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MBE Advance Access originally published online on September 1, 2006
Molecular Biology and Evolution 2006 23(12):2342-2354; 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

Research Articles

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

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

Department of Botany, Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario, Canada

E-mail: david.guttman{at}utoronto.ca.

The plant pathogenic bacterium Pseudomonas syringae uses a type III secretion system 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 encoding 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 2 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 lineage supports a trench warfare coevolutionary model between P. syringae and its plant hosts.

Key Words: type III secretion system (T3SS) • diversifying selection • pilus • recombination • Pseudomonas syringae • HrpA


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