人工合成抗菌肽抑制棉花黄萎病菌的机制及应用研究
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摘要
我国是全球最大的棉花生产国,同时也是最大的消费国。棉花的生产和创收对于我国的国民经济意义重大。然而根据国家统计局提供的数据,2010年全国棉花的总产量(596.1万吨)和单产(1229k/ha)均为近五年来最低。除去人力不可控的气候灾害的影响,棉花病害的发生是限制单产的主要因子。本研究的对象就是危害棉花最严重病害之一——黄萎病,该病是海关出入境的检验检疫对象,困扰棉花产业几十年,一直未找到理想的防治对策。植物转基因抗病育种技术的不断发展,为棉花黄萎病的攻克开辟了新的途径,国内外不少学者也进行了相关的尝试。遗憾的是,截止到目前仍然没有一个抗病的转基因株系转化为品种。究其原因应该是转化的外源抗病基因不够理想,不能像苏云金芽孢杆菌内毒素基因(BT)那样强效。因此,分离和发现高效抗病的外源基因成为当前转基因抗黄萎病棉花品种选育工作中亟需解决的问题。
为此,本文以长江和黄河流域棉花两大主产区的15种黄萎病菌为材料,精心设计并合成了20条不同类型的抗真菌多肽,通过分析抗菌肽与不同黄萎病菌、抗菌肽与动物细胞、抗菌肽与棉花原生质体间的互作,筛选出能高效抑杀黄萎病菌、低毒性的小分子多肽；探讨了抗菌肽抑制黄萎病菌的可能作用机制和在大肠杆菌生物反应器中原核表达该多肽的可行性。研究的主要结果如下：
1.对来自长江和黄河流域两大主产棉区的15种黄萎病菌的地方小种进行了系统研究,首先,通过菌落形态学观察将不同的菌系按照其菌丝和微菌核的相对生长量分别划分到菌丝型、菌核型和中间型,为直观地初步判定不同地方小种奠定了基础；其次,利用4对特异引物对上述病菌材料进行了PCR分子鉴定,发现除枯萎病菌对照外,其他供试菌种均为大丽轮枝菌,并且部分为强致病力的落叶型菌系。苗期接种试验表明,黄萎病菌可能的致病因子——毒素(蛋白-脂-多糖复合物)对棉苗有明显的致萎活性,通过进一步比较试验发现,棉苗的抗氧化酶系统对毒素和分生孢子液的响应模式存在明显的差异,毒素处理后棉苗的反应更加迅速(特别是根部),同一处理的不同器官内的防御酶活性变化也不相同。
2.采用温室鉴定和病圃鉴定相结合的方法,观察了黄萎病菌在棉花上的发生与危害情况,并对本课题组现有的三系杂交棉材料进行了为期2年的调查鉴定。其中,2007年8月份30℃以上的月均温度以及同期较高的旬均温度导致田间发生了黄萎病隐症的情况,直到8月底才出现较高的病情指数。2008年田间病田的发病比较严重(同期温度较2007年低很多,雨水足,适宜发病)。比较不同时期、不同材料的田间发病规律,结论是未发现免疫水平的材料。本试验用到的16个三系杂交棉材料可以划分为4个类群,海岛棉恢复系具有高抗特性,鸡脚叶恢复系和对照“湘杂棉2号”为高感病,其他多数材料均为耐病性或介于耐病与感病之间。相关性分析结果表明,各三系材料最终产量和纤维品质的表现与黄萎病的发病程度相关显著。陆地棉杂交种和海陆杂种F1组合的各项指标均有所改良,但未表现出明显的杂种优势。
3.收集国内外各种数据库和文献报道的抗菌肽序列1500多条,找出有抗真菌特性的600条,最终选定20条为母体肽,分别利用不同的抗菌肽修饰手段,对母体肽进行加工修饰,保留其保守的抗菌核心区(或氨基酸残基),得到新型的潜在抗黄萎病菌多肽20条,体外人工合成后进行抑菌试验。结果表明,不同的抗菌肽对黄萎病菌的作用差异很大,同一抗菌肽对不同的黄萎病菌小种之间也存在差异。经过筛选得到抗菌肽0-防御素类BTD-S和杂合肽CM-S可以分别抑制全部5种或其中4种供试黄萎病菌,并且最小抑菌浓度均在5μM以下,二者均表现了很强的抑菌能力,比目前研究利用最成熟的多肽D4E1效果好(MIC=9.61μM),而且抑菌力更持久。分别用绵羊血红细胞和棉花原生质体为材料,对BTD-S和CM-S的生物安全性进行了评定,结果表明,二者仅在浓度达到200μg/ml时才会出现轻微的溶血性,对棉花原生质体在200μg/ml时未发现毒害性。
4.通过生物信息学分析得出BTD-S为β-折叠肽,CM-S为α-螺旋肽。随后利用圆二色谱技术测定了2种多肽分子的二级结构,BTD-S在远紫外区的CD谱特征为195nm处正峰,205nm处负峰,为典型的β-折叠构象；CM-S则在190nm处正峰,222nm和208nm处出现明显的负峰,为α-螺旋构象,试验测定的数据与软件预测的结果完全一致。抗菌肽的高级结构分析表明,BTD-S分子内6个半胱氨酸结合为3对二硫键,呈梯状,整条多肽结构非常稳定,为其持久杀菌特性提供了可能；CM-S为α-螺旋,带7个净正电荷,分子具有两亲特性(有明显的疏水表面),这些特质使其更容易通过膜作用机制抑菌。
5.在普通光学显微镜下发现,20μg/ml抗菌肽的处理会导致病菌分生孢子无法正常萌发,并出现部分小号细胞群体；利用荧光显微技术观察发现抗菌肽处理的真菌孢子细胞膜受到严重损伤,大分子碘化丙啶(P1)渗入病菌细胞内部,细胞核被染色,经荧光激发显红色；扫描电镜(SEM)观察抗菌肽对细胞形态的影响,BTD-S处理后真菌孢子不能萌发,细胞表面出现明显的外渗物,甚至发生细胞的破裂和解体,CM-S处理后也见到类似的现象,由此可见,BTD-S和CM-S都能与病原真菌细胞膜互作,改变膜的透性,进而使细胞内必需物质外渗。流式细胞仪分析表明,BTD-S处理会使病菌细胞群体中逐渐分化出一批小号细胞,并且随着BTD-S浓度的增加,该类小号细胞的群体呈明显扩大趋势,这一结果与光学镜下的发现相吻合；另一方面随着BTD-S处理剂量的加大,病菌细胞对PI的吸收显著增强,即细胞受损伤(或死亡)程度逐渐加重。
6.根据BTD-S的氨基酸序列反译为DNA序列,将编码DNA序列插入到原核表达载体pET32a,构建了重组表达载体BTD-pET32a。在IPTG诱导下,检测到目的蛋白明显地过量表达,并且融合蛋白主要以可溶性形式表达,镍柱纯化可得到高纯度的目标蛋白。
Cotton production occupies a central position in national economy of China contributed from agriculture sector. According to the data provided by the National Bureau of Statistics of China, the average yield (1229kg/ha) of cotton from2010is declined as compared to last five years. This reduction in the cotton yield is mainly due to the occurrence of a devasting pathogen Verticillium dahliae in cotton growing areas and caused a severe disease known as Verticillium wilt. For so long time, scientists are engaged for identifying resistant resources against this pathogen but could not find any one in commercially grown tetraploid cotton(Gossypium hirsutum). However biotechnology and genetic engineering as new emerging sciences set up new avenues for combating Verticillium wilt in cotton by transferring resistant genes from sources other than plants.
Yangtze River and Yellow River are the two main cotton growing areas in China. About15different isolates of Verticillium dahliae, were collected from these two places and maintained in our laboratory for future work. The isolates were characterized into hyphae, sclerotia and intermediate-type on the basis of colony morphology. Further molecular identification of these isolates using four pairs of specific primers indicated that, except Fusarium oxysporum and Zhengzhou strain of Verticillium dahliae, all the other tested strains belong to Verticillium daliae including some virulent defoliating strains. To understand the interaction between cotton and Verticillium dahliae, seedling bioassays were performed using VD(Verticillium dahliae) toxin (protein-lipids-polysaccharide complexes, PLPs) and spore suspension following root dip method. The VD-toxin caused the cotton seedlings to wilt immediately while symptoms appearance with spore suspension was little delayed. Moreover, antioxidant activity in different organs of the same treatment was not the same.
In addition to greenhouse screening, field screening against Verticillium dahliae was also during2007and2008conducted using16CMS-based hybrid cotton developed by our lab. In august2007, monthly average temperature was above30℃and no wilting was recorded. However at the end of august the high disease index was observed. Whereas in2008due to low temperature and frequent rainfall, which are suitable factors for the growth of Verticillium dahliae, the incidence of field disease reached at peak in August. Moreover at different time period, cotton materials exhibited different disease index for Verticillium wilt and according to their performance,16CMS-based hybrid cotton can be divided into four groups, highly resistant sea island cotton restorer line, highly susceptible chicken leaf recovery line and 'Xiangzamian2'while other materials were either tolerant to disease or between tolerant and susceptible. The correlation analysis results showed that the final yield and fiber quality performance of the CMS-based materials were significantly correlated with the disease severity. In order to utilize the phenomenon of heterosis, F1intraspecific hybrids of upland cotton and interspecific hybrids between sea and upland cotton were developed. Hybrids though exhibited some resistance but it was not as high as that of sea iseland cotton.
From already available database having more than1500antimicrobial peptide sequences,600were identified to possess antifungal properties. Out of these, finally20different types of anti-fungal peptides were selected as a parent peptide and modified for high resistance against Verticillium dahliae and low toxicity to other organisms. However, their conservative antibacterial core domain (or amino acid residues) was retained. The interaction of these antimicrobial peptides with fungal, animal, bacterial cells and cotton protoplast was studied. Results revealed that these antimicrobial peptides efficiently inhibited the growth of Verticillium dahliae, low toxicity to animal red blood cells and cotton protoplast. The interaction between fungus isolate and antimicrobial peptide was highly significant and0-defensin BTD-S can inhibit five different isolates while hybrid peptide CM-S can inhibit four kinds of Verticillium dahliae. The minimum inhibitory concentration (MIC) for these two peptides was less than5μM and possessed stronger antimicrobial activity as compared to synthetic peptide D4E1(MIC=9.61μM). No hemolytic activities were observed to sheep red blood cells and cotton protoplast even at concentration level up to200μg/ml. These qualities make these two antimicrobial peptides more demanding for using them in developing wilt resistant cultivars.
Circular dichroism (CD) spectra of BTD-S in the far UV wavelength displayed a characteristic positive peak is195nm and205nm negative peak, indicating a typical β-sheet conformation of BTD-S. Similarly a positive peak at190nm and the negative peak at222nm and208nm for CM-S indicated a a-helix conformation and match well with the prediction from bioinformatics softwares. The advanced structural analysis of antimicrobial peptides showed that the six cysteins amino acid residues within the molecule of the BTD-S formed three disulfide bonds (like a ladder) making it more stable with durable microbicidal properties. Wherease CM-S with a-helix structure having seven net positive charge and amphiphilic properties (hydrophobic surface) make it easier to interact with the membrane of Verticillium dahliae.
Under the optical microscope, antimicrobial peptides concentration (20μg/ml) leads to the significant inhibition of conidial germination. Cell membrane permeation of fungal spores was also observed using fluorescence microscopy technique and severe cell injury was observed in response to treatment with antimicrobial peptides. This injury can be visualized from permeation of large molecules of propidium iodide (PI) into the fungus cells which then stained the nucleus and emitted red fluorescence after excitation. Similarly scanning electron microscopy (SEM) also revealed retarded growth of fungal spores with some extravasations on the cell surface and rupturing of the cell. Whereas flow cytometric analysis (FCA) showed that BTD-S treatment differentiated fungal cells into a new group of small sized cells (mini cells) and their number increased continuosly upon increasing the concentration of the BTD-S. These findings were inconsistent to that of optical microscopy, florescence microscopy and scanning electron microscopy. Therefore it can be concluded from this study that the BTD-S and CM-S interacted with pathogenic fungal cell membranes, changed the membrane permeability and thus disturbing the normal metabolism of the cells.
Using bioinformatics tools, amino acid sequence of the BTD-S was translated into coding nucleotide sequence and then inserted into the prokaryotic expression vector pET32a to construct the recombinant expression vector of the BTD-pET32a. This recombinant vector was then transferred into Escherichia coli BL21(DE3) and after IPTG induction a significant overexpression of the target protein was detected. The study provided a comprehend mechanisim of antimicrobial peptide interaction with Verticillium dahliae and laid a basis for utilizing the coding sequences of these peptides to transfer into cotton for developing transgenic wilt resistant cultivars.
为此,本文以长江和黄河流域棉花两大主产区的15种黄萎病菌为材料,精心设计并合成了20条不同类型的抗真菌多肽,通过分析抗菌肽与不同黄萎病菌、抗菌肽与动物细胞、抗菌肽与棉花原生质体间的互作,筛选出能高效抑杀黄萎病菌、低毒性的小分子多肽；探讨了抗菌肽抑制黄萎病菌的可能作用机制和在大肠杆菌生物反应器中原核表达该多肽的可行性。研究的主要结果如下：
1.对来自长江和黄河流域两大主产棉区的15种黄萎病菌的地方小种进行了系统研究,首先,通过菌落形态学观察将不同的菌系按照其菌丝和微菌核的相对生长量分别划分到菌丝型、菌核型和中间型,为直观地初步判定不同地方小种奠定了基础；其次,利用4对特异引物对上述病菌材料进行了PCR分子鉴定,发现除枯萎病菌对照外,其他供试菌种均为大丽轮枝菌,并且部分为强致病力的落叶型菌系。苗期接种试验表明,黄萎病菌可能的致病因子——毒素(蛋白-脂-多糖复合物)对棉苗有明显的致萎活性,通过进一步比较试验发现,棉苗的抗氧化酶系统对毒素和分生孢子液的响应模式存在明显的差异,毒素处理后棉苗的反应更加迅速(特别是根部),同一处理的不同器官内的防御酶活性变化也不相同。
2.采用温室鉴定和病圃鉴定相结合的方法,观察了黄萎病菌在棉花上的发生与危害情况,并对本课题组现有的三系杂交棉材料进行了为期2年的调查鉴定。其中,2007年8月份30℃以上的月均温度以及同期较高的旬均温度导致田间发生了黄萎病隐症的情况,直到8月底才出现较高的病情指数。2008年田间病田的发病比较严重(同期温度较2007年低很多,雨水足,适宜发病)。比较不同时期、不同材料的田间发病规律,结论是未发现免疫水平的材料。本试验用到的16个三系杂交棉材料可以划分为4个类群,海岛棉恢复系具有高抗特性,鸡脚叶恢复系和对照“湘杂棉2号”为高感病,其他多数材料均为耐病性或介于耐病与感病之间。相关性分析结果表明,各三系材料最终产量和纤维品质的表现与黄萎病的发病程度相关显著。陆地棉杂交种和海陆杂种F1组合的各项指标均有所改良,但未表现出明显的杂种优势。
3.收集国内外各种数据库和文献报道的抗菌肽序列1500多条,找出有抗真菌特性的600条,最终选定20条为母体肽,分别利用不同的抗菌肽修饰手段,对母体肽进行加工修饰,保留其保守的抗菌核心区(或氨基酸残基),得到新型的潜在抗黄萎病菌多肽20条,体外人工合成后进行抑菌试验。结果表明,不同的抗菌肽对黄萎病菌的作用差异很大,同一抗菌肽对不同的黄萎病菌小种之间也存在差异。经过筛选得到抗菌肽0-防御素类BTD-S和杂合肽CM-S可以分别抑制全部5种或其中4种供试黄萎病菌,并且最小抑菌浓度均在5μM以下,二者均表现了很强的抑菌能力,比目前研究利用最成熟的多肽D4E1效果好(MIC=9.61μM),而且抑菌力更持久。分别用绵羊血红细胞和棉花原生质体为材料,对BTD-S和CM-S的生物安全性进行了评定,结果表明,二者仅在浓度达到200μg/ml时才会出现轻微的溶血性,对棉花原生质体在200μg/ml时未发现毒害性。
4.通过生物信息学分析得出BTD-S为β-折叠肽,CM-S为α-螺旋肽。随后利用圆二色谱技术测定了2种多肽分子的二级结构,BTD-S在远紫外区的CD谱特征为195nm处正峰,205nm处负峰,为典型的β-折叠构象；CM-S则在190nm处正峰,222nm和208nm处出现明显的负峰,为α-螺旋构象,试验测定的数据与软件预测的结果完全一致。抗菌肽的高级结构分析表明,BTD-S分子内6个半胱氨酸结合为3对二硫键,呈梯状,整条多肽结构非常稳定,为其持久杀菌特性提供了可能；CM-S为α-螺旋,带7个净正电荷,分子具有两亲特性(有明显的疏水表面),这些特质使其更容易通过膜作用机制抑菌。
5.在普通光学显微镜下发现,20μg/ml抗菌肽的处理会导致病菌分生孢子无法正常萌发,并出现部分小号细胞群体；利用荧光显微技术观察发现抗菌肽处理的真菌孢子细胞膜受到严重损伤,大分子碘化丙啶(P1)渗入病菌细胞内部,细胞核被染色,经荧光激发显红色；扫描电镜(SEM)观察抗菌肽对细胞形态的影响,BTD-S处理后真菌孢子不能萌发,细胞表面出现明显的外渗物,甚至发生细胞的破裂和解体,CM-S处理后也见到类似的现象,由此可见,BTD-S和CM-S都能与病原真菌细胞膜互作,改变膜的透性,进而使细胞内必需物质外渗。流式细胞仪分析表明,BTD-S处理会使病菌细胞群体中逐渐分化出一批小号细胞,并且随着BTD-S浓度的增加,该类小号细胞的群体呈明显扩大趋势,这一结果与光学镜下的发现相吻合；另一方面随着BTD-S处理剂量的加大,病菌细胞对PI的吸收显著增强,即细胞受损伤(或死亡)程度逐渐加重。
6.根据BTD-S的氨基酸序列反译为DNA序列,将编码DNA序列插入到原核表达载体pET32a,构建了重组表达载体BTD-pET32a。在IPTG诱导下,检测到目的蛋白明显地过量表达,并且融合蛋白主要以可溶性形式表达,镍柱纯化可得到高纯度的目标蛋白。
Cotton production occupies a central position in national economy of China contributed from agriculture sector. According to the data provided by the National Bureau of Statistics of China, the average yield (1229kg/ha) of cotton from2010is declined as compared to last five years. This reduction in the cotton yield is mainly due to the occurrence of a devasting pathogen Verticillium dahliae in cotton growing areas and caused a severe disease known as Verticillium wilt. For so long time, scientists are engaged for identifying resistant resources against this pathogen but could not find any one in commercially grown tetraploid cotton(Gossypium hirsutum). However biotechnology and genetic engineering as new emerging sciences set up new avenues for combating Verticillium wilt in cotton by transferring resistant genes from sources other than plants.
Yangtze River and Yellow River are the two main cotton growing areas in China. About15different isolates of Verticillium dahliae, were collected from these two places and maintained in our laboratory for future work. The isolates were characterized into hyphae, sclerotia and intermediate-type on the basis of colony morphology. Further molecular identification of these isolates using four pairs of specific primers indicated that, except Fusarium oxysporum and Zhengzhou strain of Verticillium dahliae, all the other tested strains belong to Verticillium daliae including some virulent defoliating strains. To understand the interaction between cotton and Verticillium dahliae, seedling bioassays were performed using VD(Verticillium dahliae) toxin (protein-lipids-polysaccharide complexes, PLPs) and spore suspension following root dip method. The VD-toxin caused the cotton seedlings to wilt immediately while symptoms appearance with spore suspension was little delayed. Moreover, antioxidant activity in different organs of the same treatment was not the same.
In addition to greenhouse screening, field screening against Verticillium dahliae was also during2007and2008conducted using16CMS-based hybrid cotton developed by our lab. In august2007, monthly average temperature was above30℃and no wilting was recorded. However at the end of august the high disease index was observed. Whereas in2008due to low temperature and frequent rainfall, which are suitable factors for the growth of Verticillium dahliae, the incidence of field disease reached at peak in August. Moreover at different time period, cotton materials exhibited different disease index for Verticillium wilt and according to their performance,16CMS-based hybrid cotton can be divided into four groups, highly resistant sea island cotton restorer line, highly susceptible chicken leaf recovery line and 'Xiangzamian2'while other materials were either tolerant to disease or between tolerant and susceptible. The correlation analysis results showed that the final yield and fiber quality performance of the CMS-based materials were significantly correlated with the disease severity. In order to utilize the phenomenon of heterosis, F1intraspecific hybrids of upland cotton and interspecific hybrids between sea and upland cotton were developed. Hybrids though exhibited some resistance but it was not as high as that of sea iseland cotton.
From already available database having more than1500antimicrobial peptide sequences,600were identified to possess antifungal properties. Out of these, finally20different types of anti-fungal peptides were selected as a parent peptide and modified for high resistance against Verticillium dahliae and low toxicity to other organisms. However, their conservative antibacterial core domain (or amino acid residues) was retained. The interaction of these antimicrobial peptides with fungal, animal, bacterial cells and cotton protoplast was studied. Results revealed that these antimicrobial peptides efficiently inhibited the growth of Verticillium dahliae, low toxicity to animal red blood cells and cotton protoplast. The interaction between fungus isolate and antimicrobial peptide was highly significant and0-defensin BTD-S can inhibit five different isolates while hybrid peptide CM-S can inhibit four kinds of Verticillium dahliae. The minimum inhibitory concentration (MIC) for these two peptides was less than5μM and possessed stronger antimicrobial activity as compared to synthetic peptide D4E1(MIC=9.61μM). No hemolytic activities were observed to sheep red blood cells and cotton protoplast even at concentration level up to200μg/ml. These qualities make these two antimicrobial peptides more demanding for using them in developing wilt resistant cultivars.
Circular dichroism (CD) spectra of BTD-S in the far UV wavelength displayed a characteristic positive peak is195nm and205nm negative peak, indicating a typical β-sheet conformation of BTD-S. Similarly a positive peak at190nm and the negative peak at222nm and208nm for CM-S indicated a a-helix conformation and match well with the prediction from bioinformatics softwares. The advanced structural analysis of antimicrobial peptides showed that the six cysteins amino acid residues within the molecule of the BTD-S formed three disulfide bonds (like a ladder) making it more stable with durable microbicidal properties. Wherease CM-S with a-helix structure having seven net positive charge and amphiphilic properties (hydrophobic surface) make it easier to interact with the membrane of Verticillium dahliae.
Under the optical microscope, antimicrobial peptides concentration (20μg/ml) leads to the significant inhibition of conidial germination. Cell membrane permeation of fungal spores was also observed using fluorescence microscopy technique and severe cell injury was observed in response to treatment with antimicrobial peptides. This injury can be visualized from permeation of large molecules of propidium iodide (PI) into the fungus cells which then stained the nucleus and emitted red fluorescence after excitation. Similarly scanning electron microscopy (SEM) also revealed retarded growth of fungal spores with some extravasations on the cell surface and rupturing of the cell. Whereas flow cytometric analysis (FCA) showed that BTD-S treatment differentiated fungal cells into a new group of small sized cells (mini cells) and their number increased continuosly upon increasing the concentration of the BTD-S. These findings were inconsistent to that of optical microscopy, florescence microscopy and scanning electron microscopy. Therefore it can be concluded from this study that the BTD-S and CM-S interacted with pathogenic fungal cell membranes, changed the membrane permeability and thus disturbing the normal metabolism of the cells.
Using bioinformatics tools, amino acid sequence of the BTD-S was translated into coding nucleotide sequence and then inserted into the prokaryotic expression vector pET32a to construct the recombinant expression vector of the BTD-pET32a. This recombinant vector was then transferred into Escherichia coli BL21(DE3) and after IPTG induction a significant overexpression of the target protein was detected. The study provided a comprehend mechanisim of antimicrobial peptide interaction with Verticillium dahliae and laid a basis for utilizing the coding sequences of these peptides to transfer into cotton for developing transgenic wilt resistant cultivars.
引文
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