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MBE Advance Access published online on September 1, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl103
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted August 28, 2006

Research Article

Diversifying Selection Drives the Evolution of the Type III Secretion System Pilus of Pseudomonas syringae

David S. Guttman 1 *, Susan J. Gropp 1, Robyn L. Morgan 1, and Pauline W. Wang 1

1 Department of Botany, Centre for the Analysis of Genome Evolution and Function, University of Toronto, 25 Willcocks St., Toronto, ON M5S 3B2, CANADA

* To whom correspondence should be addressed.
David S. Guttman, E-mail: david.guttman{at}utoronto.ca


  Abstract

The plant pathogenic bacterium Pseudomonas syringae uses a type III secretion system (T3SS) to inject virulence proteins directly into the cytoplasm of its hosts. The P. syringae type III secretion apparatus is encoded, in part, by the HrpZ operon, which carries the hrpA gene that encodes the pilin subunit of the pilus, various components of the structural apparatus, and the HrpZ harpin protein that is believed to produce pores in the host cell membrane. The pilus of the type III system comes into direct contact with the host cell, and is therefore a likely target of the host's pathogen surveillance systems. We sequenced and analyzed 22 HrpZ operons from P. syringae strains spanning the diversity of the species. Selection analyses, including Ka/Ks tests and Tajima's D, revealed strong diversifying selection acting on the hrpA gene. This form of selection enables pathogens to maintain genetic diversity within their populations, and is often driven by selection imposed by host defense systems. The HrpZ operon also revealed a single significant recombination event that dramatically changed the evolutionary relationships among P. syringae strains from two quite distinct phylogroups. This recombination event appears to have introduced genetic diversity into a clade of strains that may now be undergoing positive selection. The identification of diversifying selection acting on the Hrp pilus across the whole population sample, and positive selection within one P. syringae clade supports a trench warfare co-evolutionary model between P. syringae and its plant hosts.

Keywords: type III secretion system (T3SS); diversifying selection; pilus; recombination; Pseudomonas syringae; HrpA.
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