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Hrp-dependent biotrophic mechanism of virulence: How has it evolved in tumorigenic bacteria?

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Abstract

A mechanism of virulence mediated byhrp-genes is present in many Gram-negative bacterial pathogens. It involves delivery of effector proteins into host cellsvia the type III secretion system (TTSS) and the interaction of TTSS effectors with plant proteins. These interactions may either promote responses beneficial to the pathogen or trigger the hypersensitive response if an effector is recognized by corresponding resistance protein.Pantoea agglomerans, which is widespread in nature mainly as an epiphyte, has evolved into ahrp-dependent and host-specific tumorigenic pathogen by acquiring a plasmid containing a pathogenicity island (PAI). This PAI harbors ahrp-gene cluster, and genes encoding for TTSS effector proteins and biosynthesis of IAA and cytokinins. The results reviewed describe how the interplay between negative-acting and positive-acting TTSS effectors determines the transformation ofP. agglomerans into two related pathovars. Furthermore, the PAI’s structure supports the premise that these pathovars are recently evolved pathogens. Finally, the possible interaction between TTSS effectors and phytohormones for gall formation is proposed.

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References

  1. Alfano, J.R., Charkowski, A.O., Deng, W., Badel, J.L., Petnicki-Ocwieja, T., van Dijk, K.et al. (2000) ThePseudomonas 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.PNAS 97:4856–4861.

    Article  PubMed  CAS  Google Scholar 

  2. Burr, T.J., Katz, B.H., Abawi, G.S. and Crosier, D.C. (1991) Comparison of tumorigenic strains ofErwinia herbicola isolated from table beet withE.h. gypsophilae.Plant Dis. 75:855–858.

    Google Scholar 

  3. Chalupowicz, L., Schwarz, M., Aloni, R., Barash, I. and Manulis, M. (2003) Anatomical structure of galls induced byErwinia herbicola pv.gypsophilae onGypsophila paniculata.Abstr. 8th Int. Congr. Plant Pathology (Christchurch, New Zealand), p. 13.

  4. Chang, J.F., Goel, A.K., Grant, S.R. and Dangl, J.L. (2004) Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria.Curr. Opin. Microbiol. 7:11–18.

    Article  PubMed  CAS  Google Scholar 

  5. Clark, E., Manulis, S., Ophir, Y., Barash, I. and Gafni, Y. (1993) Cloning and characterization ofiaaM andiaaH fromErwinia herbicola pathovargypsophilae.Phytopathology 83:234–240.

    Article  CAS  Google Scholar 

  6. Collmer, A., Lindeberg, M., Petnicki-Ocwieja, T., Schneider, D.J. and Alfano, J.R. (2002) Genomic mining type III secretion system effectors inPseudomonas syringae yields new picks for all TTSS prospectors.Trends Microbiol. 10:462–469.

    Article  PubMed  CAS  Google Scholar 

  7. Cooksey, D.A. (1986) Galls ofGypsophila paniculata caused byErwinia herbicola.Plant Dis. 70:464–468.

    Article  Google Scholar 

  8. Dangl, J.L. and Jones, J.D.G. (2001) Plant pathogens and integrated defense responses to infection.Nature 411:826–833.

    Article  PubMed  CAS  Google Scholar 

  9. Ezra, D., Barash, I., Valinsky, L. and Manulis, S. (2000) The dual function in virulence and host range restriction of a gene isolated from the pPATH Ehg plasmid ofErwinia herbicola pv.gypsophilae.Mol. Plant-Microbe Interact. 13:693–698.

    Article  Google Scholar 

  10. Ezra, D., Barash, I., Weinthal, D.M., Gaba, V. and Manulis, S. (2004)pthG fromPantoea agglomerans pv.gypsophilae encodes an avirulence effector that determines incompatibility in multiple beet species.Mol. Plant Pathol. 5:105–114.

    Article  CAS  Google Scholar 

  11. Galan, J.E. and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells.Science 284:1322–1328.

    Article  PubMed  CAS  Google Scholar 

  12. Grauer, D. and Wen-Hsiung, L. (2000) Fundamentals of Molecular Evolution. Sinauer Associates, Inc., Publishers, Sunderland, MA, USA.

    Google Scholar 

  13. Guo, M., Manulis, S., Mor, H. and Barash, I. (2002) The presence of diverse IS elements and anavrPphD homologue that acts as a virulence factor on the pathogenicity plasmid ofErwinia herbicola pv.gypsophilae.Mol. Plant-Microbe Interact. 15:709–716.

    Article  PubMed  CAS  Google Scholar 

  14. Hacker, J. and Kaper, J.B. (2000) Pathogenicity islands and the evolution of microbes.Annu. Rev. Microbiol. 54:641–679.

    Article  PubMed  CAS  Google Scholar 

  15. He, S.Y, and Jin, Q. (2003) The Hrp pilus: learning from flagella.Curr. Opin. Microbiol. 6:15–19.

    Article  PubMed  CAS  Google Scholar 

  16. Iacobellis, N.S., Sisto, A., Surico, G., Evidente, A. and DiMaio, E. (1994) Pathogenicity ofPseudomonas syringae subsp.savastanoi mutants defective in phytohormone production.J. Phytopathol. 140:238–248.

    Article  Google Scholar 

  17. Innes, R. (2003) New effects of type III effectors.Mol. Microbiol. 50:363–365.

    Article  PubMed  CAS  Google Scholar 

  18. Keen, N.T. (1990) Gene-for-gene complementarity in plant pathogen interactions.Annu. Rev. Genet. 24:447–463.

    Article  PubMed  CAS  Google Scholar 

  19. Kjemtrup, S., Nimchuk, Z. and Dangl, J.L. (2000) Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition.Curr. Opin. Microbiol. 3:73–78.

    Article  PubMed  CAS  Google Scholar 

  20. Laby, R.J. and Beer, S.V. (1992) Hybridization and functional complementation of thehrp gene cluster fromErwinia amylovora strain Ea321 with DNA of other bacteria.Mol. Plant-Microbe Interact. 5:412–419.

    CAS  Google Scholar 

  21. Lahaye, T. and Bonas, U. (2001) Molecular secretes of bacterial type III proteins.Trends Plant Sci. 6:479–484.

    Article  PubMed  CAS  Google Scholar 

  22. Leach, J.E. and White, F.F. (1996) Bacterial avirulence genes.Annu. Rev. Phytopathol. 34:153–179.

    Article  PubMed  CAS  Google Scholar 

  23. Lichter, A., Barash, I., Valinsky, L. and Manulis, S. (1995) The genes involved in cytokinin biosynthesis inErwinia herbicola pv.gypsophilae: characterization and role in gall formation.J. Bacteriol. 177:4457–4465.

    PubMed  CAS  Google Scholar 

  24. Lindgren, P.B. (1997) The role ofhrp genes during plant-bacterial interactions.Annu. Rev. Phytopathol. 35:129–152.

    Article  PubMed  CAS  Google Scholar 

  25. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R. and Dangl, J.L. (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance.Cell 112:379–389.

    Article  PubMed  CAS  Google Scholar 

  26. Mackey, D., Holt, B.F., Wiig, A. and Dangl, J.L. (2002) RIN4 interacts withPseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance inArabidopsis.Cell 108:743–754.

    Article  PubMed  CAS  Google Scholar 

  27. Manulis, S. and Barash, I. (2003) The molecular basis for transformation of an epiphyte into a gall-forming pathogen as exemplified byErwinia herbicola pv.gypsophilae.in: Stacey, G. and Keen, N. [Eds.] Plant-Microbe Interactions. American Phytopathological Society, St. Paul, MN, USA. pp. 19–52.

    Google Scholar 

  28. Manulis, S. and Barash, I. (2003)Pantoea agglomerans pvs.gypsophilae andbetae, recently evolved pathogens?Mol. Plant Pathol. 4:307–314.

    Article  CAS  Google Scholar 

  29. Manulis, S., Gafni, Y., Clark, E., Zutra, D., Ophir, Y. and Barash, I. (1991) Identification of a plasmid DNA probe for detection ofErwinia herbicola pathogenic onGypsophila paniculata.Phytopathology 81:54–57.

    Article  Google Scholar 

  30. Manulis, S., Haviv-Chesner, A., Brandl, M.T., Lindow, S.E. and Barash, I. (1998) Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness ofErwinia herbicola pv.gypsophilae.Mol. Plant-Microbe Interact. 11:634–642.

    Article  PubMed  CAS  Google Scholar 

  31. Mor, H., Manulis, S., Zuc, M., Nizan, R., Coplin, D.L., and Barash, I. (2001) Genetic organization of thehrp gene cluster and dspAE/BF operon inErwinia herbicola pv.gypsophilae.Mol. Plant-Microbe Interact. 14:431–436.

    Article  PubMed  CAS  Google Scholar 

  32. Morris, R.O. (1986) Genes specifying auxin and cytokinin biosynthesis in phytopathogens.Annu. Rev. Plant Physiol. 37:509–538.

    Article  CAS  Google Scholar 

  33. Morschhauser, J., Kohler, G., Ziebuhr, W., Blum-Oehler, G., Dobrindt, U. and Hacker, J. (2000) Evolution of microbial pathogens.Phil. Trans. R. Soc. Lond. B 355:695–704.

    Article  CAS  Google Scholar 

  34. Nizan, R., Barash, I., Valinsky, L., Lichter, A. and Manulis, S. (1997) The presence ofhrp genes on the pathogenicity-associated plasmid of the tumorigenic bacteriumErwinia herbicola pv.gypsophilae.Mol. Plant-Microbe Interact. 10:677–682.

    Article  PubMed  CAS  Google Scholar 

  35. Patten, C.L. and Glick, B.R. (1996) Bacterial biosynthesis of indole-3-acetic acid.Can. J. Microbiol. 42:207–220.

    Article  PubMed  CAS  Google Scholar 

  36. Schneider, D.S. (2002) Plant immunity and film noir: what gumshoe detectives can teach us about plantpathogen interactions?Cell 109:537–540.

    Article  PubMed  CAS  Google Scholar 

  37. Sisto, A., Cipriani, M.G. and Morea, M. (2004) Knot formation caused byPseudomonas syringae subsp.savastanoi on olive plants ishrp-dependent.Phytopathology 94:484–489.

    Article  PubMed  CAS  Google Scholar 

  38. Valinsky, L., Barash, I., Chalupowicz, L., Ezra, D. and Manulis, S. (2002) Regulation ofhsvG, a host-specific virulence gene fromErwinia herbicola pv.gypsophilae.Physiol. Mol. Plant Pathol. 60:19–29.

    Article  CAS  Google Scholar 

  39. Valinsky, L., Manulis, S., Nizan, R., Ezra, D. and Barash, I. (1998) A pathogenicity gene isolated from the pPATH ofErwinia herbicola pv.gypsophila determines host specificity.Mol. Plant-Microbe Interact. 11:753–762.

    Article  PubMed  CAS  Google Scholar 

  40. Vasanthakumar, A. and McManus, P.C. (2004) Indole-3-acetic acid-producing bacteria are associated with cranberry stem gall.P 94:1164–1171.

    CAS  Google Scholar 

  41. Yamada, Y. (1993) The role of auxin in plant-disease development.Annu. Rev. Phytopathol. 31:253–273.

    Article  PubMed  CAS  Google Scholar 

  42. Zhu, J., Oger, P.M., Schrammeijer, B., Hooykaas, P.J.J., Farrand, S.K. and Winans, S.C. (2000) The bases of crown gall tumorigenesis.J. Bacteriol. 182:3885–3895.

    Article  PubMed  CAS  Google Scholar 

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http://www.phytoparasitica.org posting June 15, 2005.

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Barash, I., Manulis, S. Hrp-dependent biotrophic mechanism of virulence: How has it evolved in tumorigenic bacteria?. Phytoparasitica 33, 317–324 (2005). https://doi.org/10.1007/BF02981296

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