核盘菌弱毒相关DNA病毒1特性及其应用潜能研究
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摘要
核盘菌(Sclerotinia sclerotiorum (Lib.) de Bary)是一种分布广泛的重要植物病原真菌。由其引起的菌核病是多种农作物的重要病害,严重威胁农产品的产量和品质。·真菌病毒广泛存在于真菌中,一些真菌病毒可以引起病原真菌致病力衰退,对作物真菌病害具有良好的生物防治潜力。
从来自油菜罹病植株的菌核中分离获得了核盘菌菌株DT-8。DT-8表现出弱毒特性,其菌丝生长缓慢、菌丝细且分支杂乱、色素分布不均、菌核小且菌核原基形成时间晚于健康菌株4～6天,致病力非常弱。在DT-8的菌丝中分离获得了两条小的ssDNA片段,大小分别为2kb和500bp左右。挑取DT-8的菌丝尖端进行培养,可以获得不携带这两条DNA片段的培养物,它们在生长、菌核形成和致病力等方面与正常菌株没有显著区别,但通过与DT-8接触后,它们可以重新获得2kb和500bp的DNA片段,并表现出弱毒特性,推定这两条的DNA片段与DT-8菌株的弱毒现象相关。经克隆和测序分析发现2.0kb DNA片段为单链环状DNA病毒,500bpDNA为其亚基因组,命名该病毒为核盘菌弱毒相关DNA病毒1(Sclerotinia sclerotiorum hypovirulence associated DNA virus1, SsHADV-1)。
病毒SsHADV-1的基因组全长2166nt,编码两个基因,病毒链编码外壳蛋白(coat protein, CP),互补链编码复制相关蛋白(Replication associated protein, Rep);两个开放阅读框由大基因间隔区(Large intergenic region, LIR)和小基因间隔区(Small intergenic region, SIR)隔开,在LIR中包含复制和转录起始的相关元件,这些结构都与双生病毒科中玉米线条病毒属的病毒基因组结构相似。对序列进行系统进化分析,发现Rep的氨基酸序列与双生病毒同源性较高可以聚为一簇,Rep中包含有类似双生病毒的保守结构域和滚环复制相关的模体；而CP在已知蛋白数据库中找不到任何同源序列。透射电镜观察SsHADV-1病毒粒子形态,呈等轴球形,直径20～22nm。该发现首次证实了真菌中存在DNA病毒,也为双生病毒的起源和进化研究提供了新的材料。
一般认为真菌病毒缺乏体外传播途径,只能通过寄主的菌丝融合和繁殖进行传播,真菌病毒的这种特性也是限制利用病毒控制真菌病害的重要因子。对峙培养试验结果表明SsHADV-1可以在核盘菌不同营养亲和型之间较高频率地扩散,预示SsHADV-1在自然界的扩散可能不会受到寄主营养体不亲和性的限制。当纯化的病毒粒子与核盘菌菌落接触后,可以直接侵入核盘菌菌丝,使其转变成弱毒菌株；进一步研究发现病毒粒子可以直接侵染所有测试的不同营养体亲和型的核盘菌菌株,表明SsHADV-1对寄主的营养亲和型没有选择性。病毒DNA没有侵染性,不能直接侵染菌丝,甚至也不能侵染核盘菌的原生质体,表明SsHADV-1的直接侵染需要有完整的病毒粒子；但研究也发现病毒DNA可以在聚乙二醇(PEG)的介导下成功转染核盘菌原生质体。这些试验结果不仅进一步证实了SsHADV-1可以引起核盘菌的致病力衰退,也首次表明有些真菌病毒,如SsHADV-1,存在体外传播途径。
SsHADV-1存在体外传播途径,预示该病毒对菌核病具有良好的生防潜力。用2mg/ml SsHADV-1病毒粒子预处理离体或活体拟南芥,可以有效抑制核盘菌的侵染和菌核病发病,在所形成的病斑上可以分离到携带SsHADV-1的菌株,表明在拟南芥叶片上的SsHADV-1病毒粒子对核盘菌有侵染能力。再者,菌核病病斑形成2天后喷洒SsHADV-1病毒粗提液,可以抑制烟草和油菜叶片上的病斑扩展,保护植株免遭核盘菌杀死,表明直接利用病毒粒子具有防治菌核病的潜能。大田试验也取得了显著的防病效果,喷洒携带SsHADV-1的核盘菌菌丝片段(～1×1O5cfu/mL)使菌核病发病率降低33.56%,促进油菜产量提高16.44%。将病毒粒子涂抹在活体拟南芥叶片表面,在15天后仍能检测到病毒存在,表明病毒粒子在体外相对稳定。研究表明SsHADV-1的寄主范围非常窄,只能侵染核盘菌属内真菌,不能够侵染与核盘菌亲缘关系相近的灰葡萄孢；荧光原位杂交试验和PCR扩增试验均表明SsHADV-1不能在拟南芥细胞中复制和增殖。这些试验结果表明可以利用SsHADV-1控制油菜菌核病。
为深入研究病毒和寄主的相互关系,本研究成功建立了包含部分重复序列的SsHADV-1病毒全长的侵染性克隆载体。分别将2.0、1.8、1.3或1个单位长度的病毒基因组序列正向重复连入载体pKS中,利用PEG介导转染核盘菌原生质体的方式实现侵染。含有两个病毒LIR的的侵染性克隆载体转染后能够得到表型异常的再生菌株,经过核酸提取、特异性引物扩增和对峙培养传毒试验分析,证明转染子中存在游离的可水平传播的SsHADV-1病毒全长；然而含有1个单位长度的病毒基因组的载体转染后不能获得带毒的转染子。统计含有两个LIR结构的不同重复长度的载体转染成功率,发现重复片段越长,获得带毒转染子的频率越高,因此推测在SsHADV-1侵染性克隆载体释放游离病毒时,病毒重复序列之间的同源重组可能是产生病毒主要的途径。
构建了缺失CP基因的SsHADV-1侵染性克隆载体,发现不含CP的缺陷病毒可以在核盘菌原生质体内复制,但是病毒核酸积累量很低而且不能系统侵染,在再生菌株中检测不到稳定存在的病毒；用绿色荧光蛋白基因eGFP替换CP基因,转染后可以在再生菌株的部分菌丝内观察到绿色荧光,但随再生菌株的生长,不能再检测到绿色荧光,说明缺乏CP的病毒在寄主中不稳定,容易丢失。这些结果说明CP基因在SsHADV-1复制和系统侵染中有非常重要的作用,是病毒不可缺少的蛋白。本研究建立的侵染性克隆体系为研究SsHADV-1与核盘菌的互作提供了非常好的平台,有助于研究真菌DNA病毒和寄主的相互关系。
Sclerotinia sclerotiorum (Lib.) de Bary is a notorious fungal pathogen with worldwide distribution. It could cause severe diseases in Brassica and affect the yield and quality of crop severely. Mycoviruses are known to infect and multiply in all major taxa belonging to the kingdom Fungi. Typically, mycoviruses have either double-stranded (ds) or single-stranded (ss) RNA genomes. They are thought not to be infectious as free particles and to lack an extracellular phase in their life cycles. Mycovirus-mediated hypovirulence is a phenomenon in which the virulence of fungal pathogens is reduced or even completely lost as a consequence of virus infection, thus these kinds of mycovirus are considered to be promising biocontrol agents against plant pathogenic fungi.
Strain DT-8was isolated from the sclerotia in the diseased rapeseed plant stem. It developed abnormal colony morphology on potato dextrose agar (PDA) and exhibited hypovirulent phenotype when inoculated onto Arabidopsis thaliana or detached leaves of Brassica napus. The total DNA of strain DT-8was extracted and besides the fungal genomic DNA, there were two additional DNA bands with sizes of about2kb--large DNA element (LDE) and0.5kb-small DNA element (SDE), respectively, which were hypovirulence related. The genome of this circular ssDNA virus, named Sclerotinia sclerotiorum hypovirulence-associated DNA virus1(SsHADV-1), is2166nt, coding for a replication initiation protein (Rep) and a coat protein (CP). ORFs are separated by a large intergenic region (LIR) and a small intergenic region (SIR). There are geminivirus related bi-promoter and conserved sequences which are important for virus replication in the LIR.
Although phylogenetic analysis of Rep showed that SsHADV-1is related to geminiviruses, it is notably distinct from geminiviruses both in genome organization and particle morphology. Surprisingly, we could not find any CP-related proteins in the known protein databases. Negatively stained viral particles observed with an electron microscope were nontwinned isometric particles,20～22nm in diameter, which are clearly different from the geminivirus. The molecular mass of CP is about35kDa by SDS/PAGE analysis. The0.5kb SDE, which is also circular single-stranded, is proved to be subgenomic DNA of SsHADV-1according to the sequence analysis. Thus, this is the first time that we demonstrated that a DNA virus could replicate in a fungus in nature and reported an ssDNA virus infecting fungi.
We found that this virus was surprisingly easy to transmit from strain DT-8to strains belonging to other vegetative compatibility groups (VCGs). Furthermore, Polyethylene glycol (PEG) mediated transfection of fungal protoplasts was successful with either purified SsHADV-1particles or viral DNA isolated directly from infected mycelium. Then we continued to test the infectivity of SsHADV-1towards S. sclerotinia. We demonstrated that purified particles of SsHADV-1are infectious when applied extracellularly to its fungal host S. sclerotiorum. Virus particles isolated from infected host can infect the hyphae of virus-free S. sclerotiorum directly when applied to hyphae grown on PDA plates or spread on leaves of Arabidopsis thaliana and Brassica napus.
When applied on leaves, virus infection could suppress development of lesions induced by S. sclerotiorum. Although SsHADV-1can infect host strains belonging to different VCGs when applied externally, it has a narrow host range. Virus particles are likely to be very stable on the leaves of Arabidopsis plants since viral DNA could be detected at15dpi on unwounded leaves and at10dpi on wounded leaves, respectively; however, this virus could not infect and move in plant cells. Our findings may prompt a change in the generalization that mycoviruses lack an extracellular phase in their life cycles; and the potential of using DNA mycoviruses as natural fungicides appear to be promising and may stimulate the search for other DNA mycoviruses.
To advance the exploration of SsHADV-1and its interaction with the fungal host, we constructed the infectious clones of SsHADV-1that contain tandemlytandemly repeated viral sequences with at least one full length SsHADV-1and two LIRs. Different repeated lengh of SsHADV-1were used to construct the vectors which are2units,1.8units,1.3units and1unit. When introduced into virulent S. sclerotinia strains by PEG-mediated transfection, a resurrected, cytoplasmically replicating DNA form is generated from the infectious copy except for the1unit vector. Comparision of the successful transformation efficiency among different infectious clone vectors showed the longer the repeated sequences, the higher the successful transformation efficiency. It suggested that the homologous recombination may play the major role in unit-length SsHADV-1DNA release from the vector.
Efforts to test whether the CP deleted SsHADV-1could exist in S. sclerotiorum cells has been made, however, we could only detect low level of viral DNA which were easily lost during subculture, strains containing stable replicating CP deleted SsHADV-1could not be abtained. eGFP was used to subsititute for CP to construct the infectious clone vector and although the efficient and stable expression constructs were not observed, transient expression of introduced foreign genes was confirmed. Thus, the coat protein of SsHADV-1plays an essential role in virus maintenance and accumulation.
从来自油菜罹病植株的菌核中分离获得了核盘菌菌株DT-8。DT-8表现出弱毒特性,其菌丝生长缓慢、菌丝细且分支杂乱、色素分布不均、菌核小且菌核原基形成时间晚于健康菌株4～6天,致病力非常弱。在DT-8的菌丝中分离获得了两条小的ssDNA片段,大小分别为2kb和500bp左右。挑取DT-8的菌丝尖端进行培养,可以获得不携带这两条DNA片段的培养物,它们在生长、菌核形成和致病力等方面与正常菌株没有显著区别,但通过与DT-8接触后,它们可以重新获得2kb和500bp的DNA片段,并表现出弱毒特性,推定这两条的DNA片段与DT-8菌株的弱毒现象相关。经克隆和测序分析发现2.0kb DNA片段为单链环状DNA病毒,500bpDNA为其亚基因组,命名该病毒为核盘菌弱毒相关DNA病毒1(Sclerotinia sclerotiorum hypovirulence associated DNA virus1, SsHADV-1)。
病毒SsHADV-1的基因组全长2166nt,编码两个基因,病毒链编码外壳蛋白(coat protein, CP),互补链编码复制相关蛋白(Replication associated protein, Rep);两个开放阅读框由大基因间隔区(Large intergenic region, LIR)和小基因间隔区(Small intergenic region, SIR)隔开,在LIR中包含复制和转录起始的相关元件,这些结构都与双生病毒科中玉米线条病毒属的病毒基因组结构相似。对序列进行系统进化分析,发现Rep的氨基酸序列与双生病毒同源性较高可以聚为一簇,Rep中包含有类似双生病毒的保守结构域和滚环复制相关的模体；而CP在已知蛋白数据库中找不到任何同源序列。透射电镜观察SsHADV-1病毒粒子形态,呈等轴球形,直径20～22nm。该发现首次证实了真菌中存在DNA病毒,也为双生病毒的起源和进化研究提供了新的材料。
一般认为真菌病毒缺乏体外传播途径,只能通过寄主的菌丝融合和繁殖进行传播,真菌病毒的这种特性也是限制利用病毒控制真菌病害的重要因子。对峙培养试验结果表明SsHADV-1可以在核盘菌不同营养亲和型之间较高频率地扩散,预示SsHADV-1在自然界的扩散可能不会受到寄主营养体不亲和性的限制。当纯化的病毒粒子与核盘菌菌落接触后,可以直接侵入核盘菌菌丝,使其转变成弱毒菌株；进一步研究发现病毒粒子可以直接侵染所有测试的不同营养体亲和型的核盘菌菌株,表明SsHADV-1对寄主的营养亲和型没有选择性。病毒DNA没有侵染性,不能直接侵染菌丝,甚至也不能侵染核盘菌的原生质体,表明SsHADV-1的直接侵染需要有完整的病毒粒子；但研究也发现病毒DNA可以在聚乙二醇(PEG)的介导下成功转染核盘菌原生质体。这些试验结果不仅进一步证实了SsHADV-1可以引起核盘菌的致病力衰退,也首次表明有些真菌病毒,如SsHADV-1,存在体外传播途径。
SsHADV-1存在体外传播途径,预示该病毒对菌核病具有良好的生防潜力。用2mg/ml SsHADV-1病毒粒子预处理离体或活体拟南芥,可以有效抑制核盘菌的侵染和菌核病发病,在所形成的病斑上可以分离到携带SsHADV-1的菌株,表明在拟南芥叶片上的SsHADV-1病毒粒子对核盘菌有侵染能力。再者,菌核病病斑形成2天后喷洒SsHADV-1病毒粗提液,可以抑制烟草和油菜叶片上的病斑扩展,保护植株免遭核盘菌杀死,表明直接利用病毒粒子具有防治菌核病的潜能。大田试验也取得了显著的防病效果,喷洒携带SsHADV-1的核盘菌菌丝片段(～1×1O5cfu/mL)使菌核病发病率降低33.56%,促进油菜产量提高16.44%。将病毒粒子涂抹在活体拟南芥叶片表面,在15天后仍能检测到病毒存在,表明病毒粒子在体外相对稳定。研究表明SsHADV-1的寄主范围非常窄,只能侵染核盘菌属内真菌,不能够侵染与核盘菌亲缘关系相近的灰葡萄孢；荧光原位杂交试验和PCR扩增试验均表明SsHADV-1不能在拟南芥细胞中复制和增殖。这些试验结果表明可以利用SsHADV-1控制油菜菌核病。
为深入研究病毒和寄主的相互关系,本研究成功建立了包含部分重复序列的SsHADV-1病毒全长的侵染性克隆载体。分别将2.0、1.8、1.3或1个单位长度的病毒基因组序列正向重复连入载体pKS中,利用PEG介导转染核盘菌原生质体的方式实现侵染。含有两个病毒LIR的的侵染性克隆载体转染后能够得到表型异常的再生菌株,经过核酸提取、特异性引物扩增和对峙培养传毒试验分析,证明转染子中存在游离的可水平传播的SsHADV-1病毒全长；然而含有1个单位长度的病毒基因组的载体转染后不能获得带毒的转染子。统计含有两个LIR结构的不同重复长度的载体转染成功率,发现重复片段越长,获得带毒转染子的频率越高,因此推测在SsHADV-1侵染性克隆载体释放游离病毒时,病毒重复序列之间的同源重组可能是产生病毒主要的途径。
构建了缺失CP基因的SsHADV-1侵染性克隆载体,发现不含CP的缺陷病毒可以在核盘菌原生质体内复制,但是病毒核酸积累量很低而且不能系统侵染,在再生菌株中检测不到稳定存在的病毒；用绿色荧光蛋白基因eGFP替换CP基因,转染后可以在再生菌株的部分菌丝内观察到绿色荧光,但随再生菌株的生长,不能再检测到绿色荧光,说明缺乏CP的病毒在寄主中不稳定,容易丢失。这些结果说明CP基因在SsHADV-1复制和系统侵染中有非常重要的作用,是病毒不可缺少的蛋白。本研究建立的侵染性克隆体系为研究SsHADV-1与核盘菌的互作提供了非常好的平台,有助于研究真菌DNA病毒和寄主的相互关系。
Sclerotinia sclerotiorum (Lib.) de Bary is a notorious fungal pathogen with worldwide distribution. It could cause severe diseases in Brassica and affect the yield and quality of crop severely. Mycoviruses are known to infect and multiply in all major taxa belonging to the kingdom Fungi. Typically, mycoviruses have either double-stranded (ds) or single-stranded (ss) RNA genomes. They are thought not to be infectious as free particles and to lack an extracellular phase in their life cycles. Mycovirus-mediated hypovirulence is a phenomenon in which the virulence of fungal pathogens is reduced or even completely lost as a consequence of virus infection, thus these kinds of mycovirus are considered to be promising biocontrol agents against plant pathogenic fungi.
Strain DT-8was isolated from the sclerotia in the diseased rapeseed plant stem. It developed abnormal colony morphology on potato dextrose agar (PDA) and exhibited hypovirulent phenotype when inoculated onto Arabidopsis thaliana or detached leaves of Brassica napus. The total DNA of strain DT-8was extracted and besides the fungal genomic DNA, there were two additional DNA bands with sizes of about2kb--large DNA element (LDE) and0.5kb-small DNA element (SDE), respectively, which were hypovirulence related. The genome of this circular ssDNA virus, named Sclerotinia sclerotiorum hypovirulence-associated DNA virus1(SsHADV-1), is2166nt, coding for a replication initiation protein (Rep) and a coat protein (CP). ORFs are separated by a large intergenic region (LIR) and a small intergenic region (SIR). There are geminivirus related bi-promoter and conserved sequences which are important for virus replication in the LIR.
Although phylogenetic analysis of Rep showed that SsHADV-1is related to geminiviruses, it is notably distinct from geminiviruses both in genome organization and particle morphology. Surprisingly, we could not find any CP-related proteins in the known protein databases. Negatively stained viral particles observed with an electron microscope were nontwinned isometric particles,20～22nm in diameter, which are clearly different from the geminivirus. The molecular mass of CP is about35kDa by SDS/PAGE analysis. The0.5kb SDE, which is also circular single-stranded, is proved to be subgenomic DNA of SsHADV-1according to the sequence analysis. Thus, this is the first time that we demonstrated that a DNA virus could replicate in a fungus in nature and reported an ssDNA virus infecting fungi.
We found that this virus was surprisingly easy to transmit from strain DT-8to strains belonging to other vegetative compatibility groups (VCGs). Furthermore, Polyethylene glycol (PEG) mediated transfection of fungal protoplasts was successful with either purified SsHADV-1particles or viral DNA isolated directly from infected mycelium. Then we continued to test the infectivity of SsHADV-1towards S. sclerotinia. We demonstrated that purified particles of SsHADV-1are infectious when applied extracellularly to its fungal host S. sclerotiorum. Virus particles isolated from infected host can infect the hyphae of virus-free S. sclerotiorum directly when applied to hyphae grown on PDA plates or spread on leaves of Arabidopsis thaliana and Brassica napus.
When applied on leaves, virus infection could suppress development of lesions induced by S. sclerotiorum. Although SsHADV-1can infect host strains belonging to different VCGs when applied externally, it has a narrow host range. Virus particles are likely to be very stable on the leaves of Arabidopsis plants since viral DNA could be detected at15dpi on unwounded leaves and at10dpi on wounded leaves, respectively; however, this virus could not infect and move in plant cells. Our findings may prompt a change in the generalization that mycoviruses lack an extracellular phase in their life cycles; and the potential of using DNA mycoviruses as natural fungicides appear to be promising and may stimulate the search for other DNA mycoviruses.
To advance the exploration of SsHADV-1and its interaction with the fungal host, we constructed the infectious clones of SsHADV-1that contain tandemlytandemly repeated viral sequences with at least one full length SsHADV-1and two LIRs. Different repeated lengh of SsHADV-1were used to construct the vectors which are2units,1.8units,1.3units and1unit. When introduced into virulent S. sclerotinia strains by PEG-mediated transfection, a resurrected, cytoplasmically replicating DNA form is generated from the infectious copy except for the1unit vector. Comparision of the successful transformation efficiency among different infectious clone vectors showed the longer the repeated sequences, the higher the successful transformation efficiency. It suggested that the homologous recombination may play the major role in unit-length SsHADV-1DNA release from the vector.
Efforts to test whether the CP deleted SsHADV-1could exist in S. sclerotiorum cells has been made, however, we could only detect low level of viral DNA which were easily lost during subculture, strains containing stable replicating CP deleted SsHADV-1could not be abtained. eGFP was used to subsititute for CP to construct the infectious clone vector and although the efficient and stable expression constructs were not observed, transient expression of introduced foreign genes was confirmed. Thus, the coat protein of SsHADV-1plays an essential role in virus maintenance and accumulation.
引文
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