马铃薯纺锤块茎类病毒遗传多样性及其诱导的基因沉默
摘要
类病毒是能够侵染多种植物并造成重大经济损失的RNA分子。类病毒由于特有的基因序列和结构特点,提供寄主-病原相互作用的一个最佳的研究模式。RNA沉默是植物和其它真核生物用来防御外来核酸侵染的一种保守的防御机制。在病毒诱导的基因沉默途径(Virus inducing gene silencing, VIGS)中, 21～24 nt病毒小分子RNAs(vsiRNA)的产生是植物抗病毒RNA沉默诱发的标志。目前对于vsiRNA生物合成的机制及其生物学功能的还没有完全研究清楚。与之相对应,很多病毒通过编码RNA沉默抑制子蛋白或直接以病毒RNA来拮抗植物的抗病毒RNA沉默。植物在受到类病毒侵染后同样会启动VIGS途径产生类病毒专化性的小RNA,然而,裸露的类病毒非编码RNAs如何能逃脱细胞内的抗病毒RNA沉默呢?
本研究针对在我国马铃薯主产区黑龙江省采集的马铃薯纺锤块茎类病毒(Potato spindle tuber viroid, PSTVd)样品,进行基因克隆和序列分析,开展PSTVd遗传变异多样性的研究。同时,以PSTVd为研究对象,利用分子生物学技术,深入研究PSTVd侵染植物后诱导的基因沉默,了解类病毒是否也会象病毒那样,对寄主的防御系统产生沉默抑制功能,从而实现其侵染目的。同时,还研究在沉默过程中所产生的siPSTVd的生物合成机制及其是否对植物体内的miRNA合成途径有所影响。研究结果如下:
1、类病毒具有遗传变异多样性,其在寄主体内以相近变异群体进行传播。
对克山马铃薯所提供的PSTVd阳性试管苗样品PKS 1-6进行序列测定,结果显示其序列与已报道的强株系(KF 440-2、RG1)与中间株系(PSTVd int)有较大的序列差异,同源性仅为97.21%、97.77%和98.61%,而与所报道的弱株系KF-5、GI333357和GBX76844同源性较大,分别为99.16%、99.72%和99.44%。因此,从序列上看PKS1-6更接近于弱株系。用PKS1-6分离物接种转GFP基因烟草16C,对侵染后阳性样品的PSTVd进行序列测定,结果发现在4个测定序列中,有3个类病毒序列与接种的PSTVd序列相比发生了变异,变异部位在中央保守区有3处(81、82和267位),在可变区有2处(127和136位),致病区有1处(56位)。说明,类病毒序列有一定保守性和可变性,其变异可能受环境条件、寄主范围等因素影响,其变化也不仅仅局限在可变区(V区)。对于采自富锦的田间PSTVd一份阳性样品进行序列分析,在6个克隆中,有5个与PKS1-6序列同源,只有一个PFJ-14有2个突变,发生在左末端区(40位)和致病区(296位)。对于采自泰康的一份阳性田间样品,对其11个克隆进行序列测定,有4个与PKS1-6同源,有7个发生了变异。
研究中共对来自克山马铃薯所和采自富锦、泰康马铃薯田的PSTVd阳性样品的22个PSTVd克隆进行序列测定,共产生12个不同序列,其中与PKS1-6分离物序列相同的变异物有10个,其核苷酸差异数量在0～3个之间,同源性在99.16%～100%。二级结构的最低自由能变化为-159.10～-173.60 kcal/mol。其序列变异主要分布在CCR区和可变区,变异频率分别为38.1%和28.9%。其次为致病区(变异频率为14.3%)和左、右末端区(变异频率均为9.5%)。
2、类病毒能诱导寄主产生沉默,但不具有沉默抑制子功能。
利用我们构建的含有类病毒正负链单体和双体的植物表达载体分别与含报道基因GFP载体的农杆菌共注射转GFP基因烟草16C,发现与类病毒共注射的叶片的荧光弱于对照,表明类病毒可能在一定程度上促进了GFP的沉默。对PSTVd和GFP的序列进行比对,其同源性仅为47.6%(Identity),最长的同源区域(Longest identitied seq)仅为9 bp,不具有产生沉默的条件。为了排除类病毒载体对共注射的GFP载体中的35S启动子产生沉默,又利用含有pdsi的发夹载体与类病毒载体共注射烟草叶片,观察叶片白化现象。结果,类病毒还是促进了烟草PDS基因的沉默。但Northern blot杂交结果表明35S启动子来源的siRNA积累水平与空载体对照没有明显差异,表明类病毒促进的沉默不是在启动子上。同时,对GFP和PSTVd共注射的样品进行mGFP的Nothern blot杂交,结果显示,GFP和PSTVd共注射的mGFP的量少于GFP与空载体共注射的量。说明,在mGFP的转录水平上,受共注射的PSTVd的影响, GFP mRNA的积累量减少,从而荧光减弱。通过这些结果我们推断,类病毒促进的基因沉默可能与甲基化有关,可能发生在转录水平上。
3、类病毒产生的siPSTVd来源于成熟的二级结构。
通过对含有PSTVd可复制的双体负链载体和非全长不可复制的载体注射烟草后的siPSTVd的检测结果显示,均检测到了特异性的siPSTVd,说明除了复制形成的dsRNA这一来源外,PSTVd形成的二级结构也是产生siPSTVd的重要来源。从诱发产生siRNA的数量比例上看,其中数量比例较多的是(+)siRNAs。这个观察结果与PSTVd RNA基因组折叠成高度结构化二级结构,然后在体内被DCL切割的理论相一致。
4、类病毒侵染产生的siPSTVd没有调控内源的miRNA途径。
对于接种番茄(Rutgers)和马铃薯的阳性样品和对照阴性样品杂交结果显示:阳性样品均检测到siPSTVd(±),证明类病毒侵染番茄和马铃薯后,诱导寄主产生基因沉默现象。而没有接种类病毒的番茄和马铃薯,没有检测到siPSTVd(±)。对同一张膜,同时检测了mi159和mi167,结果显示,受类病毒侵染的马铃薯和番茄植株与健康植株相比,miRNA积累水平无明显变化,烟草植株之间的miRNA的积累水平也没有明显变化,表明类病毒的入侵对植物体内的miRNA途径影响不大,至少对两个主要miRNA(mi159和mi167)产生途径没有影响。
研究类病毒侵染植物的策略有助于揭示基础的分子生物和细胞加工的机理,对于植物和其它有机物细胞和分子生物学的整体产生重要影响。通过对这些现象的揭示,对于了解类病毒的结构、功能及其致病途径具有重要理论意义。同时,对于揭示类病毒诱导的基因沉默机制及与寄主的互作有重要突破,为最终实现抗类病毒提供理论指导价值。
Viroids can infect various plants and thereby causing important losses in agriculture. As there is no evidence for RNA translation, their pathogenic effects must result from direct interaction with host components. Viroids thus offer a unique model for exploring host-pathogen interactions that depend strictly on the pathogen’s RNA sequence and structure. RNA silencing (RNAi) is a conserved defense mechanism plants and other eukaryotes use to protect their genomes against aberrant nucleic acids. A hallmark of this defense response is the production of 21～24 nt viral small RNAs via mechanisms that remain to be fully understand. Many viruses encode suppressors of RNA silencing, and some viral RNAs function directly as silencing suppressors, as counter-defense. The occurrence of viroids can trigger RNA silencing in a host, raising the question of how these noncoding and unencapsidated RNAs survive cellular RNA silencing systems.
In this study, the PSTVd samples collected from Heilongjiang of the main potato area were cloned and sequenced. The genetic stability of PSTVd was analyzed. The gene silencing induced by PSTVd and the interaction between viroid and host were deeply studied. This study also tried to disclose siPSTVd are mostly from structured PSTVd(+) RNAs or generated from dsRNA intermediates during viral replication. Further analysis on the accumulation levels of the endogenous tomato and potato miRNA pathway can be modulated by PSTVd infection or not. The results were as follows:
1. The diversity of the viroidosphere
PSTVd samples of PKS 1-6 plantlet in vitro supplied by Keshan Potato Research Institute was cloned and sequenced. Compared with severe strains(KF 440-2, RG1) and intermediate strain (PSTVd int) reported in Genebank, PKS 1-6 had more differences in sequence(identity were only 97.21%, 97.77% and 98.61%, respectively), whereas PKS 1-6 was more constant in sequence with mild strains(KF-5, GI 333357 and GB X76844) (identity were 99.16%, 97.72% and 99.44%, respectively). From sequence alignment, PKS 1-6 isolate can be defined as mild strain. To inoculate PKS 1-6 isolate to N. benthamiana plants that transgenically express GFP(line GFP 16C) and analysis the sequence of 16C samples infected PSTVd, three of four PKS 1-6 progenies in 16C had mutations, one maintain parental sequence. The mutant region located in the CCR(at position 81, 82 and 267), Var (at position 127 and 136), and Path(at position 56). For sequence analyses of PSTVd samples collected Fujin potato field, five in six clones had the identical sequence with PKS 1-6, and only PEF-14 variant had 2 mutants at position 4(TL) and 296(Path). But for sequence analyses of PSTVd from Taikang, four in eleven clones were identical compared with PKS 1-6.
A total of 22 clones were sequenced. Among them, 12 mutations had been observed, whereas in them 10 clones had the idential sequence as PKS 1-6. In all clones, the number of mutant nucletides was between 0～3, and the homology was between 99.16%～100%, and the lowest free energy difference was between -159.10%～-173.6% kcal/mol. The mutation mainly located in CCR and Var(variant frequent was 38.1% and 28.9%, respectively), followed by Path region(variant frequent was 14.3%) and TL and TR(variant frequent were 9.5%).
2. PSTVd did not function as an RNA silencing suppressor at the cellar and whole plant levels
We used transgenical N. benthamiana 16C to test PSTVd suppressor activity. When 16C plants were co-infiltrated by PSTVd recombinant vectors containing sense, antisense monomeric and dimeric PSTVd, respectively, together with vector containing GFP.The GFP fluorescence of local leaves was observed with dim intensity for co-infiltration with PSTVd construct than control, indicating that PSTVd induced the silencing in a certain degree. The fact that PSTVd could induce gene silencing and produced sense and antisense siPSTVd were confirmed by siRNA gel plot. To exclude the possibility that the PSTVd sequence can induce the GFP suppress for the sequence identity, we align the sequence of PSTVd and GFP. The identity was only 47.6% and longest identical sequence was only 9 bp, so the alignment results exclude the possibility. Meanwhile, we devised the experiment that we co-infiltrated hp pdsi and PSTVd vector to N.B. and observed that PSTVd vector promote silencing of plant pds gene. From the hybridization results of si35S-promoter, the level of PSTVd and control had no significant difference. This result addressed the phenomena of inducing silencing was not reduced the 35s-promoter. From northern blot of mGFP, the mGFP quantity level of PSTVd and GFP co-infiltration turned less then the control, that indicate the transcription of GFP can be affected by PSTVd, and mGFP decreased , so the fluorescence turned weak. From these results, we speculated the PSTVd can be inducer of gene silencing in the transcriptional level for the methylation.
3. siPSTVd were derived predominantly from structured RNA of PSTVd
From the results of northern blot for siPSTVd by the infiltration the vector with the dimeric replicated PSTVd and non-full length and non-replicated PSTVd to N.B., we observed that the specific PSTVd siRNA could be detected for both of them. That indicated the structured PSTVd could be the source of siPSTVd. The profile obtained in the siPSTVd showed that the majority of PSTVd siRNAs were of the (+)polarity. This observation is consistent with the notion that genomic PSTVd RNA folds into a highly structured conformation, which is then cleaved by DCL in vivo.
4. PSTVd siRNAs do not modulate miRNA pathway
Both polarities of siPSTVd could be detected for positive samples inoculated in tomato (Rutgers) and potato, which mean gene silencing was induced after the infection of PSTVd. No siPSTVd were produced for mock treatment. For the same membrane, the mi159 and mi167 blotting were done. The results showed no significantly different for the miRNA level for positive and negative samples. Our analyses showed PSTVd is unlikely to affect the pathway of endogenous miRNAs, at least for the main miRNA of both mi159 and mi167.
Studying the strategies that viroids infect a plant also helps to address basic molecular and cellular processes. It’s significant to understand the structure, function and pathway of pathogenicity. Meanwhile, it will provide important principle value for disclosing the mechanism of gene silencing and interaction between viroid host and pathogen, and also provide the reference of defence to viroid.
本研究针对在我国马铃薯主产区黑龙江省采集的马铃薯纺锤块茎类病毒(Potato spindle tuber viroid, PSTVd)样品,进行基因克隆和序列分析,开展PSTVd遗传变异多样性的研究。同时,以PSTVd为研究对象,利用分子生物学技术,深入研究PSTVd侵染植物后诱导的基因沉默,了解类病毒是否也会象病毒那样,对寄主的防御系统产生沉默抑制功能,从而实现其侵染目的。同时,还研究在沉默过程中所产生的siPSTVd的生物合成机制及其是否对植物体内的miRNA合成途径有所影响。研究结果如下:
1、类病毒具有遗传变异多样性,其在寄主体内以相近变异群体进行传播。
对克山马铃薯所提供的PSTVd阳性试管苗样品PKS 1-6进行序列测定,结果显示其序列与已报道的强株系(KF 440-2、RG1)与中间株系(PSTVd int)有较大的序列差异,同源性仅为97.21%、97.77%和98.61%,而与所报道的弱株系KF-5、GI333357和GBX76844同源性较大,分别为99.16%、99.72%和99.44%。因此,从序列上看PKS1-6更接近于弱株系。用PKS1-6分离物接种转GFP基因烟草16C,对侵染后阳性样品的PSTVd进行序列测定,结果发现在4个测定序列中,有3个类病毒序列与接种的PSTVd序列相比发生了变异,变异部位在中央保守区有3处(81、82和267位),在可变区有2处(127和136位),致病区有1处(56位)。说明,类病毒序列有一定保守性和可变性,其变异可能受环境条件、寄主范围等因素影响,其变化也不仅仅局限在可变区(V区)。对于采自富锦的田间PSTVd一份阳性样品进行序列分析,在6个克隆中,有5个与PKS1-6序列同源,只有一个PFJ-14有2个突变,发生在左末端区(40位)和致病区(296位)。对于采自泰康的一份阳性田间样品,对其11个克隆进行序列测定,有4个与PKS1-6同源,有7个发生了变异。
研究中共对来自克山马铃薯所和采自富锦、泰康马铃薯田的PSTVd阳性样品的22个PSTVd克隆进行序列测定,共产生12个不同序列,其中与PKS1-6分离物序列相同的变异物有10个,其核苷酸差异数量在0～3个之间,同源性在99.16%～100%。二级结构的最低自由能变化为-159.10～-173.60 kcal/mol。其序列变异主要分布在CCR区和可变区,变异频率分别为38.1%和28.9%。其次为致病区(变异频率为14.3%)和左、右末端区(变异频率均为9.5%)。
2、类病毒能诱导寄主产生沉默,但不具有沉默抑制子功能。
利用我们构建的含有类病毒正负链单体和双体的植物表达载体分别与含报道基因GFP载体的农杆菌共注射转GFP基因烟草16C,发现与类病毒共注射的叶片的荧光弱于对照,表明类病毒可能在一定程度上促进了GFP的沉默。对PSTVd和GFP的序列进行比对,其同源性仅为47.6%(Identity),最长的同源区域(Longest identitied seq)仅为9 bp,不具有产生沉默的条件。为了排除类病毒载体对共注射的GFP载体中的35S启动子产生沉默,又利用含有pdsi的发夹载体与类病毒载体共注射烟草叶片,观察叶片白化现象。结果,类病毒还是促进了烟草PDS基因的沉默。但Northern blot杂交结果表明35S启动子来源的siRNA积累水平与空载体对照没有明显差异,表明类病毒促进的沉默不是在启动子上。同时,对GFP和PSTVd共注射的样品进行mGFP的Nothern blot杂交,结果显示,GFP和PSTVd共注射的mGFP的量少于GFP与空载体共注射的量。说明,在mGFP的转录水平上,受共注射的PSTVd的影响, GFP mRNA的积累量减少,从而荧光减弱。通过这些结果我们推断,类病毒促进的基因沉默可能与甲基化有关,可能发生在转录水平上。
3、类病毒产生的siPSTVd来源于成熟的二级结构。
通过对含有PSTVd可复制的双体负链载体和非全长不可复制的载体注射烟草后的siPSTVd的检测结果显示,均检测到了特异性的siPSTVd,说明除了复制形成的dsRNA这一来源外,PSTVd形成的二级结构也是产生siPSTVd的重要来源。从诱发产生siRNA的数量比例上看,其中数量比例较多的是(+)siRNAs。这个观察结果与PSTVd RNA基因组折叠成高度结构化二级结构,然后在体内被DCL切割的理论相一致。
4、类病毒侵染产生的siPSTVd没有调控内源的miRNA途径。
对于接种番茄(Rutgers)和马铃薯的阳性样品和对照阴性样品杂交结果显示:阳性样品均检测到siPSTVd(±),证明类病毒侵染番茄和马铃薯后,诱导寄主产生基因沉默现象。而没有接种类病毒的番茄和马铃薯,没有检测到siPSTVd(±)。对同一张膜,同时检测了mi159和mi167,结果显示,受类病毒侵染的马铃薯和番茄植株与健康植株相比,miRNA积累水平无明显变化,烟草植株之间的miRNA的积累水平也没有明显变化,表明类病毒的入侵对植物体内的miRNA途径影响不大,至少对两个主要miRNA(mi159和mi167)产生途径没有影响。
研究类病毒侵染植物的策略有助于揭示基础的分子生物和细胞加工的机理,对于植物和其它有机物细胞和分子生物学的整体产生重要影响。通过对这些现象的揭示,对于了解类病毒的结构、功能及其致病途径具有重要理论意义。同时,对于揭示类病毒诱导的基因沉默机制及与寄主的互作有重要突破,为最终实现抗类病毒提供理论指导价值。
Viroids can infect various plants and thereby causing important losses in agriculture. As there is no evidence for RNA translation, their pathogenic effects must result from direct interaction with host components. Viroids thus offer a unique model for exploring host-pathogen interactions that depend strictly on the pathogen’s RNA sequence and structure. RNA silencing (RNAi) is a conserved defense mechanism plants and other eukaryotes use to protect their genomes against aberrant nucleic acids. A hallmark of this defense response is the production of 21～24 nt viral small RNAs via mechanisms that remain to be fully understand. Many viruses encode suppressors of RNA silencing, and some viral RNAs function directly as silencing suppressors, as counter-defense. The occurrence of viroids can trigger RNA silencing in a host, raising the question of how these noncoding and unencapsidated RNAs survive cellular RNA silencing systems.
In this study, the PSTVd samples collected from Heilongjiang of the main potato area were cloned and sequenced. The genetic stability of PSTVd was analyzed. The gene silencing induced by PSTVd and the interaction between viroid and host were deeply studied. This study also tried to disclose siPSTVd are mostly from structured PSTVd(+) RNAs or generated from dsRNA intermediates during viral replication. Further analysis on the accumulation levels of the endogenous tomato and potato miRNA pathway can be modulated by PSTVd infection or not. The results were as follows:
1. The diversity of the viroidosphere
PSTVd samples of PKS 1-6 plantlet in vitro supplied by Keshan Potato Research Institute was cloned and sequenced. Compared with severe strains(KF 440-2, RG1) and intermediate strain (PSTVd int) reported in Genebank, PKS 1-6 had more differences in sequence(identity were only 97.21%, 97.77% and 98.61%, respectively), whereas PKS 1-6 was more constant in sequence with mild strains(KF-5, GI 333357 and GB X76844) (identity were 99.16%, 97.72% and 99.44%, respectively). From sequence alignment, PKS 1-6 isolate can be defined as mild strain. To inoculate PKS 1-6 isolate to N. benthamiana plants that transgenically express GFP(line GFP 16C) and analysis the sequence of 16C samples infected PSTVd, three of four PKS 1-6 progenies in 16C had mutations, one maintain parental sequence. The mutant region located in the CCR(at position 81, 82 and 267), Var (at position 127 and 136), and Path(at position 56). For sequence analyses of PSTVd samples collected Fujin potato field, five in six clones had the identical sequence with PKS 1-6, and only PEF-14 variant had 2 mutants at position 4(TL) and 296(Path). But for sequence analyses of PSTVd from Taikang, four in eleven clones were identical compared with PKS 1-6.
A total of 22 clones were sequenced. Among them, 12 mutations had been observed, whereas in them 10 clones had the idential sequence as PKS 1-6. In all clones, the number of mutant nucletides was between 0～3, and the homology was between 99.16%～100%, and the lowest free energy difference was between -159.10%～-173.6% kcal/mol. The mutation mainly located in CCR and Var(variant frequent was 38.1% and 28.9%, respectively), followed by Path region(variant frequent was 14.3%) and TL and TR(variant frequent were 9.5%).
2. PSTVd did not function as an RNA silencing suppressor at the cellar and whole plant levels
We used transgenical N. benthamiana 16C to test PSTVd suppressor activity. When 16C plants were co-infiltrated by PSTVd recombinant vectors containing sense, antisense monomeric and dimeric PSTVd, respectively, together with vector containing GFP.The GFP fluorescence of local leaves was observed with dim intensity for co-infiltration with PSTVd construct than control, indicating that PSTVd induced the silencing in a certain degree. The fact that PSTVd could induce gene silencing and produced sense and antisense siPSTVd were confirmed by siRNA gel plot. To exclude the possibility that the PSTVd sequence can induce the GFP suppress for the sequence identity, we align the sequence of PSTVd and GFP. The identity was only 47.6% and longest identical sequence was only 9 bp, so the alignment results exclude the possibility. Meanwhile, we devised the experiment that we co-infiltrated hp pdsi and PSTVd vector to N.B. and observed that PSTVd vector promote silencing of plant pds gene. From the hybridization results of si35S-promoter, the level of PSTVd and control had no significant difference. This result addressed the phenomena of inducing silencing was not reduced the 35s-promoter. From northern blot of mGFP, the mGFP quantity level of PSTVd and GFP co-infiltration turned less then the control, that indicate the transcription of GFP can be affected by PSTVd, and mGFP decreased , so the fluorescence turned weak. From these results, we speculated the PSTVd can be inducer of gene silencing in the transcriptional level for the methylation.
3. siPSTVd were derived predominantly from structured RNA of PSTVd
From the results of northern blot for siPSTVd by the infiltration the vector with the dimeric replicated PSTVd and non-full length and non-replicated PSTVd to N.B., we observed that the specific PSTVd siRNA could be detected for both of them. That indicated the structured PSTVd could be the source of siPSTVd. The profile obtained in the siPSTVd showed that the majority of PSTVd siRNAs were of the (+)polarity. This observation is consistent with the notion that genomic PSTVd RNA folds into a highly structured conformation, which is then cleaved by DCL in vivo.
4. PSTVd siRNAs do not modulate miRNA pathway
Both polarities of siPSTVd could be detected for positive samples inoculated in tomato (Rutgers) and potato, which mean gene silencing was induced after the infection of PSTVd. No siPSTVd were produced for mock treatment. For the same membrane, the mi159 and mi167 blotting were done. The results showed no significantly different for the miRNA level for positive and negative samples. Our analyses showed PSTVd is unlikely to affect the pathway of endogenous miRNAs, at least for the main miRNA of both mi159 and mi167.
Studying the strategies that viroids infect a plant also helps to address basic molecular and cellular processes. It’s significant to understand the structure, function and pathway of pathogenicity. Meanwhile, it will provide important principle value for disclosing the mechanism of gene silencing and interaction between viroid host and pathogen, and also provide the reference of defence to viroid.
引文
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