-4-chloro-3'-indolyl phosphate(BCIP)andnitro blue tetrazolium(NBT),alkaline phosphatase was histochemically detected in the venomapparatus of P.puparum.Ultrastructural observations also demonstrated its presence in thesecretory vesicles and nuclei of the venom gland secretory cells.Using p-nitrophenyl phosphate(p-NPP)as substrate to measure the enzyme activity,this venom alkaline phosphatase wasfound to be temperature dependent and with bivalent cations effects.The full-length eDNAsequence of alkaline phosphatase was 2645 bp with 1623 bp open reading frame covered 541deduced amino acids with predicted molecular mass of 59.83 kDa and pI of 6.98.By multiplesequence alignment,the deduced amino acid sequence shared 91%,66%,48%,48% and 46%identity to its counterparts from N.vitripennis,A.mellifera,T.castaneum,A.aegypti and D.melanogaster.The transcript of alkaline phosphatase gene was detected by RT-PCR in venomapparatus with development related expression after adult wasp emergence.Compared to themRNA expression,a time-course related enzyme activity in an individual venom apparatus wasalso found.
2 Molecular mechanism of P.puparum manipulation of P.rapae
(1)Proteome changes in the plasma ofP.rapae induced by P.puparum parasitization.By examining the differential expression of plasma proteins in the parasitized and unparasitizedhosts pupae after 24 h by two-dimensional electrophoresis,7 proteins were found to vary inrelation to parasitization compared to unparasitized control samples.All of them were submittedto identification by mass spectrometry coupled with a database search.Six were identified asmasquerade-like serine proteinase homolog(MasSPH),enolase(ENO),imaginal disc growthfactor(IDGF),bilin-binding protein(BBP),ornithine decarboxylase(ODC)and cellular retinoicacid binding protein(CRABP).Next to known function proteins,one was identified asunannotated proteins.The modulated proteins were found to fall into the following functionalgroups:humoral or cellular immunity,detoxification,energy metabolism,and others.Degenerate primers designed based on peptides obtained from mass spectral analysis were usedfor PCR amplification of the fragment of the differential expressed proteins.And their fulllength eDNA were derived from RACE amplification.The gene of MasSPH,ENO and BBPwere cloned and sequenced.RT-PCR analysis indicated that parasitization by P.puparuminduced increased transcripts of MasSPH and BBP,and had no apparent impact on the level ofIDGF and ENO transcripts in the fat body of P.rapae pupae.
(2)cDNA of an arylphorin-type storage protein from P.rapae with parasitisminducible expression by P.puparum.The cDNA of a storage protein,PraAry,from P.rapaewas cloned and its expression regulated by parasitization of P.puparum was investigated.Thefull-length cDNA of PraAry was 2270 nucleotides and contains a 2121 bp open reading frameencoding 707 amino acids with calculated molecular weights of approximately 83 kDa.Analysisof the primary protein sequence revealed that it possesses a signal peptide of 16 amino acids atthe N-terminus and contains two highly conserved storage protein signature motifs.Accordingto both phylogenetic analysis and the criteria for amino acid composition,PraAry belongs to thesubfamily of arylphorin-type storage protein(1.42% methionine and 18.82% aromatic aminoacids).RT-PCR analysis indicated that the transcriptional level of PraAry mRNA in P.rapaepupae fat body is inducible upregulation in response to parasitization by P.puparum.
(3)Transcriptional changes of calreticulin from P.rapae after parasitization by P.puparum.The cDNA of calreticulin from P.rapae was cloned and its expression regulated byparasitization of P.puparum was investigated.Sequence analysis showed that P.rapaecalreticulin was of 1816 bp in full length contained an 1194 bp open reading frame whichpredicted a 398 amino acid protein.The calculated molecular mass and pI were 45.75 kDa and4.4,respectively.The deduced amino acid sequence contained N,P and C domains with special characters similar to that of other species,sharing 74%,70% and 69% homology with thecounterparts of A.mellifera,Anopheles gambiae and D.melanogaster.Expression analyses ofthe calreticulin gene in the haemocyte of P.rapae pupae parasitized and unparasitized by P.puparum were performed by RT-PCR,which indicated down regulated transcription underparasitization.
(4)Transcriptional changes of cytoskeleton related proteins of P.rapae afterparasitization by the endoparasitoid wasp P.puparum.The cDNA of actin,actindepolymerisation factor and tubulin from P.rapae was cloned and their expression regulated byparasitization of P.puparum was investigated.P.rapae actin contained an open reading frameof 1131 bp encoding for 377 amino acid residues with predicted molecular mass and pI of 41.78kDa and 5.29,respectively.The homology of P.rapae actin with other insect actin genes wasgreater than 90% in amino acids.P.rapae actin was classified as a cytoplasmic type by absenceof muscle-specific amino acids and phylogenetic tree analysis.The 1243 bp cDNA sequence ofP.rapae actin depolymerisation factor contained an open reading frame of 447 bp encoding anneutral(pI 7.11)protein of 149 amino acids predicted molecular mass of 16.97 kDa,sharing97%,87%,89% and 72% homology with the counterparts of Bombyx mori,T.castaneum,A.mellifera and Maconellicoccus hirsutus.Nucleotide sequence analysis of P.rapae tubulinshowed full length cDNA of 1757 bp with open reading frames of 1344 bp encoding proteins of448 amino acids with a predicted molecular weight and pI of 50.38 kDa and 4.86,respectively.The cDNA-deduced amino acid sequence of P.rapae tubulin showed 97%,97%,87% and 93%homology with that of B.mori beta-tubulin 1,2,3 and 4.P.rapae tubulin was classified as betatype by phylogenetic evolution analysis.RT-PCR analysis showed that P.rapae actin,actindepolymerisation factor and tubulin gene were affected by P.puparum parasitization indicatingdecreased expression.
(5)Endocrine changes in the hemolymph ofP.rapae indiced by venom of P.puparum.The changes of hemolymph juvenile hormone(JH)(only JHⅢdetected),ecdysteroid andjuvenile hormone esterase activity(JHE)over 72 h in parasitized and venom microinjected P.rapae pupae were monitored.Non-parasisized and PBS microinjected P.rapae served ascontrols.Results showed that JH titers were significant higher in parasitized and venommicroinjected pupae than that in control pupae during 24 to 72 h.After 12 h,JH titers weresignificantly promoted by parasitization and venom microinjection.JHE activities ofnon-parasitized and PBS microinjected pupae were significant higher than that of parasitizedand venom microinjected which was with a peak at 12 h(parasitized pupae)or 24 h(venommicroinjected pupae)during 6 to 48 and 12 to 36 h respectively.The hemolymph titers of ecdysteroid in non-parasitized and PBS microinjected pupae increased rapidly during 12 to 36 hwith a peak at 36 h,and were higher than treatments before 48 h,while presenting significantdifference at 24 to 48 h between the treatments and controls.The results demonstrate that venomalone of this parasitoid wasp can disrupt its host's endocrine system.
(6)Proteome changes in the plasma of Papilio xuthus induced by P.puparumparasitization.By examining the differential expression of plasma proteins in the parasitizedand non-parasitized hosts pupae after 24 h by two-dimensional electrophoresis,16 proteins werefound to vary in relation to parasitization compared to unparasitized control samples.Among ofthem,8 proteins were elevated,5 showed decreased expression,and 1 disappeared,and 2 newlyoccurred after parasitization.All of them were submitted to identification by mass spectrometrycoupled with a database search.The modulated proteins were found to fall into the followingfunctional groups:humoral or cellular immunity,detoxification,energy metabolism,and others.
In this paper,the microstructure and ultrastructure of venom apparatus of P.puparum wasclearly defined.The venom proteins of calreticulin,arginine kinase,serine protease,heat shockprotein 70,acid phosphatase and alkaline phosphatase were firtly identified from the venom ofpupal stage specific parasitoid or parasitoid belonging to Pteromalidae.The cDNA encodingvenom calreticulin,arginine kinase,acid phosphatase and alkaline phosphatase genes werecloned and sequenced,and the tissue location,biochemical characters and time-course relatedgene expression of acid and alkaline phosphatase were defined,which provided the firstevidence for the detail investigation of parasitoid venom acid and alkaline phosphatase.A novelpathogenic small RNA virus belonged to the Cripavirus genus of Dicistroviridae was reportedfrom the parasitoid.The results first revealed that the parasitization by the parasitoid onlyassociated with venom induced the proteins in the host plasma related to humoral or cellularimmunity,detoxification,energy metabolism differentially expressed,the the transcription ofnutrition metabolism related arylphorin-type storage protein gene up regulated,and thetranscription of cellular immune related calreticulin,actin,actin depolymerisation factor andtubulin genes decreased.In addition,the results firstly demonstrated that venom alone ofparasitoid can disrupted its host's endocrine system.These results not only revealed themolecular mechanisms of the interaction between parasitoid and host to a large extent,but alsomade a great contribution to gain insights into exploiting parasitoid venom for insect control.
引文
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