家蚕“明”死卵突变体l-e~m基因的定位克隆及功能研究
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摘要
家蚕是一种完全变态昆虫，以卵滞育，可以说卵是家蚕生命周期中的第一个发育阶段，蚕卵品质的好坏直接影响到幼虫、蛹和成虫的发育。正常卵通常呈短椭圆形、侧面扁平且有轻微凹陷。本课题研究对象“明”死卵突变体（lethal egg of“ming”, l-em）是在实用品种“苏·菊×明·虎”母本品系“明”的生产和保存过程中发现的一种死卵突变体，在产卵后一小时左右出现三角形凹陷，表现失水死亡特征；遗传分析发现该突变由一对隐性基因控制，纯合致死，遵循伪母性遗传规律；扫描电镜观察突变体卵壳，发现卵壳表面凹陷处小室的边缘有明显的裂纹，卵壳纵断面中间层亦出现不连续的裂缝。本研究在对l-em卵突变体遗传分析及表型观察的基础上，采用图位克隆技术对l-em基因进行了定位克隆，采用qRT-PCR、2-DE、RNAi等技术对候选基因进行表达分析和功能验证。主要研究结果如下：
一、l-em基因的定位
选择l-em卵突变体隐性纯合的雄性亲本（P1）与p50近交系的雌性亲本（P2）杂交，组配F1代群体；F1代雌性个体与雄性亲本（P1）回交，同时进行蛾区内自交分别组配BC1F群体及F2代群体。使用P1、P2和F1筛选了28个连锁群上具有多态性的SSR分子标记，并使用BC1F群体确定了l-em基因位于家蚕第十连锁群；进一步对2287个F2代群体中产死卵的雌性个体检测，使用13个与l-em基因连锁的具有多态性的SSR标记，将l-em基因定位于S65与S82两个标记之间，相距约360kb，绘制出l-em基因的分子标记遗传连锁图谱；通过与家蚕基因组比对查明该区域内包含24个基因。
二、候选基因的表达模式、基因结构分析和功能验证
通过对24个基因在正常蛾及l-em卵突变体蛾卵巢内的表达分析，明确了2个差异表达基因BmVMP23和BmEP80为候选基因。BmVMP23基因的表达量在l-em卵突变体的卵巢中出现明显下调，而在l-em卵突变体的卵巢中则未检测到BmEP80基因的表达。
反向PCR分析测序显示BmVMP23基因终止密码子后的第22个碱基至BmEP80基因ORF的第161个碱基间发生了突变，导致BmVMP23基因的3′-UTR和BmEP80基因结构的不完整性。
对2个候选基因的RNAi试验表明，经BmEP80基因干扰后的部分雌蛾所产卵发生明显的凹陷，且表型与l-em卵突变体所产卵的表型相似，而对BmVMP23基因干扰未见此现象。因而推断BmEP80基因的突变是导致l-em卵突变体产生的主要原因。
三、l-em突变体卵巢组织差异蛋白质分析
通过双向电泳技术对正常个体及l-em卵突变体的卵巢组织进行蛋白质组学分析，结果显示BmEP80基因所编码的BmEP80蛋白从蛹期第九天开始在正常个体卵巢中大量表达，而在l-em卵突变体的卵巢中则未检测到该蛋白的表达。除了BmEP80蛋白之外的其他蛋白在正常个体和l-em卵突变体之间无明显差异。进一步说明了BmEP80蛋白的缺失是l-em卵突变体产生的主要原因。
四、候选基因BmVMP23的表达调控分析
鉴于l-em卵突变体的BmVMP23基因的3′-UTR结构被破坏，而3′-UTR为miRNAs的调控位点，为了分析miRNA对BmVMP23基因的表达调控作用，将BmVMP23基因的3′-UTR序列与家蚕的miRNAs序列比对，发现了一个与BmVMP23基因的3′-UTR序列匹配度极高的miRNA（bmo-miR-1a-3p）。荧光实时定量检测该miRNA在正常个体卵巢中表达量较高，且其表达趋势与BmVMP23基因的表达趋势相反，而在l-em卵突变体卵巢中仅有微量表达。通过miRNAmimic过表达和miRNA inhibitor抑制表达体外转染实验证实了bmo-miR-1a-3p能够抑制BmVMP23基因的表达。
上述研究证实了卵黄膜蛋白BmEP80基因的突变是导致l-em卵突变体产生的主要原因，该研究为“明”死卵基因突变的分子机制的阐明提供了重要的理论依据，具有重要的科学意义和价值。
The silkworm is a complete metamorphosis insect and diapaused in egg stage. Eggstage is the first and an important stage of the silkworm (Bombyx mori) life cycle, andthe quality of the silkworm eggs has a direct impact on the development of larvae,pupae and moth. The normal eggs are usually short and elliptic, flattened laterally, thesurface of the lateral side is sometimes hollowed. The object of this study (“Ming”lethal egg mutants, l-em) is a lethal egg of mutant which was found in “ming” duingthe production and preservation of “su·ju×ming·hu”. The eggs laid by l-emmutant lostwater and became concaved around one hour, ultimately exhibiting a triangular shapeon the egg surfaces. Genetic analysis showed that the l-emmutation is dominated by arecessive gene and followed the pseudo-maternal inherited mode, and the hollowplace of surface have obvious rhagades and the cross section have cracks were foundin dead eggs using the scanning electron microscope.
In the present study, we performed positional cloning using map-based cloningbased on the phenotypic observation and genetic analysis. Expression analysis andfunctional verification of candidate genes were performed by using qRT-PCR,2-DE,RNAi. The results of the study are as follows.
1. Positional cloning of the l-emgene
The male parent (P1) and the female parent (P2) were selected from thehomozygous recessive individuals and inbred line of p50, respectively. Both of themwere used as parent strains for the mapping panel and a single-pair cross between p50and l-emmutant produced the F1offspring. The female individuals of F1offspringwere used for selfing and back-crossing with P1to produce F2and BC1F progeny. Thepolymorphic SSR markers of28linkage groups were selected using P1, P2and F1, andconfirmed the l-emgene located on the10thlinkage group using BC1F progeny. Thegenetic linkage map of the l-emgene was constructed using2,287F2femaleindividuals which laid dead eggs and13polymorphic SSR markers which linked withthe l-emgene, and a region of~360kb tightly linked to the l-emgene between themarkers S65and S82was identified.24genes within this locus were predicted byusing gene-prediction models.
2. Expression models, gene structures and functional verification of thecandidate genes
Two differentially expressed genes (BmVMP23and BmEP80) were identified ascandidate genes through investigating the expression level of the24initial candidategenes in the eggs laid by virgin WT and l-emmutant moths. The results showed thatthe expression level of BmVMP23gene in l-emmutant was much lower than inwild-type, while BmEP80gene did not express in ovaries of the l-emmutantcompletely. The results of inverse PCR showed that the mutation was located betweenthe3′-UTR of BmVMP23and the forepart of BmEP80, and destroyed the structuralintegrity of the two genes.
The results of the RNAi showed that the eggs laid by the individuals treated withBmEP80siRNAs appeared with a triangular shape on the egg surface, consistent withthe l-emmutation. However, the eggs laid by all individuals treated with BmVMP23siRNAs did not appear this phenomenon. So we concluded that BmEP80was mostlikely the gene causing the l-emmutation.
3. Differential expression of the ovary proteins between WT and l-emmutant
2-DE was used to investigate the differential expression of the egg proteins betweenthe WT and l-emmutant, and the result showed that the BmEP80protein wasexpressed in the ovary from the9thday of the pupal stage of the WT, but not wasexpressed at all in the ovary of the l-emmutant. However, there was no difference ofthe other proteins between the WT and l-emmutant except the BmEP80protein. Thisresult further indicated that the the defection of BmEP80resulted in the termination ofBmEP80protein expression, thereby triggering the l-emmutation.
4. Analysis the expression regulation of the candidate gene BmVMP23
The results of the sequence analysis have shown that the3′-UTR of BmVMP23wasdestroyed, and3′-UTR is an important regulatory site of the microRNAs. Toinvestigate the relationship between the miRNAs and the expression of BmVMP23,we downloaded all the known miRNAs of the silkworm and performed a BLASTsearch for the3′-UTR (WT) sequence of BmVMP23, and found a miRNA(bmo-miR-1a-3p) that highly matched the3′-UTR (WT) sequence of BmVMP23.
The results of the qRT-PCR indicated that the expression level ofbmo-miR-1a-3p in the ovaries of WT was higher than that in the l-emmutant, and the expression level was contrary to the expression level of BmVMP23. We confirmedthat the bmo-miR-1a-3p can inhibit the expression of BmVMP23through transfectionin vitro.
The above results confirmed that the mutation of BmEP80is responsible for thel-emmutant. This study laid a foundation for further study of the formationmechanism of the l-emmutant. It has an important scientific significance and value.
一、l-em基因的定位
选择l-em卵突变体隐性纯合的雄性亲本（P1）与p50近交系的雌性亲本（P2）杂交，组配F1代群体；F1代雌性个体与雄性亲本（P1）回交，同时进行蛾区内自交分别组配BC1F群体及F2代群体。使用P1、P2和F1筛选了28个连锁群上具有多态性的SSR分子标记，并使用BC1F群体确定了l-em基因位于家蚕第十连锁群；进一步对2287个F2代群体中产死卵的雌性个体检测，使用13个与l-em基因连锁的具有多态性的SSR标记，将l-em基因定位于S65与S82两个标记之间，相距约360kb，绘制出l-em基因的分子标记遗传连锁图谱；通过与家蚕基因组比对查明该区域内包含24个基因。
二、候选基因的表达模式、基因结构分析和功能验证
通过对24个基因在正常蛾及l-em卵突变体蛾卵巢内的表达分析，明确了2个差异表达基因BmVMP23和BmEP80为候选基因。BmVMP23基因的表达量在l-em卵突变体的卵巢中出现明显下调，而在l-em卵突变体的卵巢中则未检测到BmEP80基因的表达。
反向PCR分析测序显示BmVMP23基因终止密码子后的第22个碱基至BmEP80基因ORF的第161个碱基间发生了突变，导致BmVMP23基因的3′-UTR和BmEP80基因结构的不完整性。
对2个候选基因的RNAi试验表明，经BmEP80基因干扰后的部分雌蛾所产卵发生明显的凹陷，且表型与l-em卵突变体所产卵的表型相似，而对BmVMP23基因干扰未见此现象。因而推断BmEP80基因的突变是导致l-em卵突变体产生的主要原因。
三、l-em突变体卵巢组织差异蛋白质分析
通过双向电泳技术对正常个体及l-em卵突变体的卵巢组织进行蛋白质组学分析，结果显示BmEP80基因所编码的BmEP80蛋白从蛹期第九天开始在正常个体卵巢中大量表达，而在l-em卵突变体的卵巢中则未检测到该蛋白的表达。除了BmEP80蛋白之外的其他蛋白在正常个体和l-em卵突变体之间无明显差异。进一步说明了BmEP80蛋白的缺失是l-em卵突变体产生的主要原因。
四、候选基因BmVMP23的表达调控分析
鉴于l-em卵突变体的BmVMP23基因的3′-UTR结构被破坏，而3′-UTR为miRNAs的调控位点，为了分析miRNA对BmVMP23基因的表达调控作用，将BmVMP23基因的3′-UTR序列与家蚕的miRNAs序列比对，发现了一个与BmVMP23基因的3′-UTR序列匹配度极高的miRNA（bmo-miR-1a-3p）。荧光实时定量检测该miRNA在正常个体卵巢中表达量较高，且其表达趋势与BmVMP23基因的表达趋势相反，而在l-em卵突变体卵巢中仅有微量表达。通过miRNAmimic过表达和miRNA inhibitor抑制表达体外转染实验证实了bmo-miR-1a-3p能够抑制BmVMP23基因的表达。
上述研究证实了卵黄膜蛋白BmEP80基因的突变是导致l-em卵突变体产生的主要原因，该研究为“明”死卵基因突变的分子机制的阐明提供了重要的理论依据，具有重要的科学意义和价值。
The silkworm is a complete metamorphosis insect and diapaused in egg stage. Eggstage is the first and an important stage of the silkworm (Bombyx mori) life cycle, andthe quality of the silkworm eggs has a direct impact on the development of larvae,pupae and moth. The normal eggs are usually short and elliptic, flattened laterally, thesurface of the lateral side is sometimes hollowed. The object of this study (“Ming”lethal egg mutants, l-em) is a lethal egg of mutant which was found in “ming” duingthe production and preservation of “su·ju×ming·hu”. The eggs laid by l-emmutant lostwater and became concaved around one hour, ultimately exhibiting a triangular shapeon the egg surfaces. Genetic analysis showed that the l-emmutation is dominated by arecessive gene and followed the pseudo-maternal inherited mode, and the hollowplace of surface have obvious rhagades and the cross section have cracks were foundin dead eggs using the scanning electron microscope.
In the present study, we performed positional cloning using map-based cloningbased on the phenotypic observation and genetic analysis. Expression analysis andfunctional verification of candidate genes were performed by using qRT-PCR,2-DE,RNAi. The results of the study are as follows.
1. Positional cloning of the l-emgene
The male parent (P1) and the female parent (P2) were selected from thehomozygous recessive individuals and inbred line of p50, respectively. Both of themwere used as parent strains for the mapping panel and a single-pair cross between p50and l-emmutant produced the F1offspring. The female individuals of F1offspringwere used for selfing and back-crossing with P1to produce F2and BC1F progeny. Thepolymorphic SSR markers of28linkage groups were selected using P1, P2and F1, andconfirmed the l-emgene located on the10thlinkage group using BC1F progeny. Thegenetic linkage map of the l-emgene was constructed using2,287F2femaleindividuals which laid dead eggs and13polymorphic SSR markers which linked withthe l-emgene, and a region of~360kb tightly linked to the l-emgene between themarkers S65and S82was identified.24genes within this locus were predicted byusing gene-prediction models.
2. Expression models, gene structures and functional verification of thecandidate genes
Two differentially expressed genes (BmVMP23and BmEP80) were identified ascandidate genes through investigating the expression level of the24initial candidategenes in the eggs laid by virgin WT and l-emmutant moths. The results showed thatthe expression level of BmVMP23gene in l-emmutant was much lower than inwild-type, while BmEP80gene did not express in ovaries of the l-emmutantcompletely. The results of inverse PCR showed that the mutation was located betweenthe3′-UTR of BmVMP23and the forepart of BmEP80, and destroyed the structuralintegrity of the two genes.
The results of the RNAi showed that the eggs laid by the individuals treated withBmEP80siRNAs appeared with a triangular shape on the egg surface, consistent withthe l-emmutation. However, the eggs laid by all individuals treated with BmVMP23siRNAs did not appear this phenomenon. So we concluded that BmEP80was mostlikely the gene causing the l-emmutation.
3. Differential expression of the ovary proteins between WT and l-emmutant
2-DE was used to investigate the differential expression of the egg proteins betweenthe WT and l-emmutant, and the result showed that the BmEP80protein wasexpressed in the ovary from the9thday of the pupal stage of the WT, but not wasexpressed at all in the ovary of the l-emmutant. However, there was no difference ofthe other proteins between the WT and l-emmutant except the BmEP80protein. Thisresult further indicated that the the defection of BmEP80resulted in the termination ofBmEP80protein expression, thereby triggering the l-emmutation.
4. Analysis the expression regulation of the candidate gene BmVMP23
The results of the sequence analysis have shown that the3′-UTR of BmVMP23wasdestroyed, and3′-UTR is an important regulatory site of the microRNAs. Toinvestigate the relationship between the miRNAs and the expression of BmVMP23,we downloaded all the known miRNAs of the silkworm and performed a BLASTsearch for the3′-UTR (WT) sequence of BmVMP23, and found a miRNA(bmo-miR-1a-3p) that highly matched the3′-UTR (WT) sequence of BmVMP23.
The results of the qRT-PCR indicated that the expression level ofbmo-miR-1a-3p in the ovaries of WT was higher than that in the l-emmutant, and the expression level was contrary to the expression level of BmVMP23. We confirmedthat the bmo-miR-1a-3p can inhibit the expression of BmVMP23through transfectionin vitro.
The above results confirmed that the mutation of BmEP80is responsible for thel-emmutant. This study laid a foundation for further study of the formationmechanism of the l-emmutant. It has an important scientific significance and value.
引文
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