水稻条斑病菌致病相关基因的鉴定与功能研究

英文题名：Identification and Functional Analysis of Pathogenicity-Related Genes of Xanthomonas Oryzae Pv. Oryzicola
作者：郭威
论文级别：博士
学科专业名称：植物病理学
中文关键词：稻黄单胞菌 ; 突变体库 ; 糖代谢 ; 致病性 ; 毒性 ; hrp基因 ; 效应蛋白
英文关键词：Xanthomonas oryzae ; mutant library ; carbon metabolism ; pathogenicity ; virulence ; hrp gene ; effector
学位年度：2011
导师：陈功友
学科代码：090401
学位授予单位：南京农业大学

摘要

水稻条斑病菌(Xanthomonas oryzae pv. oryzicola, Xoc)是水稻黄单胞菌(Xanthomonas oryzae)种下两致病变种之一,引起水稻细菌性条斑病(Bacterial Leaf Streak,简称条斑病,BLS)。近年来该病发生日趋严重,成为水稻上第四大病害。该病原菌从气孔或伤口侵入,在薄壁细胞间繁殖与危害,因受叶脉限制产生条斑病症状。由于感病杂交水稻大面积推广,且生产上无有效的抗条斑病种质资源,水稻安全生产受到严重的威胁。近年来,X. oryzae pv. oryzicola大量致病性相关基因(如hrp、avr、 rpf及其它毒性候选基因等)的研究揭示,毒性相关基因的鉴别是全面解析病原菌致病机理以及发展高效生物防治的基础。
     目前,构建植物病原菌突变体库是挖掘新基因和进行功能基因组学研究的有效途径。因此,为了从全基因组范围内挖掘X. oryzae pv. oryzicola致病性相关因子,本研究以RS105为出发菌株,构建了一个包含25,000突变子的X. oryzae pv. oryzicola Tn5转座子插入突变体库,约5×ORF于基因组(约4,600个ORF)的覆盖量。Southern Blot分析表明,Tn5插入突变体库是稳定的、随机的。将每个突变子分别接种感病寄主水稻(cv. Shanyou63),经第一轮筛选共获得了1,753个致病性完全丧失或毒性减弱的突变体。为了进一步验证其在水稻上的致病表型,经第二轮筛选,共获得了114个致病性完全丧失或毒性显著减弱的突变体,其中致病性完全丧失的14个。随后,将114个致病性完全丧失或毒性显著减弱的突变体分别接种非寄主烟草(cv. Xanthi),共获得23个过敏性反应(hypersensitive response, HR)丧失或明显减弱的突变体,其中HR完全丧失的15个。以上突变体的获得,为分析X. oryzae pv. oryzicola致病性相关基因提供了材料基础。
     为了快速准确地确定Tn5插入的位点和具体功能基因,本研究采用热不对称交错PCR(TAIL-PCR)技术对114个致病性完全丧失或显著减弱的突变体进行了鉴别。结果显示,转座子Tn5插入在致病性相关基因上,包括hrp、avr、rpf、wxoc、代谢相关基因、conserved hypothetical protein及其它毒性基因等。大批致病相关基因的发现,不仅为从分子水平上解析X. oryzae pv. oryzicola的致病机理,而且对于揭示植物-病原物互作的致病性和抗病性,具有全局性的科学价值。
     关键毒性基因的功能鉴定是理解X. oryzae pv. oryzicola致病机理的先决条件。为此,对27个在水稻上完全丧失致病性或毒性显著减弱的突变体进行了分析。其中14个突变体完全丧失在水稻上的致病性和在烟草上激发过敏性反应(hypersensitive response, HR)的能力(表型为Pth-/HR-);另外13个突变体全毒性显著减弱,但仍具有在烟草上激发HR的能力(Vir-/HR+)。Tn5插入基因序列分析揭示,14个Pth-/HR-突变体是Tn5插入在以下基因上：hrcC(2个)、hrcT、hrcV(4个)、hpaP、hrcQ、(2个)/hrpF、hrpG和hrpX(2个)；13个Vir-/HR+突变体被Tn5插入的基因分别是：tal-C10c-like(TAL效应分子)、rpfC(致病性调控子)、oxyP(过氧化压力调控子)、dsbC(二硫化合物异构酶)、opgH(葡聚糖生物合成葡(萄)糖基转移酶H)、rfbA(1-磷酸葡萄糖乙酰基转移酶)、amtR(氨基转移酶)、purF(氨基磷酸核糖转移酶)、thrC(苏氨酸合成酶)、trpA(色氨酸合成酶a亚基)和3个功能未知蛋白的基因Xoryp_02235、Xoryp_00885和Xoryp_2910。即这27个突变体是Tn5插入在21个不同的ORFs上。此外上述13个全毒性减弱的突变体,功能互补都能恢复至野生型水平,这表明amtR、purF、thrC、trpA、Xoryp_02235、Xoryp_00885和Xoryp_22910是参与X. oryzae pv. oryzicola全毒性的新基因,未见在其它植物病原细菌中报道。Real-time PCR证明,上述7个新毒性基因在植物中是受诱导表达的,但是它们在参与X. oryzae pv. oryzicola致病机理上的详细功能,仍需进一步的研究。
     植物病原细菌与寄主互作的一个重要方面是病原菌在植物组织内获取营养的能力。碳水化合物的获取对于病原菌在寄主植物中生长繁殖、成功建立营养寄生关系至关重要。尽管代谢途径一般不认为是毒性因子,但是阐述碳水化合物获取与代谢的详细机制对于全面理解X. oryzae pv. oryzicola的寄生性和致病性具有重要科学意义。
     果糖-1,6-二磷酸醛缩酶(FbaB),是有机生物体糖酵解和糖异生途径中的一个重要代谢酶。X. oryzae pv. oryzicola基因组中唯一的fbaB基因突变,不仅导致病原菌丧失利用丙酮酸和苹果酸进行生长的能力,也延缓其利用果糖作为唯一碳源时的生长；而且也降低了胞外多糖(EPS)的产量及降低了细菌在水稻上毒性和生长。经序列分析发现fbaB启动子区含有一个不完全的PIP-box (Plant-inducible promoter, TTCGT-N9-TTCGT)。有意义的是,fbaB的表达受hrp调控子HrpG和HrpX的负调控,且PIP-box碱基置换改变了它们对fbaB的调控。Real-time PCR结果显示,RS105菌株中的fbaB在植物中是受诱导表达的；而且fbaB缺失抑制了hrpG和hrpX的表达,hrcC、hrpE和hpa3的转录反而增强,对其余的hrp-hrc-hpa基因表达没有影响。而碳源利用能力测定揭示,hrcC、hrpE和hpa3突变体相应减弱了病原菌利用丙酮酸和苹果酸的能力。另外,fbaB突变体在植物上的毒性和生长以及EPS的产量,功能互补能够完全恢复至野生型水平。这是第一次报道表明,X. oryzae pv. oryzicola吸收的碳水化合物在fbaB基因位点通过一个未知因子在调节hrp基因的表达上扮演着重要作用。
     另外,对X. oryzae pv. oryzicola全基因组搜索发现了两个编码6-磷酸葡萄糖脱氢酶的基因,催化6-磷酸葡萄糖转化成6-磷酸葡萄糖酸,在2-酮-3-脱氧-6-磷酸葡糖酸裂解途径(ED途径)与磷酸戊糖途径中发挥着重要作用。为了明确这两个基因的功能,本研究对X. oryzae pv. oryzicola中起主导作用的zwf(Xoryp_12765)基因进行了缺失突变。结果显示,zwf突变后,病原菌利用葡萄糖、果糖、蔗糖、甘露糖和半乳糖的能力显著降低,但不影响其利用丙酮酸或苹果酸的能力。这表明,zwf突变可能阻碍了磷酸戊糖途径和ED途径,但不影响糖异生途径。同时也发现zwf是受诱导表达的,相对于无糖条件下的,葡萄糖、蔗糖、果糖、甘露糖及半乳糖均显著增强zwf的转录水平达3倍以上。有趣的是,zwf突变导致DSF信号通路关键基因如rpfF、rpfG、clp基因的转录表达发生改变,这暗示,zwf可能参与对DSF下游某些毒性因子的调控。此外,zwf突变,X. oryzae pv. oryzicola胞外蛋白水解酶活性增强,胞外多糖的产量降低、游动性及水稻上的毒性减弱。经功能互补能够完全恢复至野生型水平。这些结果说明,zwf是X. oryzae pv. oryzicola全毒性所需的。
     6-磷酸葡萄糖异构酶在碳水化合物代谢中具有重要作用,可逆的催化6-磷酸葡萄糖转化成6-磷酸果糖。Xoryp_10540(pgi)是X. oryzae pv. oryzicola全基因组中6-磷酸葡糖异构酶唯一编码基因。实验表明,pgi突变致使病原菌不能有效利用果糖、蔗糖、甘露糖、丙酮酸,但是不影响其在葡萄糖或半乳糖作为唯一碳源的培养基上生长。值得一提的是,pgi突变导致DSF信号通路关键基因rpfF、rpfG、clp基因的转录表达发生显著改变。DSF信号检测显示,pgi突变体产生的DSF信号较野生型RS105水平明显减弱。这些结果提示,pgi突变可能对DSF信号调控网络下游基因的表达有一定的影响。同样地,pgi突变降低了病原菌的胞外多糖(EPS)的产量、游动性,并减弱病原菌在水稻上的毒性。功能互补能够完全恢复至野生型水平。这些结果说明,pgi是X. oryzae pv. oryzicola EPS产生和全毒性所需的。
     水稻白叶枯病菌(Xanthomonas oryzae pv. oryzae, Xoo)是水稻黄单胞菌(Xanthomonas oryzae)种下另一致病变种,通过T3SS将各类效应蛋白注入寄主植物细胞内,引起水稻白叶枯病(bacterial blight, BB),是水稻上三大病害之一。病原菌通过叶尖和叶缘上的水孔侵入水稻叶片,定殖于维管束中并在木质部进行传播。依据本实验室基因芯片数据,筛选获得一个参与X. oryzae pv. oryzae能量代谢的基因,PXO03531(ketoglutarate transport protein, kgtP)。该基因在hrpX或hrpG突变体中的表达显著下调。分析发现,kgtP启动子区存在一个不完全的PIP-box (TTCGA-N21-TTCGC),且其编码产物KgtP的N端前50个氨基酸具有典型的Ⅲ型分泌信号。这提示,X. oryzae pv. oryzae kgtP可能是HrpX的调节子及T3SS效应分子。RT-PCR实验证实,HrpX和HrpG正调控kgtP的表达。免疫杂交结果显示,KgtP依赖T3SS,但不依赖于T3S出口控制蛋白HpaB进行分泌。细胞定位结果显示KgtP定位在细胞膜上,推测其结合到植物细胞膜上从而有利于从植物体内获取α-酮戊二酸。kgtP缺失突变,减弱了病原菌在植物上的生长与毒性,且细菌不能在含有α-酮戊二酸或琥珀酸钠为唯一碳源的基本培养基上生长,功能互补能有效恢复至野生型水平。RT-PCR结果显示,X. oryzae pv. oryzae在加入α-酮戊二酸为唯一碳源的基本培养基或与水稻悬浮细胞互作,kgtP的表达受到显著诱导,表明kgtP是受诱导表达的。有趣的是,kgtP缺失突变可以导致水稻上合成α-酮戊二酸的异柠檬酸脱氢酶基因表达明显下降。据此推测,在腐生状态下,X. oryzae pv. oryzae借助KgtP把体外的α-酮戊二酸转运至细胞内；当与水稻细胞互作时,则在HrpX调控下进行表达,通过T3SS进行分泌,结合在寄主细胞膜上,并把寄主细胞内的α-酮戊二酸转运至细菌细胞内以获得营养。
Xanthomonas oryzae pv. oryzicola (Xoc) is one of two pathovars in Xanthomonas oryzae, causing serious bacterial leaf streak (BLS) in rice which becomes the fourth destructive rice diseases recently in China. The pathogen enters through leaf stomata or wounds and colonizes the parenchyma apoplast, causing interveinal lesions that appear as water soaked initially and then develop into translucent, yellow-to-white streaks. As the susceptible hybrid rice grows in large scale and particularly there is no simply inherited gene for resistance to the disease, rice production encounters a serious threat of security. In recent years, a number of pathogenicity-related genes, such as hrp, avr, rpf and other candidate virulence genes, have been discovered in X. oryzae pv. oryzicola, suggesting that genome-widely identification of virulence genes is necessary for fully understanding the bacterial pathogenicity and for developing biotechnology to control the disease.
     Currently, it is accepted that construction of a Tn5-tagged mutant library is an effective approach to mine pathogenicity-related genes at functional genomic level in various plant pathogens. Therefore, to genome-widely mine pathogenesis-related genes of X. oryzae pv. oryzicola, a Tn5transposon-mediated mutation library was generated using the wild-type RS105as a recipient in this study. Twenty-five thousand transformants were produced by inserting the Tn5transposon, appropriately corresponding to5×ORF coverage of the genome. Southern Blot analysis suggested that Tn5-mediated mutant library is stable and random. Each transformant of the library is inoculated into susceptible host rice (cv. Shanyou63) to screen candidate virulence genes. Totally, in comparison to the wild-type, there were1,753mutants with virulence reduced or lost after the first screening. In order to accurately confirm the phenotypes achieved, we re-inoculated those mutants into rice seedlings. After the second screening,114mutants were obtained with virulence reduced or lost compared to the wild-type. Of those, there were14mutants completely losing pathogenicity in rice. Finishing the virulence assay in rice, we then injected114mutants into tobacco (cv. Xanthi) for HR induction assay. There were23 mutants with the ability of HR induction reduced or lost, compared to the wild-type RS105. Of these, there were15mutants completely losing the ability to trigger HR in tobacco. The mutants identified above may provide a basis for analysis of pathogenesis-related genes in X. oryzae pv. oryzicola.
     In order to rapidly and accurately identify Tn5insertion positions of corresponding genes in each mutants of this library, thermal asymmetric interlaced PCR (TAIL-PCR) was adopted to isolate Tn5-tagged genes of114mutants. The results suggest that random insertions of Tn5targets set at a large number of genes associated with the pathogenicity, including hrp, avr, rpf, wxoc, metabolism-related genes, genes encoding conserved hypothetical proteins, and other known or unknown virulence factors. Novel pathogenicity-related genes were revealed that they play important roles in pathogenesis of X. oryzae pv. oryzicola in rice at molecular level.
     Identification of key virulence genes/factors is prerequisite for understanding pathogenesis of X. oryzae pv. oryzicola in rice. Therefor,27Tn5insertional mutants that either completely lost pathogenicity or reduced virulence in rice were thorough analysed. Specifically,14mutants completely lost pathogenicity in rice and the ability to trigger HR in tobacco (classified as Pth-/HR-) and13reduced the full virulence in rice but kept HR induction in tobacco (Vir-/HR+). Sequencing analysis of the Tn5-tagged genes indicated that these14Pth-/HR-mutants include hrcC (2mutants), hrcT, hrcV (4mutants), hpaP, hrcQ (2mutants), hrpF, hrpG and hrpX (2mutants) genes. The13Vir-/HR+mutants include tal-C10c-like (encodes a TAL effector), rpfC (a regulator of pathogenicity factors), oxyP (an oxidative stress transcriptional regulator), dsbC (a disulfide isomerase), opgH (a glucans biosynthesis glucosyltransferase H), rfbA (a glucose-1-phosphate thymidylyltranssferase), amtR (an aminotransferase), purF (an amidophosphoribosyl-transferase), thrC (a threonine synthase), trpA (a tryptophan synthase alpha subunit), as well as3hypothetical protein coding genes Xoryp_02235, Xoryp_00885and Xoryp_22910. Together, these27Tn5insertions are located in21different open reading frames (ORFs). Reduced virulence by the thirteen mutants above was complemented to the wild-type level in trans by the present of the corresponding wild-type genes above. These results suggested that amtR, purF, thrC, trpA, Xoryp_02235, Xoryp_00885and Xoryp_22910are novel virulence genes involved in X. oryzae pv. oryzicola pathogenesis in rice. Real-time PCR demonstrated that the seven novel virulence genes were significantly (P=0.01, t test) induced in planta, although their precise functions during X. oryzae pv. oryzicola pathogenesis await further investigation.
     One important aspect of interactions between plant pathogens and their hosts is the ability of the pathogen to obtain nutrients within the plant tissue. The ability to acquire carbohydrate is essential for a pathogen to propagate and establish an infection relationship in host plant successfully. Although metabolic pathways are generally not considered to be virulence factors, elucidation of the mechanism to acquire and metabolize carbohydrates is critically important for fully understanding the pathogenicity of X. oryzae pv. oryzicola.
     Fructose-bisphophate aldolase (FbaB), is an enzyme in glycolysis and gluconeogenesis in living organisms. The mutagenesis in a unique fbaB gene of X. oryzae pv. oryzicola, led the pathogen not only to be unable to use pyruvate and malate for growth and delay its growth when fructose was used as the sole carbon source, but also to reduce extracellular polysaccharide (EPS) production and impaired bacterial virulence and growth in rice. Intriguingly, the fbaB promoter contains an imperfect PIP-box (plant-inducible promoter)(TTCGT-N9-TTCGT). The expression of fbaB was negatively regulated by a key hrp regulatory HrpG and HrpX cascade. Base substitution in the PIP-box altered the regulation of fbaB with the cascade. Furthermore, real-time PCR suggested that the expression of fbaB in X. oryzae pv. oryzicola RS105strain was inducible in planta rather than in a nutrient-rich medium. Except other hrp-hrc-hpa genes, the expression of hrpG and hrpX was repressed and the transcripts of hrcC, hrpE and hpa3were enhanced when fbaB was deleted. The mutation in hrcC, hrpE or hpa3reduced the ability of the pathogen to acquire pyruvate and malate. In addition, bacterial virulence and growth in planta and EPS production in R△fbaB mutant were completely restored to the wild-type level by the presence of fbaB in trans. This is the first report to demonstrate that carbohydrates, assimilated by X. oryzae pv. oryzicola, play critical roles in coordinating hrp gene expression through a yet unknown regulator.
     In addition, two genes encoding glucose6-phosphate dehydrogenase, which catalyzes glucose6-phosphate into gluconate6-phosphate and plays an important role in Entner-Doudoroff pathway (ED pathway) and pentose phosphate pathway, were identified from the mutant library of X. oryzae pv. oryzicola. In order to clarify the functions of these two genes, we took zwf (Xoryp_12765) as our target since it is reported that it plays a dominant role in the pathways above in Xanthomonas species. The deletion mutation in zwf of X. oryzae pv. oryzicola could significantly reduce the ability of pathogen to use glucose, fructose, sucrose, mannose and galactose for growth other than pyruvate and malate. These suggest that the zwf mutation may hinder the pentose phosphate pathway and ED pathway instead of glycolysis. Simultaneously, the expression of zwf was strongly induced by glucose, sucrose, fructose, mannose and galactose at least3times higher than that by the medium without sugar. Interestingly, The mutagenesis in this unique zwf gene of X. oryzae pv. oryzicola also led the alteration in the expression of key genes in DSF signaling pathway, such as rpfF, rpfG and clp, suggesting that zwf may be involved in regulation of virulence factors in the downstream of DSF signaling. In addition, the deletion mutation in zwf resulted in impairment of bacterial virulence in planta, and reduction of motility and extracellular polysaccharide (EPS), but enhanced the activity of extracellular protease. Bacterial virulence and motility and EPS production in RAzwf mutant were completely restored to the wild-type level by the presence of zwf in trans. All these results indicate that zwf is required for the full virulence of X. oryzae pv. oryzicola in rice.
     Glucose6-phosphate isomerase, reversibly converting glucose6-phosphate to fructose6-phosphate, plays an important role in carbohydrate metabolism. There is only one Xoryp_10540(pgi) gene, encoding6-phosphate glucose isomerase, in the genome of X. oryzae pv. oryzicola. The mutagenesis in pgi led the pathogen unable to use fructose, sucrose, mannose and pyruvate for growth effectively, but did not affect its growth when glucose or galactose as the sole carbon source. It is worth mentioning that the mutation in pgi also resulted in alteration of key genes in DSF signaling pathway, such as rpfF, rpfG and clp. Furthermore, detection of DSF signal showed the mutant significantly reduced DSF production compared to the wild-type RS105. These results indicated that, the mutation in pgi may have impacts on the downstream of DSF signal regulatory. Similarly, the deletion in pgi not only impaired bacterial virulence in planta, but also reduced bacterial motility and EPS production. Bacterial virulence and motility and EPS production in RApgi mutant were completely restored to the wild-type level by the presence of pgi in trans. All these results indicate that pgi is essential for EPS production and full virulence of X. oryzae pv. oryzicola.
     Xanthomonas oryzae pv. oryzae (Xoo) is another pathovar of Xanthomonas oryzae that also possesses a type-Ⅲ secretion system (T3SS) to deliver repertoires of T3SS effectors into plant cell to cause serious bacterial blight (BB) in rice. The pathogen invades rice leaves through hydathode openings on leaf tip and leaf margin, and then colonizes the vascular tissues by propagating in the xylem. Based on microarray data in our laboratory, an energy metabolism related-gene, PXO_03531(ketoglutarate transport protein, kgtP), in X. oryzae pv. oryzae was found that it was remarkably downregulated in hrpX or hrpG mutant. Bioinformatic analysis revealed that there is an imperfect PIP-box (TTCGA-N21-TTCGC) in the promoter region of kgtP and the first50amino acids of N-terminal in KgtP possesses a typical T3SS signal. All the above indicated that kgtP may be a HrpX regulon and a T3SS effector in X. oryzae pv. oryzae. RT-PCR assay demonstrated that the kgtP expression was positively regulated by the HrpX and HrpG cassette. Southern Blot assay indicated that the KgtP was secreted in an HpaB-independent manner through the T3SS of X. oryzae pv. oryzae PXO99A strain. Subcellular localization showed that KgtP could be located into plant cell membrane, suggesting that it binds to plant cell membrane to transport a-ketoglutarate from plant cells into bacterial cells. The deletion mutation in kgtP reduced not only bacterial virulence and growth in planta, but also the growth in a minimal medium without a-ketoglutaric acid or sodium succinate. The reduced virulence and the impairment of a-ketoglutaric acid utilization in the kgtP mutant were restored to the wild-type levels by the presence of kgtP in trans. The kgtP expression was strongly induced when the pathogen either grew in the minimal medium supplemented with a-ketoglutaric acid or interacted with rice cells, suggesting the expression of kgtp is induced. Importantly, the expression of OsIDH, which is responsible for the synthesis of a-ketoglutaric acid in rice, was enhanced when kgtP presents in the pathogen. Taken together, we hypothesize that KgtP transports a-ketoglutaric acid to X. oryzae pv. oryzae from outside substrates for saprophytic growth and from rice cells for parasitism.

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