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6 - Genomic Islands in Plant-pathogenic Bacteria

from PART III - Paradigms of Bacterial Evolution

Published online by Cambridge University Press:  16 September 2009

By
Dawn L. Arnold  and
Robert W. Jackson
Edited by
Michael Hensel  and
Herbert Schmidt
Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
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Summary

INTRODUCTION

The evolution of bacterial pathogens from non-pathogens or from avirulent strains is a major cause for concern in agriculture. As exemplified by the explosion of antibiotic resistance in human pathogens, bacteria can rapidly overcome control strategies and host resistance. As we are now discovering, the intrinsic plasticity of the bacterial genome combined with horizontal gene transfer is the major determinant influencing the expression of pathogenicity. Many of the disease symptoms caused by pathogens on plants, including blights, galls, chlorosis, scabs, leaf spots, and wilting, are attributable to genes that are often clustered together and, in some cases, acquired from distantly related bacteria. One mechanism that affects the virulence of plant pathogens is the loss or gain of DNA regions called genomic islands (GEI).

GEI were first described as pathogenicity islands (PAI) in human pathogenic Escherichia coli by Hacker et al. (1990), who discovered that a region of chromosomally located, virulence-associated genes of uropathogenic E. coli was absent from some E. coli isolates (Blum et al., 1994). The term GEI is now more appropriate given that the features of PAI are displayed by a number of regions of DNA with functions other than pathogenicity, for example, symbiosis, metabolic, or resistance islands (Hacker and Kaper, 2000; Hentschel and Hacker, 2001).

Type
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Horizontal Gene Transfer in the Evolution of Pathogenesis , pp. 137 - 158
Publisher: Cambridge University Press
Print publication year: 2008

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References

Alarcón-Chaidez, F. J., Peñaloza-Vázquez, A., Ullrich, M., and Bender, C. L. (1999). Characterization of plasmids encoding the phytotoxin coronatine in Pseudomonas syringae. Plasmid, 42, 210–20.CrossRefGoogle ScholarPubMed
Alfano, J. R., and Collmer, A. (1997). The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol, 179, 5655–62.CrossRefGoogle ScholarPubMed
Alfano, J. R., Charkowski, A. O., Deng, W., et al. (2000). The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci USA, 97, 4856–61.CrossRefGoogle Scholar
Antonenka, U., Nolting, C., Heesemann, J., and Rakin, A. (2005). Horizontal transfer of Yersinia high-pathogenicity island by the conjugative RP4 attB target-presenting shuttle plasmid. Mol Microbiol 57, 727–34.CrossRefGoogle ScholarPubMed
Araki, H., Tian, D., Goss, E. M., et al. (2006). Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. Proc Natl Acad Sci USA, 103, 5887–92.CrossRefGoogle ScholarPubMed
Arnold, D. L., Jackson, R. W., and Vivian, A. (2000). Evidence for the mobility of an avirulence gene, avrPpiA1, between the chromosome and plasmids of races of Pseudomonas syringae pv. pisi. Mol Plant Pathol, 1, 195–9.CrossRefGoogle ScholarPubMed
Arnold, D. L., Jackson, R. W., Fillingham, A. J., et al. (2001). Highly conserved (DNA) sequences flank avirulence genes: isolation of novel avirulence genes from Pseudomonas syringae pv pisi. Microbiology, 147, 1171–82.CrossRefGoogle ScholarPubMed
Bell, K. S., Avrova, A. O., Holeva, M. C., et al. (2002). Sample sequencing of a selected region of the genome of Erwinia carotovora subsp. atroseptica reveals candidate phytopathogenicity genes and allows comparison with Escherichia coli. Microbiology, 148, 1367–78.CrossRefGoogle ScholarPubMed
Bell, K. S., Sebaihia, M., Pritchard, L., et al. (2004). Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA, 101, 11105–10.CrossRefGoogle ScholarPubMed
Bender, C. L., Alarcón-Chaidez, F., and Gross, D. C. (1999). Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63, 266–92.Google ScholarPubMed
Blum, G., Ott, M., Lischewski, A., et al. (1994). Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type. Infect Immun, 62, 606–14.Google ScholarPubMed
Bogdanove, A., Kim, J. F., Wei, Z., et al. (1998). Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE or Pseudomonas syringae pathovar tomato. Proc Natl Acad Sci USA, 95, 1325–30.CrossRefGoogle ScholarPubMed
Büttner, D., and Bonas, U. (2002). Getting across – bacterial type III effector proteins on their way to the plant cell. EMBO J, 21, 13–22.CrossRefGoogle ScholarPubMed
Casper-Lindley, C., Dahlbeck, D., Clark, Eszter, T, ., and Staskawicz, B. J. (2002). Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc Natl Acad Sci USA, 99, 8336–41.CrossRefGoogle ScholarPubMed
Charity, J. C., Pak, K., Delwiche, C. F., and Hutcheson, S. W. (2003). Novel exchangeable effector loci associated with the Pseudomonas syringae hrp pathogenicity island: evidence for integron-like assembly from transposed gene cassettes. Mol Plant-Microbe Interact, 16, 495–507.CrossRefGoogle ScholarPubMed
Chen, L. L. (2006). Identification of genomic islands in six plant pathogens. Gene, 374, 134–41.CrossRefGoogle ScholarPubMed
Dangl, J. L., Ritter, C., Gibbon, M. J., et al. (1992). Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell, 4, 1359–69.CrossRefGoogle ScholarPubMed
Deng, W. L., Rehm, A. H., Charkowski, A. O., Rojas, C. M., and Collmer, A. (2003). Pseudomonas syringae exchangeable effector loci: Sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J Bacteriol, 185, 2592–602CrossRefGoogle Scholar
Feil, H., Feil, W. S., Chain, P., et al. (2005). Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci USA, 102, 11064–9.CrossRefGoogle ScholarPubMed
Frederick, R. D., Ahmad, M., Majerczak, D. R., et al. (2001). Genetic organization of the Pantoea stewartii subsp. Stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN and wtsE operons. Mol Plant-Microbe Interact, 14, 1213–22.CrossRefGoogle ScholarPubMed
Gao, F., and Zhang, C.-T. (2006). GC-Profile: a web-based tool for visualizing and analyzing the variation of GC content in genomic sequences. Nucleic Acids Res, 34 http://nar.oxfordjournals.org/cgi/content/full/34/suppl_2/W686doi:10.1093/nar/gkl040CrossRefGoogle ScholarPubMed
Genin, S., and Boucher, C. (2004). Lessons learned from the genome analysis of Ralstonia solanacearum. Annu Rev Phytopathol, 42, 107–34.CrossRefGoogle ScholarPubMed
Groisman, E. A., and Ochman, H. (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell, 87, 791–4.CrossRefGoogle ScholarPubMed
Guo, M., Manulis, S., Mor, H., and Barash, I. (2002). The presence of diverse IS elements and an avrPphD homologue that acts as a virulence factor on the pathogenicity plasmid of Erwinia herbicola pv. gypsophilae. Mol Plant-Microbe Interact, 15, 709–16.CrossRefGoogle ScholarPubMed
Hacker, J., and Carniel, E. (2001). Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep, 2, 376–81.CrossRefGoogle ScholarPubMed
Hacker, J., and Kaper, J.B. (2000). Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol, 54, 641–79.CrossRefGoogle ScholarPubMed
Hacker, J., Bender, L., Ott, M., et al. (1990). Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. Microb Pathog 8, 213–25.CrossRefGoogle ScholarPubMed
He, J., Baldini, R. L., Deziel, E., et al. (2004). The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc Natl Acad Sci USA, 101, 2530–5.CrossRefGoogle ScholarPubMed
Hentschel, U., and Hacker, J. (2001). Pathogenicity islands: the tip of the iceberg. Microbes Infect, 3, 545–8.CrossRefGoogle ScholarPubMed
Jackson, R. W., Athanassopoulos, E., Tsiamis, G., et al. (1999). Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc Natl Acad Sci USA, 96, 10875–80.CrossRefGoogle ScholarPubMed
Jackson, R. W., Mansfield, J. W., Arnold, D. L., et al. (2000). Excision from tRNA genes of a large chromosomal region, carrying avrPphB, associated with race change in the bean pathogen, Pseudomonas syringae pv. phaseolicola. Mol Microbiol, 38, 186–97.CrossRefGoogle ScholarPubMed
Jackson, R. W., Mansfield, J. W., Ammouneh, H., et al. (2002). Location and activity of members of a family of virPphA homologues in pathovars of Pseudomonas syringae and P. savastanoi. Mol Plant Pathol, 3, 205–16.CrossRefGoogle ScholarPubMed
Kang, H., and Gross, D. C. (2005). Characterization of a resistance-nodulation-cell division transporter system associated with the syr-syp genomic island of Pseudomonas syringae pv. syringae. Appl Environ Microbiol, 71, 5056–65.CrossRefGoogle ScholarPubMed
Keen, N. T. (1990). Gene-for-gene complementarity in plant–pathogen interactions. Ann Rev Genet, 24, 421–40.CrossRefGoogle ScholarPubMed
Kers, J. A., Cameron, K. D., Joshi, M. V., et al. (2005). A large, mobile pathogenicity island confers plant pathogenicity on Streptomyces species. Mol Microbiol, 55, 1025–33.CrossRefGoogle ScholarPubMed
Kim, J. F., Charkowski, A. O., Alfano, J. A., Collmer, A., and Beer, S. V. (1998). Sequences related to transposable elements and bacteriophages flank avirulence genes of Pseudomonas syringae. Mol Plant-Microbe Interact, 11, 1247–52.CrossRefGoogle Scholar
Kim, J. G., Park, B. K., Yoo, C. H., et al. (2003). Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J Bacteriol, 185, 3155–66.CrossRefGoogle ScholarPubMed
Kinscherf, T. G., and Willis, D. K. (2005). The biosynthetic gene cluster for the beta-lactam antibiotic tabtoxin in Pseudomonas syringae. J Antibiot (Tokyo), 58, 817–21.CrossRefGoogle ScholarPubMed
Kinscherf, T. G., Coleman, R. H., Barta, T. M., and Willis, D. K. (1991). Cloning and expression of the tabtoxin biosynthetic region from Pseudomonas syringae. J Bacteriol, 173, 4124–32.CrossRefGoogle ScholarPubMed
Lavie, M., Seunes, B., Prior, P., and Boucher, C. (2004). Distribution and sequence analysis of a family of type III-dependent effectors correlate with the phylogeny of Ralstonia solanacearum strains. Mol Plant-Microbe Interact, 17, 931–40.CrossRefGoogle ScholarPubMed
Lesic, B., and Carniel, E. (2005). Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. J Bacteriol, 187, 3352–8.CrossRefGoogle ScholarPubMed
Lima, W. C., Sluys, M., and Menck, C. F. M. (2005). Non-Gamma-Proteobacteria gene islands contribute to the Xanthomonas genome. OMICS, 9, 160–72.CrossRefGoogle ScholarPubMed
Mitchell, R. E. (1991). Implications of toxins in the ecology and evolution of plant pathogenic microorganisms: bacteria. Experientia, 47, 791–803.CrossRefGoogle ScholarPubMed
Mor, H., Manulis, S., Zuck, M., et al. (2001). Genetic organization of the hrp gene cluster and dspAE/BF operon in Erwinia herbicola pv. gypsophilae. Mol Plant-Microbe Interact 14, 431–6.CrossRefGoogle ScholarPubMed
Moreira, L. M., Souza, R. F., Digiampietri, L. A., Da Silva, A. C., and Setubal, J. C. (2005). Comparative analyses of Xanthomonas and Xylella complete genomes. OMICS, 9, 43–76CrossRefGoogle ScholarPubMed
Noël, L., Thieme, F., Nennstiel, D., and Bonas, U. (2002). Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J Bacteriol, 184, 1340–8.CrossRefGoogle ScholarPubMed
Nunes, L. R., Rosato, Y. B., Muto, N. H., et al. (2003). Microarray analyses of Xylella fastidiosa provide evidence of coordinated transcription control of laterally transferred elements. Genome Res, 13, 570–8.CrossRefGoogle ScholarPubMed
Oh, C-S., Kim, J. F., and Beer, S. V. (2005). The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infection. Mol Plant Pathol, 6, 125–38.CrossRefGoogle Scholar
Patil, P. B., and Sonti, R. V. (2004). Variation suggestive of horizontal gene transfer at a lipopolysaccharide (lps) biosynthetic locus in Xanthomonas oryzae pv. oryzae, the bacterial leaf blight pathogen of rice. BMC Microbiol, 4, 40.CrossRefGoogle Scholar
Pickard, D., Wain, J., Baker, S., et al. (2003). Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica pathogenicity island SPI-7. J Bacteriol, 185, 5055–65.CrossRefGoogle ScholarPubMed
Pitman, A. R., Jackson, R. W., Mansfield, J. W., et al. (2005). Exposure to host resistance mechanisms drives evolution of bacterial virulence in plants. Curr Biol, 15, 2230–5.CrossRefGoogle ScholarPubMed
Rivas, L. A., Mansfield, J., Tsiamis, G., Jackson, R. W., and Murillo, J. (2005). Changes in race-specific virulence in Pseudomonas syringae pv. phaseolicola are associated with a chimeric transposable element and rare deletion events in a plasmid borne pathogenicity island. Appl Environ Microbiol, 71, 3778–85.CrossRefGoogle Scholar
Rohmer, L., Kjemtrup, S., Marchesini, P., and Dangl, J. L. (2003). Nucleotide sequence, functional characterization and evolution of pFKN, a virulence plasmid in Pseudomonas syringae pathovar maculicola. Mol Microbiol, 47, 1545–62.CrossRefGoogle ScholarPubMed
Rossier, O., Ackerveken, G., and Bonas, U. (2000). HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol Microbiol, 38, 828–38.CrossRefGoogle ScholarPubMed
Sawada, H., Kanaya, S., Tsuda, M., et al. (2002). A phylogenomic study of the OCTase genes in Pseudomonas syringae pathovars: the horizontal transfer of the argK-tox cluster and the evolutionary history OCTase genes on their genomes. J Mol Evol, 54, 437–57.CrossRefGoogle ScholarPubMed
Scholz-Schroeder, B. K., Hutchison, M. L., Grgurina, I., and Gross, D. C. (2001). The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Mol Plant-Microbe Interact, 14, 336–48.CrossRefGoogle ScholarPubMed
Stavrinides, J., Ma, W., and Guttman, D. (2006). Terminal reassortment drives the quantum evolution of type III effectors in bacterial pathogens. PLoS Pathog, 2, e104.CrossRefGoogle ScholarPubMed
Sugio, A., Yang, B., and White, F. F. (2005). Characterization of the hrpF pathogenicity peninsula of Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact, 18, 546–54.CrossRefGoogle ScholarPubMed
Toth, I. K., Bell, K. S., Holeva, M. C., and Birch, P. R. J. (2003). Soft rot erwiniae: From genes to genomes. Mol Plant Pathol, 4, 17–30.CrossRefGoogle ScholarPubMed
Meer, J. R., and Sentchilo, V. (2003). Genomic islands and the evolution of catabolic pathways in bacteria. Curr Opin Biotechnol, 14, 248–54.CrossRefGoogle ScholarPubMed
Dijk, K., Fouts, D. E., Rehm, A. H., et al. (1999). The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J Bacteriol, 181, 4790–7.Google Scholar
Sluys, M. A., Oliveira, M. C., Monteiro-Vitorello, C. B., et al. (2003). Comparative analyses of the complete genome sequences of Pierce's disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol, 185, 1018–26.CrossRefGoogle ScholarPubMed
Wang, N., Lu, S. E., Yang, Q., Sze, S. H., and Gross, D. C. (2006). Identification of the syr-syp box in the promoter regions of genes dedicated to syringomycin and syringopeptin production by Pseudomonas syringae pv. syringae B301D. J Bacteriol, 188, 160–8.CrossRefGoogle ScholarPubMed
Wilson, J. W., and Nickerson, C. A. (2006). A new experimental approach for studying bacterial genomic island evolution identifies island genes with bacterial host-specific expression patterns. BMC Evol Biol, 6, 2.CrossRefGoogle ScholarPubMed
Zhang, Y., Rowley, K. B., and Patil, S. S. (1993). Genetic organization of a cluster of genes involved in the production of phaseolotoxin, a toxin produced by Pseudomonas syringae pv. phaseolicola. J Bacteriol, 175, 6451–8.CrossRefGoogle ScholarPubMed

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