Plant Cell Advance Online Publication
Published on August 3, 2007; 10.1105/tpc.107.051037
Received February 10, 2007
Returned for revision June 30, 2007
Accepted July 7, 2007
Adaptive Evolution Has Targeted the C-Terminal Domain of the RXLR Effectors of Plant Pathogenic Oomycetes
Joe Win 1, William Morgan 2, Jorunn Bos 1, Ksenia V. Krasileva 3, Liliana M. Cano 1, Angela Chaparro-Garcia 1, Randa Ammar 1, Brian J. Staskawicz 3, and Sophien Kamoun 1*
1 Department of Plant Pathology, Ohio State University Ohio Agricultural Research and Development Center, Wooster, Ohio 44691
2 Department of Biology, College of Wooster, Wooster, Ohio 44691
3 Department of Plant and Microbial Biology, University of California, Berkeley, California 94270
* To whom correspondence should be addressed. E-mail: kamoun.1{at}osu.edu.
Oomycete plant pathogens deliver effector proteins inside host cells to modulate plant defense circuitry and to enable parasitic colonization. These effectors are defined by a conserved motif, termed RXLR (for Arg, any amino acid, Leu, Arg), that is located downstream of the signal peptide and that has been implicated in host translocation. Because the phenotypes of RXLR effectors extend to plant cells, their genes are expected to be the direct target of the evolutionary forces that drive the antagonistic interplay between pathogen and host. We used the draft genome sequences of three oomycete plant pathogens, Phytophthora sojae, Phytophthora ramorum, and Hyaloperonospora parasitica, to generate genome-wide catalogs of RXLR effector genes and determine the extent to which these genes are under positive selection. These analyses revealed that the RXLR sequence is overrepresented and positionally constrained in the secretome of Phytophthora relative to other eukaryotes. The three examined plant pathogenic oomycetes carry complex and diverse sets of RXLR effector genes that have undergone relatively rapid birth and death evolution. We obtained robust evidence of positive selection in more than two-thirds of the examined paralog families of RXLR effectors. Positive selection has acted for the most part on the C-terminal region, consistent with the view that RXLR effectors are modular, with the N terminus involved in secretion and host translocation and the C-terminal domain dedicated to modulating host defenses inside plant cells.
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