DNA microarray-based genome comparison of a pathogenic and a nonpathogenic strain of Xylella fastidiosa delineates genes important for bacterial virulence

Journal of Bacteriology

Volumn 186, Issue 16, 2004, Pages 5442-5449

  Koide, Tie ^a   Zaini, Paulo A ^a   Moreira, Leandro M ^a   Vêncio, Ricardo Z N ^a   Matsukuma, Adriana Y ^a   Durham, Alan M ^a   Teixeira, Diva C ^b   El Dorry, Hamza ^a   Monteiro, Patrícia B ^b,c   Da Silva, Ana Claudia R ^a   Verjovski Almeida, Sergio ^a   Da Silva, Aline M ^a   Gomes, Suely L ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Fundo de Defesa da Citricultura   (Brazil)

^c Alellyx Applied Genomics   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ARGINASE; FIMBRIA ADHESIN; NITRIC OXIDE; PROTEIN PRECURSOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM PILUS; BACTERIUM PILUS TYPE III; CELL AGGREGATION; CHLOROSIS; CITRUS FRUIT; CITRUS VARIEGATED CHLOROSIS; CROP PRODUCTION; DNA MICROARRAY; DNA SEQUENCE; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; NONHUMAN; NONPATHOGENIC BACTERIUM; PATHOGENIC BACTERIUM; PHENOTYPE; PHYTOPATHOGENIC BACTERIUM; PLANT DISEASE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TOBACCO; XYLELLA FASTIDIOSA; XYLELLA FASTIDIOSA STRAIN 9A5C; XYLELLA FASTIDIOSA STRAIN J1A12;

ADHESINS, BACTERIAL; ARGINASE; BACTERIAL ADHESION; BACTERIAL PROTEINS; CITRUS; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENES, BACTERIAL; GENOME, BACTERIAL; GENOMICS; NITRIC OXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT DISEASES; TOBACCO; VIRULENCE; VIRULENCE FACTORS; XYLELLA;

BACTERIA (MICROORGANISMS); CITRUS; NEGIBACTERIA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; XYLELLA FASTIDIOSA;

EID: 3843141577     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.16.5442-5449.2004     Document Type: Article

References (39)

1. Almeida, R. P. P., and A. H. Purcell. 2003. Transmission of Xylella fastidiosa to grapevines by Homalodisca coagulata (Hemiptera: Cicadellidae). J. Econ. Entomol. 96:264-271.
2. Araujo, W. L., J. Marcon, W. Maccheroni, Jr., J. D. Van Elsas, J. W. Van Vuurde, and J. L. Azevedo. 2002. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl. Environ. Microbiol. 68:4906-4914.
3. Behr, M. A., M. A. Wilson, W. P. Gill, H. Salamon, G. K. Schoolnik, S. Rane, and P. M. Small. 1999. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284:1520-1523.
4. Bhattacharyya, A., S. Stilwagen, G. Reznik, H. Feil, W. S. Feil, I. Anderson, A. Bernal, M. D'Souza, N. Ivanova, V. Kapatral, N. Larsen, T. Los, A. Lykidis, E. Selkov, Jr., T. L. Walunas, A. Purcell, R. A. Edwards, T. Hawkins, R. Haselkorn, R. Overbeek, N. C. Kyrpides, and P. F. Predki. 2002. Draft sequencing and comparative genomics of Xylella fastidiosa strains reveal novel biological insights. Genome Res. 12:1556-1563.
5. Chandok, M. R., A. J. Ytterberg, K. J. van Wijk, and D. F. Klessig. 2003. The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell 113:469-482.
6. da Silva Neto, J. F., T. Koide, S. L. Gomes, and M. V. Marques. 2002. Site-directed gene disruption in Xylella fastidiosa. FEMS Microbiol. Lett. 210:105-110.
7. Davis, M. J., W. J. French, and N. W. Schaad. 1981. Axenic culture of the bacteria associated with phony disease of peach and plum leaf scald. Curr. Microbiol. 6:309-314.
8. de Souza, A. A., M. A. Takita, H. D. Coletta, C. Caldana, G. H. Goldman, G. M. Yanai, N. H. Muto, R. C. de Oliveira, L. R. Nunes, and M. A. Machado. 2003. Analysis of gene expression in two growth states of Xylella fastidiosa and its relationship with pathogenicity. Mol. Plant-Microbe Interact. 16:867-875.
9. Feil, H., W. S. Feil, J. C. Detter, A. H. Purcell, and S. E. Lindow. 2003. Site-directed disruption of the fimA and fimF fimbrial genes of Xylella fastidiosa. Phytopathology 93:675-682.
10. Gobert, A. P., D. J. McGee, M. Akhtar, G. L. Mendz, J. C. Newton, Y. Cheng, H. L. Mobley, and K. T. Wilson. 2001. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc. Natl. Acad. Sci. USA 98:13844-13849.
11. Guo, F. Q., M. Okamoto, and N. M. Crawford. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100-103.
12. Hinchliffe, S. J., K. E. Isherwood, R. A. Stabler, M. B. Prentice, A. Rakin, R. A. Nichols, P. C. F. Oyston, J. Hinds, R. W. Titbal, and B. W. Wren. 2003. Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. Genome Res. 13:2018-2029.
13. Hopkins, D. L. 1989. Xylella fastidiosa-xylem-limited bacterial pathogen of plants. Annu. Rev. Phytopathol. 27:271-290.
14. Hopkins, D. L., and A. H. Purcell. 2002. Xylella fastidiosa: cause of Pierce's disease of grapevine and other emergent diseases. Plant Dis. 86:1056-1066.
15. Karlin, S. 2001. Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol. 9:335-343.
16. Kim, C. C., E. A. Joyce, K. Chan, and S. Falkow. 2002. Improved analytical methods for microarray-based genome-composition analysis. Genome Biol. 3:RESEARCH0065.
17. Koide, T., J. F. da Silva Neto, S. L. Gomes, and M. V. Marques. 2004. Insertional transposon mutagenesis in the Xylella fastidiosa citrus variegated chlorosis strain with transposome. Curr. Microbiol. 48:247-250.
18. Langstraat, J., M. Bohse, and S. Clegg. 2001. Type 3 fimbrial shaft (MrkA) of Klebsiella pneumoniae, but not the fimbrial adhesin (MrkD), facilitates biofilm formation. Infect. Immun. 69:5805-5812.
19. Leite, B., M. L. Ishida, E. Alves, H. Carrer, S. F. Pascholati, and E. W. Kitajima. 2002. Genomics and X-ray microanalysis indicate that Ca2+ and thiols mediate the aggregation and adhesion of Xylella fastidiosa. Braz. J. Med. Biol. Res. 35:645-650.
20. Li, W. B., L. Zreik, N. G. Fernandes, V. S. Miranda, D. C. Teixeira, A. J. Ayres, M. Garnier, and J. M. Bove. 1999. A triply cloned strain of Xylella fastidiosa multiplies and induces symptoms of citrus variegated chlorosis in sweet orange. Curr. Microbiol. 39:106-108.
21. Lopes, S. A., D. M. Ribeiro, P. G. Roberto, S. C. Franca, and J. M. Santos. 2000. Nicotiana tabacum as an experimental host for the study of plant-Xylella fastidiosa interactions. Plant Dis. 84:827-830.
22. Machado, M. A., A. A. Souza, H. D. Coletta-Filho, E. E. Kuramae, and M. A. Takita. 2001. Genome and pathogenicity of Xylella fastidiosa. Mol. Biol. Today 2:33-43.
23. Monteiro, P. B., D. C. Teixeira, R. R. Palma, M. Garnier, J. M. Bove, and J. Renaudin. 2001. Stable transformation of the Xylella fastidiosa citrus variegated chlorosis strain with oriC plasmids. Appl. Environ. Microbiol. 67:2263-2269.
24. Nunes, L. R., Y. B. Rosato, N. H. Muto, G. M. Yanai, V. S. da Silva, D. B. Leite, E. R. Goncalves, A. A. de Souza, H. D. Coletta-Filho, M. A. Machado, S. A. Lopes, and R. C. de Oliveira. 2003. Microarray analyses of Xylella fastidiosa provide evidence of coordinated transcription control of laterally transferred elements. Genome Res. 13:570-578.
25. Pooler, M. R., and J. S. Hartung. 1995. Specific PCR detection and identification of Xylella fastidiosa strains causing citrus variegated chlorosis. Curr. Microbiol. 31:377-381.
26. Purcell, A. H., and D. L. Hopkins. 1996. Fastidious xylem-limited bacterial plant pathogens. Annu. Rev. Phytopathol. 34:131-151.
27. Purcell, A. H., and S. R. Saunders. 1999. Fate of Pierce's disease strains of Xylella fastidiosa in common riparian plants in California. Plant Dis. 83:825-830.
28. Read, T. D., S. N. Peterson, N. Tourasse, L. W. Baillie, I. T. Paulsen, K. E. Nelson, H. Tettelin, D. E. Fouts, J. A. Eisen, S. R. Gill, E. K. Holtzapple, O. A. Okstad, E. Helgason, J. Rilstone, M. Wu, J. F. Kolonay, M. J. Beanan, R. J. Dodson, L. M. Brinkac, M. Gwinn, R. T. DeBoy, R. Madpu, S. C. Daugherty, A. S. Durkin, D. H. Haft, W. C. Nelson, J. D. Peterson, M. Pop, H. M. Khouri, D. Radune, J. L. Benton, Y. Mahamoud, L. X. Jiang, I. R. Hance, J. F. Weidman, K. J. Berry, R. D. Plant, A. M. Wolf, K. L. Watkins, W. C. Nierman, A. Hazen, R. Cline, C. Redmond, J. E. Thwaite, O. White, S. L. Salzberg, B. Thomason, A. M. Friedlander, T. M. Koehler, P. C. Hanna, A. B. Kolsto, and C. M. Fraser. 2003. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81-86.
29. Salama, N., K. Guillemin, T. K. McDaniel, G. Sherlock, L. Tompkins, and S. Falkow. 2000. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. USA 97:14668-14673.
30. Sebghati, T. A. S., T. K. Korhonen, D. B. Hornick, and S. Clegg. 1998. Characterization of the type 3 fimbrial adhesins of Klebsiella strains. Infect. Immun. 66:2887-2894.
31. Silverman, B. W. 1986. Density estimation. Chapman and Hall, London, England.
32. Simpson, A. J., F. C. Reinach, P., Arruda, F. A. Abreu, M. Acencio, R. Alvarenga, L. M. Alves, J. E. Araya, G. S. Baia, C. S. Baptista, M. H. Barros, E. D. Bonaccorsi, S. Bordin, J. M. Bove, M. R. Briones, M. R. Bueno, A. A. Camargo, L. E. Camargo, D. M. Carraro, H. Carrer, N. B. Colauto, C. Colombo, F. F. Costa, M. C. Costa, C. M. Costa-Neto, L. L. Coutinho, M. Cristofani, E. Dias-Neto, C. Docena, H. El-Dorry, A. P. Facincani, A. J. Ferreira, V. C. Ferreira, J. A. Ferro, J. S. Fraga, S. C. Franca, M. C. Franco, M. Frohme, L. R. Furlan, M. Garnier, G. H. Goldman, M. H. Goldman, S. L. Gomes, A. Gruber, P. L. Ho, J. D. Hoheisel, M. L. Junqueira, E. L. Kemper, J. P. Kitajima, J. E. Krieger, E. E. Kuramae, F. Laigret, M. R. Lambais, L. C. Leite, E. G. Lemos, M. V. Lemos, S. A. Lopes, C. B. Lopes, J. A. Machado, M. A. Machado, A. M. Madeira, H. M. Madeira, C. L. Marino, M. V. Marques, E. A. Martins, E. M. Martins, A. Y. Matsukuma, C. F. Menck, E. C. Miracca, C. Y. Miyaki, C. B. Monteriro-Vitorello, D. H. Moon, M. A. Nagai, A. L. Nascimento, L. E. Netto, A. Nhani, Jr., F. G. Nobrega, L. R. Nunes, M. A. Oliveira, M. C. de Oliveira, R. C. de Oliveira, D. A. Palmieri, A. Paris, B. R. Peixoto, G. A. Pereira, H. A. Pereira, Jr., J. B. Pesquero, R. B. Quaggio, P. G. Roberto, V. Rodrigues, A. J. de M. Rosa, V. E. de Rosa, Jr., R. G. de Sa, R. V. Santelli, H. E. Sawasaki, A. C. da Silva, A. M. da Silva, F. R. da Silva, W. A. da Silva, Jr., J. F. da Silveira, M. L. Silvestri, W. J. Siqueira, A. A. de Souza, A. P. de Souza, M. F. Terenzi, D. Truffi, S. M. Tsai, M. H. Tsuhako, H. Vallada, M. A. Van Sluys, S. Verjovski-Almeida, A. L. Vettore, M. A. Zago, M. Zatz, J. Meidanis, and J. C. Setubal. 2000. The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406:151-157.
33. Smolka, M. B., D. Martins, F. V. Winck, C. E. Santoro, R. R. Castellari, F. Ferrari, I. J. Brum, E. Galembeck, H. Della Coletta Filho, M. A. Machado, S. Marangoni, and J. C. Novello. 2003. Proteome analysis of the plant pathogen Xylella fastidiosa reveals major cellular and extracellular proteins and a peculiar codon bias distribution. Proteomics 3:224-237.
34. Tarkkanen, A. M., R. Virkola, S. Clegg, and T. K. Korhonen. 1997. Binding of the type 3 fimbriae of Klebsiella pneumoniae to human endothelial and urinary bladder cells. Infect. Immun. 65:1546-1549.
35. Tyson, G. E., B. J. Stojanovic, R. F. Kuklinski, T. J. Divittorio, and M. L. Sullivan. 1985. Scanning electron-microscopy of Pierce's disease bacterium in petiolar xylem of grape leaves. Phytopathology 75:264-269.
36. Vaara, M., and M. Nurminen. 1999. Outer membrane permeability barrier in Escherichia coli mutants that are defective in the late acyltransferases of lipid A biosynthesis. Antimicrob. Agents Chemother. 43:1459-1462.
37. Van Sluys, M. A., M. C. de Oliveira, C. B. Monteiro-Vitorello, C. Y. Miyaki, L. R. Furlan, L. E. Camargo, A. C. da Silva, D. H. Moon, M. A. Takita, E. G. Lemos, M. A. Machado, M. I. Ferro, F. R. da Silva, M. H. Goldman, G. H. Goldman, M. V. Lemos, H. El-Dorry, S. M. Tsai, H. Carrer, D. M. Carraro, R. C. de Oliveira, L. R. Nunes, W. J. Siqueira, L. L. Coutinho, E. T. Kimura, E. S. Ferro, R. Harakava, E. E. Kuramae, C. L. Marino, E. Giglioti, I. L. Abreu, L. M. Alves, A. M. do Amaral, G. S. Baia, S. R. Blanco, M. S. Brito, F. S. Cannavan, A. V. Celestino, A. F. da Cunha, R. C. Fenille, J. A. Ferro, E. F. Formighieri, L. T. Kishi, S. G. Leoni, A. R. Oliveira, V. E. Rosa, Jr., F. T. Sassaki, J. A. Sena, A. A. de Souza, D. Truffi, F. Tsukumo, G. M. Yanai, L. G. Zaros, E. L. Civerolo, A. J. Simpson, N. F. Almeida, Jr., J. C. Setubal, and J. P. Kitajima. 2003. Comparative analyses of the complete genome sequences of Pierce's disease and citrus variegated chlorosis strains of Xylella fastidiosa. J. Bacteriol. 185:1018-1026.
38. Wolfgang, M. C., B. R. Kulasekara, X. Y. Liang, D. Boyd, K. Wu, Q. Yang, C. G. Miyada, and S. Lory. 2003. Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 100:8484-8489.
39. Yang, Y. H., S. Dudoit, P. Luu, D. M. Lin, V. Peng, J. Ngai, and T. P. Speed. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:e15.