RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members

*Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061; and
^†Laboratory of Phytopathology, Wageningen University, and Centre for BioSystems Genomics, NL-6709 PD, Wageningen, The Netherlands

Edited by Jeffrey L. Dangl, University of North Carolina, Chapel Hill, NC, and approved January 8, 2008 (received for review October 2, 2007)

Abstract

Pathogens secrete effector molecules that facilitate the infection of their hosts. A number of effectors identified in plant pathogenic Phytophthora species possess N-terminal motifs (RXLR-dEER) required for targeting these effectors into host cells. Here, we bioinformatically identify >370 candidate effector genes in each of the genomes of P. sojae and P. ramorum. A single superfamily, termed avirulence homolog (Avh) genes, accounts for most of the effectors. The Avh proteins show extensive sequence divergence but are all related and likely evolved from a common ancestor by rapid duplication and divergence. More than half of the Avh proteins contain conserved C-terminal motifs (termed W, Y, and L) that are usually arranged as a module that can be repeated up to eight times. The Avh genes belong to the most rapidly evolving part of the genome, and they are nearly always located at synteny breakpoints. The superfamily includes all experimentally identified oomycete effector and avirulence genes, and its rapid pace of evolution is consistent with a role for Avh proteins in interaction with plant hosts.

Footnotes

^‡To whom correspondence should be addressed. E-mail: bmtyler{at}vt.edu
Author contributions: R.H.Y.J. and B.M.T. designed research; R.H.Y.J. and B.M.T. performed research; R.H.Y.J. and S.T. contributed new reagents/analytic tools; R.H.Y.J. and B.M.T. analyzed data; and R.H.Y.J., F.G., and B.M.T. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The amino acid and DNA sequences of the effector candidate genes have been deposited in the Virginia Bioinformatics Institute Microbial Database, vmd.vbi.vt.edu (accession nos. 158991–159443 for P. sojae and 97196–97586 for P. ramarum), and in GenBank as part of the P. sojae and P. ramorum whole-genome shotgun projects (accession nos. AAQY01000000 for P. sojae and AAQX01000000 for P. ramorum). Virginia Bioinformatics Institute Microbial Database accession nos. of individual genes are listed in SI Table 2.
This article contains supporting information online at www.pnas.org/cgi/content/full/0709303105/DC1.