水稻白叶枯病菌△gacAxoo和△fleQxoo突变体基因芯片转录谱分析
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摘要
水稻白叶枯病是由黄单胞菌水稻致病变种(Xanthomonas oryzae pv．oryzae，简称Xoo)引起的、严重危害水稻生产的一种细菌性病害。通过对Xoo致病相关基因的研究，使人们对Xoo致病机理以及与水稻互作的分子基础有了不少认识。然而，Xoo致病机制非常复杂，许多毒性和无毒机制目前仍不得而知，致病基因表达调控及其网络尚不清楚。前期研究已鉴定出Xoo TCS(two-component system)应答调控因子GacAxoo和鞭毛基因簇转录调控因子FleQxoo，它们参与病菌毒性和鞭毛运动性的调控。为了进一步从基因组水平上阐明GacAxoo和FleQxoo的调控作用及其机理，本研究利用基因芯片技术，比较分析了Xoo野生型菌株PXO99~A及其突变体ΔgacAxoo和ΔfleQxDD的基因转录谱，旨在发现GacAxoo和FleQxoo转录调控元(regulon)，为全面揭示Xoo基因表达调控网络提供重要的信息。
利用Xoo菌株KACC10331全基因组序列信息，选择出560个致病相关基因、调控因子基因、特有基因和保守基因、以及鞭毛基因簇基因，点制了一批Xoo基因芯片。对在丰富培养基(NBY)和hrp诱导培养基(XOM2)中生长到对数生长期(OD=1.2)的PXO99~A及其突变体ΔgacAxoo和ΔfleQxoo转录谱进行了比较测定。
与NBY培养条件相比，PXO99~A在XOM2中培养时有17个基因发生了差异性表达，其中10个基因上调表达，7个下调表达。在10个表达上调的基因中，7个为T3SS(hrpB、hrpB1、hrpB3、hrpD6、hrpF)及其效应子(hpa1、hpaB)基因，其中hpa1上调表达最为显著，可达到13倍。Xoo hrp基因的表达显著地受到诱导型培养基XOM2培养条件的诱导。
与PXO99~A相比，ΔgacAxoo在XOM2中培养时有28个基因发生了差异性表达，其中17个基因上调表达，11下调表达。在17个表达上调的基因中，1个为vieA基因，7个为假定蛋白的基因。这些基因受到GacAxoo负调控而抑制表达。在11个表达下调的基因中，1个为GGDEF家族成员基因，1个T3SS效应子基因hpa1，4个为鞭毛基因(flgC、fliC、fliO、cheA)。GacAxoo不仅调控了T3SS效应子基因hpa1的表达，而且也通过正向调控了部分鞭毛基因的表达，影响Xoo鞭毛运动性。此外，GacAxoo还可能通过正、负向调控vieA和GGDEF家族成员基因，影响第二信使c-di-GMP的代谢，从而调控了Xoo的诸多生物学性状。
与PXO99~A相比，ΔfleOxoo在NBY中培养时有16个基因发生了差异性表达，其中12个基因上调表达，4个下调表达。在12个表达上调的基因中，4个为T2SS(xpsJ、xpsL、xpsN)及其效应子(egl)基因，3个为胞外降解酶(polygalacturonase，protease，cellulase S)基因，3个为鞭毛基因簇(flhA、fliK、fliO)基因，1个为GGDEF家族成员基因，1个为O抗原生物合成基因(rbfC)。这些基因的表达受到FleQxoo负调控而被抑制。4个下调表达的基因包括鞭毛蛋白基因fliE、hrpB4、果胶酯酶基因和蛋白酶基因。RT-PCR分析验证了fliE基因的表达显著地受到FleQxoo正调控。值得注意的是，fleQxoo基因自身的表达在ΔfleQxoo中非常显著，而在PXO99~A中基本不表达或表达量极低。结果表明，fleQxoo基因表达可能受到自身的抑制。
总之，本研究利用基因芯片技术，通过构建Xoo及其ΔgacAxoo和ΔfleQxoo的基因转录谱，鉴别了GacAxoo和FleQxoo的部分调控元和差异性表达的基因，深入分析这些基因表达和调控的生物学信息，有助于阐明Xoo致病的分子机制。
Bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) is one of most important bacterial diseases of rice worldwide. Understanding of molecular basis of interactions between rice and Xoo has been promoted by elucidating the roles of genes associated with pathogenesis. Nevertheless, the pathogenicity mechanisms of Xoo are complex, many aspects of virulence and avirulence mechanisms are still not understood. The whole genome sequence of Xoo has provided a very useful tool to study the pathogenicity/virulence mechanisms on genome-wide scale.
GacAxoo, a response regulator of TCS and FleQxoo, a transcriptional regulator of flagellar gene cluster have been indentified in our previous study, which function as the regulators during the expression of virulence and motility of Xoo. To understand the regulatory roles and mechanisms of GacAxoo and FleQxoo on the genome scale, the transcriptional profiles of△gacAxoo,△fleQxoo and wildtype PXO99~A were revealed by DNA microarray analysis. Discovery of GacAxoo and FleQxoo regulons will provide important informations for interpretation of regulatory network of gene expression in Xoo.
560 genes of Xoo were selected for the microarray fabrication including regulator genes, pathogenicity-related genes, specific genes of Xoo, genes of flagella gene cluster and conserved genes of bacteria according to the genome sequence of KACC10331. With the labeling of cDNA probes with Cy3 and/or Cy5, the transcriptional profiles of PXO99~A,△gaeAxoo and△fleQxoo grown in nutrition-rich medium NBY and hrp-inducing medium XOM2 were analysed and compared.
17 differentially-expressed genes of PXO99~A were observed in XOM2 compared with NBY. 10 of them are up-regulated while 7 down-regulated. Among the 10 up-regulated genes, 7 of them are hrp genes (hrpB, hrpB1, hrpB3, hrpD6, hrpF) and effector genes (hpal, hpaB), hpal gene is the most obviously up-regulated with an over expression of 13 folds. Thus, the results show that hrp genes of Xoo are significantly induced in XOM2.
28 genes of AgacAxoo were found to be differentially expressed when grown in XOM2 compared with PXO99~A. 17 of them are up-regulated, while 12 down-regulated. Among 17 up-regulated genes, 7 of them encode hypothetical proteins and one is vieA gene. These genes may be suppressed by GacAxoo. Among 12 down-regulated genes, there are one gene for GGDEF family protein, one T3SS effector gene hpal, 4 genes of flagella gene cluster (flgC、fliC、fliO、cheA). GacAxoo regulate the expression of hpal and influence the motility through induction of some flagella genes. Furthermore, GacAxoo may influence the biosynthesis and degradation of c-di-GMP through negative or positive regulation of vieA and GGDEF family gene to modify the phenotypes of Xoo.
16 differentially-expressed genes of△fleQxoo cultured in NBY were found in comparison to PXO99~A. 12 of them are up-regulated, while 4 down-regulated. Among 12 up-regulated genes, there are 4 genes encoding components of T2SS, one T2SS effector gene egl, 3 genes encoding extracellular enzyme (polygalacturonase, protease, cellulase S), 3 genes of flagella gene cluster, one GGDEF family gene and one O-antigen biosynthesis gene rbfC. These genes may be negatively regulated and suppressed by FleQXoo. Four down-regulated genes arefliE, hrpB4, one pectinesterase gene and one protease gene. RT-PCR analysis confirmed that fliE is obviously a gene positively-regulated by FleQxoo. Mostly importantly, RT-PCR assay shows that fleQxoo is highly expressed in△fleQxoo, while expression offleQxoo is relatively low in PXO99~A. Therefore, results suggest that expression of fleQxoo may be self-suppressed.
In summary, DNA microarray analysis was used to reveal the transcriptional profiles of△gacAxoo,△fleQxoo and PXO99~A, and GacAxoo and FleQxoo regulons and parts of differentially-expressed genes were identified from the pathogen. Further analysis of these informations will help us to interprete the molecular mechanisms of pathogenicity in Xoo.
利用Xoo菌株KACC10331全基因组序列信息，选择出560个致病相关基因、调控因子基因、特有基因和保守基因、以及鞭毛基因簇基因，点制了一批Xoo基因芯片。对在丰富培养基(NBY)和hrp诱导培养基(XOM2)中生长到对数生长期(OD=1.2)的PXO99~A及其突变体ΔgacAxoo和ΔfleQxoo转录谱进行了比较测定。
与NBY培养条件相比，PXO99~A在XOM2中培养时有17个基因发生了差异性表达，其中10个基因上调表达，7个下调表达。在10个表达上调的基因中，7个为T3SS(hrpB、hrpB1、hrpB3、hrpD6、hrpF)及其效应子(hpa1、hpaB)基因，其中hpa1上调表达最为显著，可达到13倍。Xoo hrp基因的表达显著地受到诱导型培养基XOM2培养条件的诱导。
与PXO99~A相比，ΔgacAxoo在XOM2中培养时有28个基因发生了差异性表达，其中17个基因上调表达，11下调表达。在17个表达上调的基因中，1个为vieA基因，7个为假定蛋白的基因。这些基因受到GacAxoo负调控而抑制表达。在11个表达下调的基因中，1个为GGDEF家族成员基因，1个T3SS效应子基因hpa1，4个为鞭毛基因(flgC、fliC、fliO、cheA)。GacAxoo不仅调控了T3SS效应子基因hpa1的表达，而且也通过正向调控了部分鞭毛基因的表达，影响Xoo鞭毛运动性。此外，GacAxoo还可能通过正、负向调控vieA和GGDEF家族成员基因，影响第二信使c-di-GMP的代谢，从而调控了Xoo的诸多生物学性状。
与PXO99~A相比，ΔfleOxoo在NBY中培养时有16个基因发生了差异性表达，其中12个基因上调表达，4个下调表达。在12个表达上调的基因中，4个为T2SS(xpsJ、xpsL、xpsN)及其效应子(egl)基因，3个为胞外降解酶(polygalacturonase，protease，cellulase S)基因，3个为鞭毛基因簇(flhA、fliK、fliO)基因，1个为GGDEF家族成员基因，1个为O抗原生物合成基因(rbfC)。这些基因的表达受到FleQxoo负调控而被抑制。4个下调表达的基因包括鞭毛蛋白基因fliE、hrpB4、果胶酯酶基因和蛋白酶基因。RT-PCR分析验证了fliE基因的表达显著地受到FleQxoo正调控。值得注意的是，fleQxoo基因自身的表达在ΔfleQxoo中非常显著，而在PXO99~A中基本不表达或表达量极低。结果表明，fleQxoo基因表达可能受到自身的抑制。
总之，本研究利用基因芯片技术，通过构建Xoo及其ΔgacAxoo和ΔfleQxoo的基因转录谱，鉴别了GacAxoo和FleQxoo的部分调控元和差异性表达的基因，深入分析这些基因表达和调控的生物学信息，有助于阐明Xoo致病的分子机制。
Bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) is one of most important bacterial diseases of rice worldwide. Understanding of molecular basis of interactions between rice and Xoo has been promoted by elucidating the roles of genes associated with pathogenesis. Nevertheless, the pathogenicity mechanisms of Xoo are complex, many aspects of virulence and avirulence mechanisms are still not understood. The whole genome sequence of Xoo has provided a very useful tool to study the pathogenicity/virulence mechanisms on genome-wide scale.
GacAxoo, a response regulator of TCS and FleQxoo, a transcriptional regulator of flagellar gene cluster have been indentified in our previous study, which function as the regulators during the expression of virulence and motility of Xoo. To understand the regulatory roles and mechanisms of GacAxoo and FleQxoo on the genome scale, the transcriptional profiles of△gacAxoo,△fleQxoo and wildtype PXO99~A were revealed by DNA microarray analysis. Discovery of GacAxoo and FleQxoo regulons will provide important informations for interpretation of regulatory network of gene expression in Xoo.
560 genes of Xoo were selected for the microarray fabrication including regulator genes, pathogenicity-related genes, specific genes of Xoo, genes of flagella gene cluster and conserved genes of bacteria according to the genome sequence of KACC10331. With the labeling of cDNA probes with Cy3 and/or Cy5, the transcriptional profiles of PXO99~A,△gaeAxoo and△fleQxoo grown in nutrition-rich medium NBY and hrp-inducing medium XOM2 were analysed and compared.
17 differentially-expressed genes of PXO99~A were observed in XOM2 compared with NBY. 10 of them are up-regulated while 7 down-regulated. Among the 10 up-regulated genes, 7 of them are hrp genes (hrpB, hrpB1, hrpB3, hrpD6, hrpF) and effector genes (hpal, hpaB), hpal gene is the most obviously up-regulated with an over expression of 13 folds. Thus, the results show that hrp genes of Xoo are significantly induced in XOM2.
28 genes of AgacAxoo were found to be differentially expressed when grown in XOM2 compared with PXO99~A. 17 of them are up-regulated, while 12 down-regulated. Among 17 up-regulated genes, 7 of them encode hypothetical proteins and one is vieA gene. These genes may be suppressed by GacAxoo. Among 12 down-regulated genes, there are one gene for GGDEF family protein, one T3SS effector gene hpal, 4 genes of flagella gene cluster (flgC、fliC、fliO、cheA). GacAxoo regulate the expression of hpal and influence the motility through induction of some flagella genes. Furthermore, GacAxoo may influence the biosynthesis and degradation of c-di-GMP through negative or positive regulation of vieA and GGDEF family gene to modify the phenotypes of Xoo.
16 differentially-expressed genes of△fleQxoo cultured in NBY were found in comparison to PXO99~A. 12 of them are up-regulated, while 4 down-regulated. Among 12 up-regulated genes, there are 4 genes encoding components of T2SS, one T2SS effector gene egl, 3 genes encoding extracellular enzyme (polygalacturonase, protease, cellulase S), 3 genes of flagella gene cluster, one GGDEF family gene and one O-antigen biosynthesis gene rbfC. These genes may be negatively regulated and suppressed by FleQXoo. Four down-regulated genes arefliE, hrpB4, one pectinesterase gene and one protease gene. RT-PCR analysis confirmed that fliE is obviously a gene positively-regulated by FleQxoo. Mostly importantly, RT-PCR assay shows that fleQxoo is highly expressed in△fleQxoo, while expression offleQxoo is relatively low in PXO99~A. Therefore, results suggest that expression of fleQxoo may be self-suppressed.
In summary, DNA microarray analysis was used to reveal the transcriptional profiles of△gacAxoo,△fleQxoo and PXO99~A, and GacAxoo and FleQxoo regulons and parts of differentially-expressed genes were identified from the pathogen. Further analysis of these informations will help us to interprete the molecular mechanisms of pathogenicity in Xoo.
引文
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55. Rhodius V, Van Dyk T K, Gross C et al. Impact of genomic technologies on studies of bacterial gene expression. Annual Review of Microbiology. 2002, 56: 599-624.
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58. Rohlin L, Oh M K, Liao J C. DNA microarray for microbial biotechnology: gene expression profiles in Escherichia coli during protein overexpression. Journal of the Chinese Institute of Chemical Engineers. 2002, 33: 103-112
59. Ronald P, Leung H. The Rice Genome: The most precious things are not jade and pearls. Science. 2002, 296: 58-59.
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61. Rossier O, Wengelnik K, Hahn K. The Xanthomonas hrp type Ⅲ system secretes proteins from plant and mammalian bacterial pathogens. Proceedings of the National Academy of Sciences. 1999, 96: 9368-9373.
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78． Tischler A D,Camilli A.Cyclic Diguanylate Regulates Vibrio cholerae Virulence Gene Expression.Infection and Immunity.2005,73(9) :5873-5882．
79． Tsai R T,Leu W M,Chen L Y,Hu N T.A reversibly dissociable ternary complex formed by XpsL,XpsM and XpsN of the Xanthomonas campestris pv.campestris type Ⅱ secretion apparatus.Biochemistry.2002,367:865-871．
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51. Nino-Liu D, Ronald P, Bogdanove A J. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology. 2006, 7: 303-324.
52. Noel L, Thieme F, Nennstiel D. Two novel type Ⅲ secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. Journal of Bacteriology. 2002, 184: 1340-1348.
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55. Rhodius V, Van Dyk T K, Gross C et al. Impact of genomic technologies on studies of bacterial gene expression. Annual Review of Microbiology. 2002, 56: 599-624.
56. Richard C W, Paul W O, Kieran A R. The FliK protein and flagellar hook-length control. Protein Science. 2007, 16: 769-780.
57. Rogers T J, Paton J C, Wang H, Talbot U M, Paton A W. Reduced Virulence of an fliC Mutant of Shiga-Toxigenic Escherichia coli O 113:H21. Infection and Immunity. 2006, 74(3): 1962-1966.
58. Rohlin L, Oh M K, Liao J C. DNA microarray for microbial biotechnology: gene expression profiles in Escherichia coli during protein overexpression. Journal of the Chinese Institute of Chemical Engineers. 2002, 33: 103-112
59. Ronald P, Leung H. The Rice Genome: The most precious things are not jade and pearls. Science. 2002, 296: 58-59.
60. Rosa G J, de Leon N, Rosa A J. Review of microarray experimental design strategies for genetical genomics studies. Physiological Genomics. 2006, 13, 28(1): 15-23.
61. Rossier O, Wengelnik K, Hahn K. The Xanthomonas hrp type Ⅲ system secretes proteins from plant and mammalian bacterial pathogens. Proceedings of the National Academy of Sciences. 1999, 96: 9368-9373.
62. Sabatti C, Rohlin L, Oh M-K, Liao J C. Co-expression pattern from DNA microarray experiments as a tool for operon prediction. Nucleic Acids Research. 2002, 30: 2886-2893.
63. Saijo-Hamano Y, Imada K, Minamino T, Kihara M, Macnab R M, Namba K. Crystallization and preliminary X-ray analysis of the C-terminal cytoplasmic domain of FlhA, a membrane-protein subunit of the bacterial flagellar type Ⅲ protein-export apparatus. Acta Crystallographica Section F Structural Biology and Crystallization Communications.2005,61(Pt 6) :599-602．
64． Saijo-Hamano Y,Uchida N,Namba K,Oosawa K.In vitro characterization of FlgB,FlgC,FlgF,FlgG,and FliE,flagellar basal body proteins of Salmonella.Journal of Molecular Biology.2004,339(2) :423-435．
65． Sarah B N,Noonberg S H,Scott G K et al.Highly sensitive Northern hybridization of rare mRNA using a positively charged nylon membrane.Biotechniques.1994,16(6) :1074-1077．
66． Sarkar S F,Gordon J S,Martin G B,Guttman D S.Comparative genomics of host-specific virulence in Pseudomonas syringae.Genetics,2006,174(2) :1041-1056．
67． Sasaki T,Burr B.International rice genome sequencing project the effort to completely sequence the rice genome.Current Opinions in Plant Biology.2000,3:138-141．
68． Shen Y W,Ronald P.Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv.oryzae and rice.Microbes and Infection.2002,4:1361-1367
69． Shen Y,Chern M,Silva F.Isolation of a Xanthamonas oryzae pv.oryzae flagellar operon region and molecular characterization of flhF.Molecular Plant-Microbe Interactions,2001,14:204-213．
70． Simm R,Jacqueline D F,Kader A,Ro mling U,Robert D P.Phenotypic convergence mediated by GGDEF-domain-containing proteins.Journal of Bacteriology.2005,187(19) :6816-6823
71． Simm R,Morr M,Kader A,Nimtz M,Ro mling U.GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility.Molecular Microbiology.2004,53:1123-1134．
72． Song W Y,Wang G L,Chen L.The rice disease resistance gene,Xa21,encodes a receptor-like protein kinase.Science.1995,270:1804-1806．
73． Talaat A M,Hunter P,Johnston S A.Genome-directed primers for selective labeling of bacterial transcripts for DNA microarray analysis.Nature Biotechnology.2000,18:679-682．
74． Talaat A M,Lyons R,Howard S T,Johnston S A.The temporal expression profile of Mycobacterium tuberculosis infection in mice.Proceedings of the National Academy of Sciences.2004,101(13) :4602-4607．
75． Tamayo R,Tischler A D,Camilli A.The EAL Domain Protein VieA Is a Cyclic Diguanylate Phosphodiesterase.The Journal of Biological Chemistry.2005,280(39) :33324-33330．
76． Tang J L,Feng J X,Li Q Q.Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv.oryzae involvement in exopolysaccharide production and virulence to rice.Molecular Plant-Microbe Interactions.1996,9:664-666．
77． Tischler A D,Camilli A.Cyclic diguanylate(c-di-GMP)regulates Vibrio cholerae biofílm formation.Molecular Microbiology.2004 53:857-869．
78． Tischler A D,Camilli A.Cyclic Diguanylate Regulates Vibrio cholerae Virulence Gene Expression.Infection and Immunity.2005,73(9) :5873-5882．
79． Tsai R T,Leu W M,Chen L Y,Hu N T.A reversibly dissociable ternary complex formed by XpsL,XpsM and XpsN of the Xanthomonas campestris pv.campestris type Ⅱ secretion apparatus.Biochemistry.2002,367:865-871．
80. Tsuge S, Furutani A, Fukunaka R et al. Expression of Xanthomonas oryzae pv. Oryzae hrp Genes in XOM2, a Novel Synthetic Medium. Journal of General Plant Pathology. 2002, 68: 363-371.
81. Tsuge S, Nakayama T, Terashima Set al. Gene involved in Transcriptional Activation of the hrp Regulatory Gene hrpG in Xanthomonas oryzae pv. Oryzae. Journal of bacteriology. 2006, 188(11): 4158-4162.
82. Tunlid A. Exploring plant-microbe interactions using DNA microarrays. New Phytologist. 2003, 158: 227-238.
83. Vidaver A K. Synthetic and Complex Media for the Rapid Detection of Fluorescence of Phytopathogenic Pseudomonads: Effect of the Carbon Source. Applied Microbiology. 1967, 15(6): 1523-1524.
84. Yang B, Zhu W G, Johnson L B. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type Ⅲ secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proceedings of the National Academy of Sciences. 2000, 97: 9807-9812.
85. Yang G P, Ross D T, Kuang W Wet al. Combining SSH and cDNA microarrays for rapid identification of differentially expressed genes. Nucleic Acids Research. 1999, 27(6): 1517-1521.
86. Yang Y H, Speed T. Design issues for cDNA microarray experiments. Nature Reviews Genetics. 2002, 3: 579-588.
87. Yuan L, Hillman J D, Progulske-Fox A. Microarray analysis of quorum-sensing-regulated genes in Porphyromonas gingivalis. Infection and Immunity. 2005, 73(7): 4146-4154.
88. Zhu W, Magbanua M M, White F F, Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthornonas oryzae pv. oryzae. Journal of Bacteriology. 2000, 182: 1844-1853.
89. Zhu W, Yang B, Wills N, Johnson L B, White F F. The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP 16 from the herpes simplex virus. Plant Cell. 1999, 11: 1665-1674.
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