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Journal of Bacteriology, April 2005, p. 2458-2468, Vol. 187, No. 7
0021-9193/05/$08.00+0     doi:10.1128/JB.187.7.2458-2468.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

The Type III-Dependent Hrp Pilus Is Required for Productive Interaction of Xanthomonas campestris pv. vesicatoria with Pepper Host Plants

Ernst Weber,1 Tuula Ojanen-Reuhs,2,{dagger} Elisabeth Huguet,3,{ddagger} Gerd Hause,4 Martin Romantschuk,2,§ Timo K. Korhonen,2 Ulla Bonas,1,3 and Ralf Koebnik1*

Institute of Genetics,1 Biozentrum, Martin Luther University, Halle, Germany,4 General Microbiology, Faculty of Biosciences, University of Helsinki, Helsinki, Finland,2 Institut des Sciences Végétales, CNRS, Gif-sur-Yvette, France3

Received 10 November 2004/ Accepted 28 December 2004

The plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria expresses a type III secretion system that is necessary for both pathogenicity in susceptible hosts and the induction of the hypersensitive response in resistant plants. This specialized protein transport system is encoded by a 23-kb hrp (hypersensitive response and pathogenicity) gene cluster. Here we show that X. campestris pv. vesicatoria produces filamentous structures, the Hrp pili, at the cell surface under hrp-inducing conditions. Analysis of purified Hrp pili and immunoelectron microscopy revealed that the major component of the Hrp pilus is the HrpE protein which is encoded in the hrp gene cluster. Sequence homologues of hrpE are only found in other xanthomonads. However, hrpE is syntenic to the hrpY gene from another plant pathogen, Ralstonia solanacearum. Bioinformatic analyses suggest that all major Hrp pilus subunits from gram-negative plant pathogens may share the same structural organization, i.e., a predominant alpha-helical structure. Analysis of nonpolar mutants in hrpE demonstrated that the Hrp pilus is essential for the productive interaction of X. campestris pv. vesicatoria with pepper host plants. Furthermore, a functional Hrp pilus is required for type III-dependent protein secretion. Immunoelectron microscopy revealed that type III-secreted proteins, such as HrpF and AvrBs3, are in close contact with the Hrp pilus during and/or after their secretion. By systematic analysis of nonpolar hrp/hrc (hrp conserved) and hpa (hrp associated) mutants, we found that Hpa proteins as well as the translocon protein HrpF are dispensable for pilus assembly, while all other Hrp and Hrc proteins are required. Hence, there are no other conserved Hrp or Hrc proteins that act downstream of HrpE during type III-dependent protein translocation.

* Corresponding author. Mailing address: Martin-Luther-Universität, Institut für Genetik, Weinbergweg 10, D-06120 Halle (Saale), Germany. Phone: 49 345 5526293. Fax: 49 345 5527151. E-mail: koebnik{at}gmx.de.

{dagger} Present address: Purdue University, Department of Food Sciences, West Lafayette, IN 47907.

{ddagger} Present address: Institut de Recherche sur la Biologie de l'Insecte, UMR, CNRS 6035, Faculté des Sciences, F-37200 Tours, France.

§ Present address: University of Helsinki, Department of Ecological and Environmental Sciences, FIN-15140 Lahti, Finland.

Journal of Bacteriology, April 2005, p. 2458-2468, Vol. 187, No. 7
0021-9193/05/$08.00+0     doi:10.1128/JB.187.7.2458-2468.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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