黑腐皮壳侵染苹果的组织细胞学及转录组学研究
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摘要
由黑腐皮壳(Valsa mali)引起的苹果树腐烂病,是我国苹果生产上危害最为严重的枝干皮层腐烂病害,该病害在我国分布广、危害重、防治难,被果农称为苹果树“癌症”。病害轻时引起树皮大面积腐烂坏死、树势衰弱、苹果产量和品质下降；严重时引起主干、大枝以及整树枯死,甚至造成毁园,给果农带来严重经济损失,已成为制约我国苹果产业发展的重要因素。生产上对该病害的防治主要采取刮除病斑结合药剂防治的方法,但其防治效果很差且费工费时。所以,对该病害持续控制的关键技术进行研究已经成为目前苹果生产中急需解决的重大问题,而要尽快解决腐烂病的防治问题,揭示该病菌的侵染过程及其致病机理显得尤为迫切。因此,本论文从以上问题出发,采用生物电镜技术揭示病菌的侵染过程,并结合二代测序技术及PEG介导的病菌遗传转化体系,挖掘病菌的致病相关基因并对其功能进行验证,共取得了以下重要研究结果：
1.利用电镜技术首次在国际上系统揭示了黑腐皮壳菌分生孢子在苹果树皮上的侵染过程。研究结果表明,分生孢子在烫伤以及健康的富士苹果树皮表面均可萌发,但在烫伤树皮表面的萌发率较高,接种后24h平均分生孢子萌发率达87%,而在健康树皮表面为24.7%,且在健康树皮表面没有观察到芽管侵入寄主的现象。在烫伤树皮表面,分生孢子于接种后6h开始吸胀,由腊肠形吸胀至球形或椭球形；接种后16h可从孢子的不同部位萌发产生1-3个芽管,且芽管具分枝；接种后20h芽管可直接穿透寄主细胞侵入寄主组织,并不形成附着胞等特化的侵染结构；接种后4d病菌菌丝体可扩展至皮层和韧皮部,引起树皮表面出现明显的腐烂症状；接种后15d病菌菌丝体继续扩展,并深入木质部导管扩展,同时在表皮形成分生孢子器。组织学观察发现,病菌菌丝体周围的寄主细胞消解,组织解离；细胞学观察表明,病菌菌丝体主要在皮层和韧皮部的细胞间隙扩展,也可在细胞壁内及木质部导管中扩展危害,导致寄主细胞出现质壁分离、细胞壁降解,原生质体凝结、细胞器消解、细胞坏死等。
2.利用酶-胶体金及免疫细胞化学标记技术,对植物细胞壁的主要成分纤维素、木聚糖和果胶质进行了细胞化学标记。酶-胶体金标记结果表明,与健康寄主细胞壁相比,受侵染的寄主细胞壁上纤维素和木聚糖的金标记密度虽有减少,但差异不显著；而果胶的金标记密度与健康对照相比显著下降,表明寄主细胞壁的果胶成分被大量降解,因而推测病菌分泌的果胶酶在侵染致病过程中起着重要的作用。
3.利用High-Seq2000测序平台,分别对黑腐皮壳菌菌丝体及其侵染的苹果树皮病组织的转录组进行测序分析。测序共获得2个样本的原始数据超过3.5Gb, de novo拼接共获得66,982个contig,预测获得13,046个编码蛋白基因；采用FPKM法计算各基因在2个样本中的差异表达情况,共分析获得差异表达基因437个,在侵染中上调表达的有139个；基因功能注释发现,139个上调表达基因中包含16个细胞壁水解酶基因和10个次生代谢相关基因；对差异表达基因进行GO和KEGG功能富集,分析结果表明在黑腐皮壳菌侵染过程中,淀粉和糖代谢、果胶裂解通路及水解酶基因等明显富集；PHI(Pathogen-Host Interaction database)注释和生物信息学预测,共得到585个致病相关基因以及215个效应蛋白；此外,以G6PDH为内参基因,对随机挑选的15个差异表达基因进行了qRT-PCR验证,结果与转录组基本一致。
4.利用PEG介导的黑腐皮壳菌转化体系,对转录组中预测获得的2个上调表达的果胶酶基因m.12056(Vmpg-2)和m.13113(Vmpg-3)进行了功能验证。基于2个果胶酶基因编码区的侧翼序列,设计引物从病菌基因组中扩增上下游同源片段,以含潮霉素的质粒PHIG2RHPH2-GFP-GUS为模板,扩增潮霉素全长,利用Double joint-PCR技术成功构建了Vmpg-2和Vmpg-3的基因敲除盒。利用PEG介导的原生质体转化法,以潮霉素为筛选标记筛选阳性转化子,其中Vmpg-2敲除后没有获得阳性转化子。Vmpg-3敲除后共获得152个阳性转化子,转化子的PCR验证共获得6个阳性克隆,对这6个PCR检测阳性的转化子提取基因组DNA,以潮霉素片段为探针进行Southern杂交验证,获得1个Vmpg-3基因缺失突变株。并采用离体叶片针刺接种法,对Vmpg-3缺失突变株进行了致病力鉴定,结果表明Vmpg-3缺失突变体的致病力有所下降,但与野生型菌株相比差异不显著。表明Vmpg-3对黑腐皮壳菌的致病力有一定影响,但并非致病力的决定因子。
Apple valsa canker, caused by the fungus Valsa mali Mayabe et Yamada, anamorph: Cytospora sacculus [Schwein.] Gvrit., is one of the major diseases of apple in China. However, limited knowledge exists about the infection process and the mechanisms of the fungal pathogenicity, especially the development of the pathogen in host tissues and the genes involved in fungal pathogenesis, which will impede to develop efficient management strategies to control the apple valsa canker in apple. Thus, the objectives of the current study were (1) to elucidate the behavior and infection processes including conidia germination, pen-etration and spread in host tissues of V. mali using light, scanning and transmission electron microscopy.(2) Enzyme-and immune-gold labeling was conducted to detect the cell wall components alteration.(3) Based on the transcriptome analysis to explicited genes involved in the fungal pathogenesis.(4) Knockout the pectinase gene from the V. mali genome based on the PEG mediated transformation to detect the function of pectinase during the fungal infection.
1, the infection process of V. mali, the causal agent of apple canker, in apple (Malus domestica cv. Fuji) tissue was investigated by light and electron microscopy. The germination pattern of conidia was sim-ilar on wounded or intact twigs, but there was a time delay on intact bark. On intact bark tissue, conidia swell-ing could be observed at16h post inoculation (hpi) and conidia germinated at20hpi, however, no infection was observed. And the germinaton ratio was significantly difference on wounded and intact bark,87%of the conidia were germinated on wounded bark while24.7%of the conidia were germinated on the intact bark. On the wounded twig surface, conidia swelled at6hpi, and germinated at16hpi. Direct penetration of germ tubes was observed by20hpi and the pathogen caused canker lesions4days post inoculation (dpi) on wounded twigs and colonized in cortex and phelome tissues. By15dpi, hyphae colonized all bark tissues and xylem vessels and generated pycnidia on the canker region under epidermal. Electron microscopy observation of the canker region showed that fungal hyphae mainly spread intercellularly causing severe tissue maceration and cell necrosis. Fungal colonization resulted in marked alterations in host tissues including plasmolysis and degeneration of protoplasts and cell walls.
2, to illustration the function of cell wall enzymes produced by V. mali, cytochemical labeling was conducted by the enzyme-and immuno-gold of cell wall components of the infected tissues. Cellulase and xylanse-gold labeling showed that the density of gold particles of cellulose and xylan was difference insignificantly. However, the pectin over the infected cell wall showed a significant increase in gold particles density. The results indicated that pectinases were involved in pathogenesis of V. mali of apple tissue rather than the cellulase or xylanase.
3, a better understanding of this host-pathogen interaction is urgently needed to improve management strategies. In the current study we sequenced the transcriptomes of V. mali during infection of apple bark and mycelium grown in axenic culture using Illumina RNA-Seq technology. A total of66,982contigs were assembled and resulted in13,046genes. We identified437genes that were differentially expressed during fungal infection compared to fungal mycelium grown in axenic culture. One hundred and thirty nine of these437genes showed more than three fold higher transcript abundance during infection. Functional categorization of these139genes revealed that most of them were related to cell wall hydrolysis and secondary metabolite biosynthesis. GO and KEGG enrichment analyses of the induced genes suggest prevalence of genes associated with pectin catabolic, hydrolase activity and secondary metabolite biosynthesis during fungal infection. Our results indicate that cell wall degradation accompanied by cell necrosis-probably caused by secondary metabolites-is essential for disease establishment. Furthermore,585putative pathogenicity determinants and215candidate effectors in V. mali were identified. Additionally,15different expressed genes were chosen for qRT-PCR verification and the results were consistent to FPKM analysis.
4, based on the transcriptome seuqneces, two pectinase genes, m.12056(Vmpg-2) and m.13113(Vmpg-3), were chosen for gene function verification. Double-joint PCR was used for the gene knockout cassetes development, and the PEG mediated transformation was used for the pectinase genes knockout from the V. mali genome. Unfortunately, there was no transformant abtained from Vmpg-2deletion. And a total of152transformants were collected from Vmpg-3deletion. Screening the Vmpg-3deletion transformants on the PDA medium that contain100μg/mL hygromycin, PCR applification and the southern blot verification, a mutant of Vmpg-3gene deletion was obtained. Bioassay of the Vmpg-3deletion mutant on the exised leaves was performed and the results showed that the pathogenicity of the Vmpg-3delection mutant decreased but the difference was insignificantly compared with the wild type. The pectinase gene deletion indicated that Vmpg-3affected the pathogenicity of V. mali but really not the determinated factor.
1.利用电镜技术首次在国际上系统揭示了黑腐皮壳菌分生孢子在苹果树皮上的侵染过程。研究结果表明,分生孢子在烫伤以及健康的富士苹果树皮表面均可萌发,但在烫伤树皮表面的萌发率较高,接种后24h平均分生孢子萌发率达87%,而在健康树皮表面为24.7%,且在健康树皮表面没有观察到芽管侵入寄主的现象。在烫伤树皮表面,分生孢子于接种后6h开始吸胀,由腊肠形吸胀至球形或椭球形；接种后16h可从孢子的不同部位萌发产生1-3个芽管,且芽管具分枝；接种后20h芽管可直接穿透寄主细胞侵入寄主组织,并不形成附着胞等特化的侵染结构；接种后4d病菌菌丝体可扩展至皮层和韧皮部,引起树皮表面出现明显的腐烂症状；接种后15d病菌菌丝体继续扩展,并深入木质部导管扩展,同时在表皮形成分生孢子器。组织学观察发现,病菌菌丝体周围的寄主细胞消解,组织解离；细胞学观察表明,病菌菌丝体主要在皮层和韧皮部的细胞间隙扩展,也可在细胞壁内及木质部导管中扩展危害,导致寄主细胞出现质壁分离、细胞壁降解,原生质体凝结、细胞器消解、细胞坏死等。
2.利用酶-胶体金及免疫细胞化学标记技术,对植物细胞壁的主要成分纤维素、木聚糖和果胶质进行了细胞化学标记。酶-胶体金标记结果表明,与健康寄主细胞壁相比,受侵染的寄主细胞壁上纤维素和木聚糖的金标记密度虽有减少,但差异不显著；而果胶的金标记密度与健康对照相比显著下降,表明寄主细胞壁的果胶成分被大量降解,因而推测病菌分泌的果胶酶在侵染致病过程中起着重要的作用。
3.利用High-Seq2000测序平台,分别对黑腐皮壳菌菌丝体及其侵染的苹果树皮病组织的转录组进行测序分析。测序共获得2个样本的原始数据超过3.5Gb, de novo拼接共获得66,982个contig,预测获得13,046个编码蛋白基因；采用FPKM法计算各基因在2个样本中的差异表达情况,共分析获得差异表达基因437个,在侵染中上调表达的有139个；基因功能注释发现,139个上调表达基因中包含16个细胞壁水解酶基因和10个次生代谢相关基因；对差异表达基因进行GO和KEGG功能富集,分析结果表明在黑腐皮壳菌侵染过程中,淀粉和糖代谢、果胶裂解通路及水解酶基因等明显富集；PHI(Pathogen-Host Interaction database)注释和生物信息学预测,共得到585个致病相关基因以及215个效应蛋白；此外,以G6PDH为内参基因,对随机挑选的15个差异表达基因进行了qRT-PCR验证,结果与转录组基本一致。
4.利用PEG介导的黑腐皮壳菌转化体系,对转录组中预测获得的2个上调表达的果胶酶基因m.12056(Vmpg-2)和m.13113(Vmpg-3)进行了功能验证。基于2个果胶酶基因编码区的侧翼序列,设计引物从病菌基因组中扩增上下游同源片段,以含潮霉素的质粒PHIG2RHPH2-GFP-GUS为模板,扩增潮霉素全长,利用Double joint-PCR技术成功构建了Vmpg-2和Vmpg-3的基因敲除盒。利用PEG介导的原生质体转化法,以潮霉素为筛选标记筛选阳性转化子,其中Vmpg-2敲除后没有获得阳性转化子。Vmpg-3敲除后共获得152个阳性转化子,转化子的PCR验证共获得6个阳性克隆,对这6个PCR检测阳性的转化子提取基因组DNA,以潮霉素片段为探针进行Southern杂交验证,获得1个Vmpg-3基因缺失突变株。并采用离体叶片针刺接种法,对Vmpg-3缺失突变株进行了致病力鉴定,结果表明Vmpg-3缺失突变体的致病力有所下降,但与野生型菌株相比差异不显著。表明Vmpg-3对黑腐皮壳菌的致病力有一定影响,但并非致病力的决定因子。
Apple valsa canker, caused by the fungus Valsa mali Mayabe et Yamada, anamorph: Cytospora sacculus [Schwein.] Gvrit., is one of the major diseases of apple in China. However, limited knowledge exists about the infection process and the mechanisms of the fungal pathogenicity, especially the development of the pathogen in host tissues and the genes involved in fungal pathogenesis, which will impede to develop efficient management strategies to control the apple valsa canker in apple. Thus, the objectives of the current study were (1) to elucidate the behavior and infection processes including conidia germination, pen-etration and spread in host tissues of V. mali using light, scanning and transmission electron microscopy.(2) Enzyme-and immune-gold labeling was conducted to detect the cell wall components alteration.(3) Based on the transcriptome analysis to explicited genes involved in the fungal pathogenesis.(4) Knockout the pectinase gene from the V. mali genome based on the PEG mediated transformation to detect the function of pectinase during the fungal infection.
1, the infection process of V. mali, the causal agent of apple canker, in apple (Malus domestica cv. Fuji) tissue was investigated by light and electron microscopy. The germination pattern of conidia was sim-ilar on wounded or intact twigs, but there was a time delay on intact bark. On intact bark tissue, conidia swell-ing could be observed at16h post inoculation (hpi) and conidia germinated at20hpi, however, no infection was observed. And the germinaton ratio was significantly difference on wounded and intact bark,87%of the conidia were germinated on wounded bark while24.7%of the conidia were germinated on the intact bark. On the wounded twig surface, conidia swelled at6hpi, and germinated at16hpi. Direct penetration of germ tubes was observed by20hpi and the pathogen caused canker lesions4days post inoculation (dpi) on wounded twigs and colonized in cortex and phelome tissues. By15dpi, hyphae colonized all bark tissues and xylem vessels and generated pycnidia on the canker region under epidermal. Electron microscopy observation of the canker region showed that fungal hyphae mainly spread intercellularly causing severe tissue maceration and cell necrosis. Fungal colonization resulted in marked alterations in host tissues including plasmolysis and degeneration of protoplasts and cell walls.
2, to illustration the function of cell wall enzymes produced by V. mali, cytochemical labeling was conducted by the enzyme-and immuno-gold of cell wall components of the infected tissues. Cellulase and xylanse-gold labeling showed that the density of gold particles of cellulose and xylan was difference insignificantly. However, the pectin over the infected cell wall showed a significant increase in gold particles density. The results indicated that pectinases were involved in pathogenesis of V. mali of apple tissue rather than the cellulase or xylanase.
3, a better understanding of this host-pathogen interaction is urgently needed to improve management strategies. In the current study we sequenced the transcriptomes of V. mali during infection of apple bark and mycelium grown in axenic culture using Illumina RNA-Seq technology. A total of66,982contigs were assembled and resulted in13,046genes. We identified437genes that were differentially expressed during fungal infection compared to fungal mycelium grown in axenic culture. One hundred and thirty nine of these437genes showed more than three fold higher transcript abundance during infection. Functional categorization of these139genes revealed that most of them were related to cell wall hydrolysis and secondary metabolite biosynthesis. GO and KEGG enrichment analyses of the induced genes suggest prevalence of genes associated with pectin catabolic, hydrolase activity and secondary metabolite biosynthesis during fungal infection. Our results indicate that cell wall degradation accompanied by cell necrosis-probably caused by secondary metabolites-is essential for disease establishment. Furthermore,585putative pathogenicity determinants and215candidate effectors in V. mali were identified. Additionally,15different expressed genes were chosen for qRT-PCR verification and the results were consistent to FPKM analysis.
4, based on the transcriptome seuqneces, two pectinase genes, m.12056(Vmpg-2) and m.13113(Vmpg-3), were chosen for gene function verification. Double-joint PCR was used for the gene knockout cassetes development, and the PEG mediated transformation was used for the pectinase genes knockout from the V. mali genome. Unfortunately, there was no transformant abtained from Vmpg-2deletion. And a total of152transformants were collected from Vmpg-3deletion. Screening the Vmpg-3deletion transformants on the PDA medium that contain100μg/mL hygromycin, PCR applification and the southern blot verification, a mutant of Vmpg-3gene deletion was obtained. Bioassay of the Vmpg-3deletion mutant on the exised leaves was performed and the results showed that the pathogenicity of the Vmpg-3delection mutant decreased but the difference was insignificantly compared with the wild type. The pectinase gene deletion indicated that Vmpg-3affected the pathogenicity of V. mali but really not the determinated factor.
引文
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