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Comparison of the genomes of two Xanthomonas pathogens with differing host specificities

Abstract

The genus Xanthomonas is a diverse and economically important group of bacterial phytopathogens, belonging to the γ-subdivision of the Proteobacteria. Xanthomonas axonopodis pv. citri (Xac) causes citrus canker, which affects most commercial citrus cultivars, resulting in significant losses worldwide. Symptoms include canker lesions, leading to abscission of fruit and leaves and general tree decline1. Xanthomonas campestris pv. campestris (Xcc) causes black rot, which affects crucifers such as Brassica and Arabidopsis. Symptoms include marginal leaf chlorosis and darkening of vascular tissue, accompanied by extensive wilting and necrosis2. Xanthomonas campestris pv. campestris is grown commercially to produce the exopolysaccharide xanthan gum, which is used as a viscosifying and stabilizing agent in many industries3. Here we report and compare the complete genome sequences of Xac and Xcc. Their distinct disease phenotypes and host ranges belie a high degree of similarity at the genomic level. More than 80% of genes are shared, and gene order is conserved along most of their respective chromosomes. We identified several groups of strain-specific genes, and on the basis of these groups we propose mechanisms that may explain the differing host specificities and pathogenic processes.

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Figure 1: Nucleotide alignment between Xac and Xcc.
Figure 2: Comparative genome map.

References

  1. Gottwald, T. R. & Graham, J. H. in Compendium of Citrus Diseases (eds Timmer, L. W., Garnsey, S. M. & Graham, J. H.) 5–7 (Am. Phytopathol. Soc., St. Paul, 2000)

    Google Scholar 

  2. Hayward, A. C. in Xanthomonas (eds Swings, J. G. & Civerolo, E. L.) 51–54 (Chapman & Hall, London, 1993)

    Google Scholar 

  3. Becker, A., Katzen, F., Puhler, A. & Ielpi, L. Xanthan gum biosynthesis and application: a biochemical/genetic perspective. Appl. Microbiol. Biotechnol. 50, 145–152 (1998)

    CAS  Article  Google Scholar 

  4. Menestrina, G. & Semjen, B. V. in The Comprehensive Sourcebook of Bacterial Proteins Toxins (ed. Alouf, J. E.) 287–309 (Academic, London, 1999)

    Google Scholar 

  5. Simpson, A. J. et al. The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406, 151–157 (2000)

    ADS  CAS  Article  Google Scholar 

  6. Göttfert, M., Grob, P. & Hennecke, H. Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc. Natl Acad. Sci. USA 87, 2680–2684 (1990)

    ADS  Article  Google Scholar 

  7. Chang, K. H. et al. Sequence analysis and expression of the filamentous phage phi Lf gene I encoding a 48-kDa protein associated with host cell membrane. Biochem. Biophys. Res. Commun. 245, 313–318 (1998)

    CAS  Article  Google Scholar 

  8. Breedveld, M. W., Hadley, J. A. & Miller, K. J. A novel cyclic β-1,2-glucan mutant of Rhizobium meliloti. J. Bacteriol. 177, 6346–6351 (1995)

    CAS  Article  Google Scholar 

  9. Ronald, P. C. & Staskawicz, B. J. The avirulence gene avrBs1 from Xanthomonas campestris pv. vesicatoria encodes a 50-kD protein. Mol. Plant-Microbe Interact. 1, 191–198 (1988)

    CAS  Article  Google Scholar 

  10. Bhat, T. K., Singh, B. & Sharma, O. P. Microbial degradation of tannins—a current perspective. Biodegradation 9, 343–357 (1998)

    CAS  Article  Google Scholar 

  11. Beyer, S., Distler, J. & Piepersberg, W. The str gene cluster for the biosynthesis of 5′-hydroxy-streptomycin in Streptomyces glaucescens GLA.0 (ETH 22794): new operons and evidence for pathway-specific regulation by StrR. Mol. Gen. Genet. 250, 775–784 (1996)

    CAS  PubMed  Google Scholar 

  12. Lin, J. T., Goldman, B. S. & Stewart, V. The nasFEDCBA operon for nitrate and nitrite assimilation in Klebsiella pneumoniae M5al. J. Bacteriol. 176, 2551–2559 (1994)

    CAS  Article  Google Scholar 

  13. Chen, J. H., Hsieh, Y. Y., Hsiau, S. L., Lo, T. C. & Shau, C. C. Characterization of insertions of IS476 and two newly identified insertion sequences, IS1478 and IS1479, in Xanthomonas campestris pv. campestris. J. Bacteriol. 181, 1220–1228 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Tang, J. L. et al. 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 (1991)

    CAS  Article  Google Scholar 

  15. Dow, J. M., Feng, J. X., Barber, C. E., Tang, J. L. & Daniels, M. J. Novel genes involved in the regulation of pathogenicity factor production within the rpf gene cluster of Xanthomonas campestris. Microbiology 146, 885–891 (2000)

    CAS  Article  Google Scholar 

  16. Dow, J. M. & Daniels, M. J. Xylella genomics and bacterial pathogenicity to plants. Yeast 17, 263–271 (2000)

    CAS  Article  Google Scholar 

  17. Rudolf, K. in Xanthomonas (eds Swings, J. G. & Civerolo, E. L.) 193–264 (Chapman & Hall, London, 1993)

    Book  Google Scholar 

  18. Cao, H., Baldini, R. L. & Rahme, L. G. Common mechanisms for pathogens of plants and animals. Annu. Rev. Phytopathol. 39, 259–284 (2001)

    CAS  Article  Google Scholar 

  19. Noël, L., Thieme, F., Nennstiel, D. & Bonas, U. cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol. Microbiol. 41, 1271–1281 (2001)

    Article  Google Scholar 

  20. Dow, J. M., Osbourn, A. E., Wilson, T. J. & Daniels, M. J. A locus determining pathogenicity of Xanthomonas campestris is involved in lipopolysaccharide biosynthesis. Mol. Plant-Microbe Interact. 8, 768–777 (1995)

    CAS  Article  Google Scholar 

  21. Vorhölter, F. J., Niehaus, K. & Puhler, A. Lipopolysaccharide biosynthesis in Xanthomonas campestris pv. campestris: a cluster of 15 genes is involved in the biosynthesis of the LPS O-antigen and the LPS core. Mol. Genet. Genomics. 266, 79–95 (2001)

    Article  Google Scholar 

  22. Dums, F., Dow, J. M. & Daniels, M. J. Structural characterization of protein secretion genes of the bacterial phytopathogen Xanthomonas campestris pathovar campestris: relatedness to secretion systems of other gram-negative bacteria. Mol. Gen. Genet. 229, 357–364 (1991)

    CAS  Article  Google Scholar 

  23. Bonas, U. et al. 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 (1991)

    ADS  CAS  Article  Google Scholar 

  24. Burns, D. L. Biochemistry of type IV secretion. Curr. Opin. Microbiol. 2, 25–29 (1999)

    CAS  Article  Google Scholar 

  25. Wengelnik, K. & Bonas, U. 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 (1996)

    CAS  Article  Google Scholar 

  26. Fenselau, S. & Bonas, U. Sequence and expression analysis of the hrpB pathogenicity operon of Xanthomonas campestris pv. vesicatoria which encodes eight proteins with similarity to components of the Hrp, Ysc, Spa, and Fli secretion systems. Mol. Plant-Microbe Interact. 8, 845–854 (1995)

    CAS  Article  Google Scholar 

  27. Lahaye, T. & Bonas, U. Molecular secrets of bacterial type III effector proteins. Trends Plant Sci. 6, 479–485 (2001)

    CAS  Article  Google Scholar 

  28. Yang, Y. & Gabriel, D. W. Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities. J. Bacteriol. 177, 4963–4968 (1995)

    CAS  Article  Google Scholar 

  29. Young, N. D. The genetic architecture of resistance. Curr. Opin. Plant Biol. 3, 285–290 (2000)

    CAS  Article  Google Scholar 

  30. Gueneron, M., Timmers, A. C., Boucher, C. & Arlat, M. Two novel proteins, PopB, which has functional nuclear localization signals, and PopC, which has a large leucine-rich repeat domain, are secreted through the hrp-secretion apparatus of Ralstonia solanacearum. Mol. Microbiol. 36, 261–277 (2000)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank A. M. da Silva, S. Verjovski-Almeida and D. W. Wood for reading of the manuscript; our steering committee (S. Oliver, A. Goffeau, J. Sgouros, A. C. M. Paiva and J. L. Azevedo) for their critical accompaniment; and all the technicians in the sequencing laboratories of ONSA involved in this project. Project funding was from FAPESP, Fundecitrus, Fundect-MS and CNPq.

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Correspondence to A. C. R. da Silva.

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da Silva, A., Ferro, J., Reinach, F. et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417, 459–463 (2002). https://doi.org/10.1038/417459a

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