The xrvA gene of Xanthomonas oryzae pv. oryzae, encoding an H-NS-like protein, regulates virulence in rice

Microbiology

Volumn 155, Issue 9, 2009, Pages 3033-3044

  Feng, Jia Xun ^a   Song, Zhi Zhong ^a   Duan, Cheng Jie ^a   Zhao, Shuai ^a   Wu, Ying Qiao ^a   Wang, Chao ^a   Dow, J Maxwell ^b   Tang, Ji Liang ^a  

^a GUANGXI UNIVERSITY   (China)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE LIKE NUCLEOID STRUCTURING PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; DNA HYBRIDIZATION; DOWN REGULATION; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENE NUMBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT MICROORGANISM INTERACTION; PRIORITY JOURNAL; REGULATORY MECHANISM; RICE; XANTHOMONAS; XANTHOMONAS ORYZAE;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLYCOGEN; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT DISEASES; POLYSACCHARIDES, BACTERIAL; RICINUS; TRANSCRIPTION, GENETIC; VIRULENCE; VIRULENCE FACTORS; XANTHOMONAS;

BACTERIA (MICROORGANISMS); XANTHOMONAS; XANTHOMONAS ORYZAE PV. ORYZAE;

EID: 69949120096     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.028910-0     Document Type: Article

References (64)

1. Alfano, J. R. & Collmer, A. (1997). The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179, 5655-5662.
2. Alwine, J. C., Kemp, D. J. & Stark, G. R. (1977). Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A 74, 5350-5354.
3. Arlat, M., Gough, C. L., Barber, C., Boucher, C. & Daniels, M. J. (1991). Xanthomonas campestris contains a cluster of hrp genes related to the larger hrp cluster of Pseudomonas solanacearum. Mol Plant Microbe Interact 4, 593-601.
4. Bai, J., Choi, S. H., Ponciano, G., Leung, H. & Leach, J. E. (2000). Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Mol Plant Microbe Interact 13, 1322-1329.
5. Barber, C. E., Tang, J. L., Feng, J. X., Pan, M. Q., Wilson, T. J., Slater, H., Dow, J. M., Williams, P. & Daniels, M. J. (1997). A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24, 555-566.
6. Bertin, P., Hommais, F., Krin, E., Soutourina, O., Tendeng, C., Derzelle, S. & Danchin, A. (2001). H-NS and H-NS-like proteins in Gram-negative bacteria and their multiple role in the regulation of bacterial metabolism. Biochimie 83, 235-241.
7. Bogdanove, A. J., Beer, S. V., Bonas, U., Boucher, C. A., Collmer, A., Coplin, D. L., Cornelis, G. R., Huang, H. C., Hutcheson, S. W. & other authors (1996). Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol Microbiol 20, 681-683.
8. Bonas, U., Schulete, R., Fenselau, S., Minsavage, G. V., Staskawicz, B. J. & Stall, R. E. (1991). Isolation of a gene cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol Plant Microbe Interact 4, 81-88.
9. Chao, N. X.,Wei, K., Chen, Q.,Meng, Q. L., Tang, D. J., He, Y. Q., Lu, G. T., Jiang, B. L., Liang, X. X. & other authors (2008). The rsmA-like gene rsmA (Xcc) of Xanthomonas campestris pv. campestris is involved in the control of various cellular processes, including pathogenesis. Mol Plant Microbe Interact 21, 411-423.
10. Chatterjee, S. & Sonti, R. V. (2002). rpfF mutants of Xanthomonas oryzae pv. oryzae are deficient for virulence and growth under low iron conditions. Mol Plant Microbe Interact 15, 463-471.
11. Dalai, B., Zhou, R., Wan, Y., Kang, M., Li, L., Li, T., Zhang, S. & Chen, H. (2009). Histone-like protein H-NS regulates biofilm formation and virulence of Actinobacillus pleuropneumoniae. Microb Pathog 46, 128-134.
12. Daniels, M. J., Barber, C. E., Turner, P. C., Sawczyc, M. K., Byrde, R. J. W. & Fielding, A. H. (1984). Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J 3, 3323-3328.
13. Dharmapuri, S. & Sonti, R. V. (1999). A transposon insertion in the gumG homologue of Xanthomonas oryzae pv. oryzae causes loss of extracellular polysaccharide production and virulence. FEMS Microbiol Lett 179, 53-59.
14. Dharmapuri, S., Yashitola, J., Vishnupriya, M. R. & Sonti, R. V. (2001). Novel genomic locus with atypical G+C content that is required for extracellular polysaccharide production and virulence in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 14, 1335-1339.
15. Dorman, C. J. (2004). H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2, 391-400.
16. Dorman, C. J. (2007). H-NS, the genome sentinel. Nat Rev Microbiol 5, 157-161.
17. Dow, M. (2008). Diversification of the function of cell-to-cell signaling in regulation of virulence within plant pathogenic Xanthomonas. Sci Signal 1, pe23.
18. Fang, F. C. & Rimsky, S. (2008). New insights into transcriptional regulation by H-NS. Curr Opin Microbiol 11, 113-120.
19. Feng, J. X., Li, Y. R., Duan, C. J. & Tang, J. L. (2001). Cloning and characterization of hrp gene from Xanthomonas oryzae pv. oryzae. In Plant Diseases and Their Control, pp. 26-27. Edited by S. M. Zeng, G. H. Zhou & H. F. Li. Beijing: China Agricultural Science and Technology Press.
20. Hanahan, D. (1983). Studies on transformation of E. coli with plasmids. J Mol Biol 166, 557-580.
21. Harrison, J. A., Pickard, D., Higgins, C. F., Khan, A., Chatfield, S. N., Ali, T., Dorman, C. J., Hormaeche, C. E. & Dougan, G. (1994). Role of hns in the virulence phenotype of pathogenic salmonellae. Mol Microbiol 13, 133-140.
22. He, Y.-W. & Zhang, L.-H. (2008). Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol Rev 32, 842-857.
23. He, Y. Q., Zhang, L., Jiang, B. L., Zhang, Z. C., Xu, R. Q., Tang, D. J., Qin, J., Jiang, W., Zhang, X. & other authors (2007). Comparative and functional genomics reveals genetic diversity and determinants of host specificity among reference strains and a large collection of Chinese isolates of the phytopathogen Xanthomonas campestris pv. campestris. Genome Biol 8, R218.
24. Hildebrand, M., Aldridge, P. & Geider, K. (2006). Characterization of hns genes from Erwinia amylovora. Mol Genet Genomics 275, 310-319.
25. Huynh, T. V., Dahlbeck, D. & Staskawicz, B. J. (1989). Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245, 1374-1377.
26. Jefferson, R. A., Burges, S. M. & Hirsh, D. (1986). β-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad Sci U S A 83, 8447-8451.
27. Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6, 3901-3907.
28. Jeong, K. S., Lee, S. E., Han, J. W., Yang, S. U., Lee, B. M., Noh, T. H. & Cha, J. S. (2008). Virulence reduction and differing regulation of virulence genes in rpf mutants of Xanthomonas oryzae pv. oryzae. Plant Pathol J 24, 143-151.
29. Katzen, F., Becker, A., Zorreguieta, A., Puhler, A. & Ielpi, L. (1996). Promoter analysis of the Xanthomonas campestris pv. campestris gum operon directing biosynthesis of the xanthan polysaccharide. J Bacteriol 178, 4313-4318.
30. Katzen, F., Becker, A., Ielmini, M. V., Oddo, C. G. & Ielpi, L. (1999). New mobilizable vectors suitable for gene replacement in Gram-negative bacteria and their use in mapping of the 3′ end of the Xanthomonas campestris pv. campestris gum operon. Appl Environ Microbiol 65, 278-282.
31. Kauffman, H. E., Reddy, A. P. K., Hsieh, S. P. Y. & Merca, S. D. (1973). An improved technique for evaluating resistence of rice varieties to Xanthomonas oryzae. Plant Dis Rep 57, 537-541.
32. Lahaye, T. & Bonas, U. (2001). Molecular secrets of bacterial type III effector proteins. Trends Plant Sci 6, 479-485.
33. Lee, B. M., Park, Y. J., Park, D. S., Kang, H. W., Kim, J. G., Song, E. S., Park, I. C., Yoon, U. H., Hahn, J. H. & other authors (2005). The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33, 577-586.
34. Lee, C. K., Lee, B. M. & Cho, J. Y. (2008a). Identification of new internal promoters of the Xanthomonas oryzae pathovar oryzae gum gene cluster. Biotechnol Lett 30, 521-527.
35. Lee, S. W., Jeong, K. S., Han, S. W., Lee, S. E., Phee, B. K., Hahn, T. R. & Ronald, P. (2008b). The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol 190, 2183-2197.
36. Leong, S. A., Ditta, G. S. & Helinski, D. R. (1982). Heme biosynthesis in Rhizobium. Identification of a cloned gene coding for delta-aminolevulinic acid synthetase from Rhizobium meliloti. J Biol Chem 257, 8724-8730.
37. Mew, T. W., Alvarez, A. M., Leach, J. E. & Swings, J. (1993). Focus on bacterial blight of rice. Plant Dis 77, 5-12.
38. Miller, G. L. (1959). Use of dinitrosalicyclic acid reagent for determination of reducing sugar. Anal Chem 31, 426-428.
39. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
40. Müller, C. M., Dobrindt, U., Nagy, G., Emödy, L., Uhlin, B. E. & Hacker, J. (2006). Role of histone-like proteins H-NS and StpA in expression of virulence determinants of uropathogenic Escherichia coli. J Bacteriol 188, 5428-5438.
41. Nasser, W., Faelen, M., Hugouvieux-Cotte-Pattat, N. & Reverchon, S. (2001). Role of the nucleoid-associated protein H-NS in the synthesis of virulence factors in the phytopathogenic bacterium Erwinia chrysanthemi. Mol Plant Microbe Interact 14, 10-20.
42. Nino-Liu, D. O., Ronald, P. C. & Bogdanove, A. J. (2006). Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7, 303-324.
43. Ochiai, H., Inoue, Y., Takeya, M., Sasaki, A. & Kaku, H. (2005). Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jpn Agric Res Q 39, 275-287.
44. Ou, S. H. (1985). Rice Diseases. Kew, UK: Commonwealth Agricultural Bureaux.
45. Ryan, R. P., Fouhy, Y., Lucey, J. F., Crossman, L. C., Spiro, S., He, Y. W., Zhang, L. H., Heeb, S., Camara, M. & other authors (2006). Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103, 6712-6717.
46. Salzberg, S. L., Sommer, D. D., Schatz, M. C., Phillippy, A. M., Rabinowicz, P. D., Tsuge, S., Furutani, A., Ochiai, H., Delcher, A. L. & other authors (2008). Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9, 204.
47. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
48. Schulte, R. & Bonas, U. (1992a). A Xanthomonas pathogenicity locu is induced by sucrose and sulfur-containing amino acids. Plant Cell 4, 79-86.
49. Schulte, R. & Bonas, U. (1992b). Expression of the Xanthomonas campestris pv. vesicatoria hrp gene cluster, which determines pathogenicity and hypersensitivity on pepper and tomato, is plant inducible. J Bacteriol 174, 815-823.
50. Slater, H., Alvarez-Morales, A., Barber, C. E., Daniels, M. J. & Dow, J.M. (2000). A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38, 986-1003.
51. Sledjeski, D. & Gottesman, S. A. (1995). A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci U S A 92, 2003-2007.
52. Swift, S., Lynch, M. J., Fish, L., Kirke, D. F., Tom-acas, J. M., Stewart, G. S. & Williams, P. (1999). Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect Immun 67, 5192-5199.
53. Tang, J. L., Liu, Y. N., Barber, C. E., Dow, J. M., Wootton, J. C. & Daniels, M. J. (1991). Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris. Mol Gen Genet 226, 409-417.
54. Tang, J. L., Feng, J. X., Li, Q. Q., Wen, H. X., Zhou, D. L., Wilson, T. J., Dow, J. M., Ma, Q. S. & Daniels, M. J. (1996). Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv. oryzae: involvement in exopolysaccharide production and virulence to rice. Mol Plant Microbe Interact 9, 664-666.
55. Tendeng, C. & Bertin, P. N. (2003). H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 11, 511-518.
56. Tsuge, S., Furutani, A., Fukunaka, R., Oku, T., Tsuno, K., Ochiai, H., Inoue, Y., Kaku, H. & Kubo, Y. (2002). Expression of Xanthomonas oryzae pv. oryzae hrp genes in XOM2, a novel synthetic medium. J Gen Plant Pathol 68, 363-371.
57. Tsuge, S., Nakayama, T., Terashima, S., Ochiai, H., Furutani, A., Oku, T., Tsuno, K., Kubo, Y. & Kaku, H. (2006). Gene involved in transcriptional activation of the hrp regulatory gene hrpG in Xanthomonas oryzae pv. oryzae. J Bacteriol 188, 4158-4162.
58. Turner, P., Barber, C. E. & Daniels, M. J. (1985). Evidence for clustered pathogenicity genes in Xanthomonas campestris pv. campestris. Mol Gen Genet 190, 338-343.
59. Wang, L. H., He, Y., Gao, Y., Wu, J. E., Dong, Y. H., He, C., Wang, S. X., Weng, L. X., Xu, J. L. & other authors (2004). A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51, 903-912.
60. Wang, J. C., So, B. H., Kim, J. H., Park, Y. J., Lee, B. M. & Kang, H. W. (2008). Genome-wide identification of pathogenicity genes in Xanthomonas oryzae pv. oryzae by transposon mutagenesis. Plant Pathol 57, 1136-1145.
61. Wengelnik, K. & Bonas, U. (1996). HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol 178, 3462-3469.
62. Wengelnik, K., Van den Ackerveken, G. & Bonas, U. (1996). HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol Plant Microbe Interact 9, 704-712.
63. Windgassen, M., Urban, A. & Jaeger, K. E. (2000). Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiol Lett 193, 201-205.
64. Yoon, K. H. & Cho, J. Y. (2007). Transcriptional analysis of the gum gene cluster from Xanthomonas oryzae pathovar oryzae. Biotechnol Lett 29, 95-103.