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454 Genome Sequencing of Pseudoperonospora cubensis Reveals Effector Proteins with a QXLR Translocation Motif

May 2011 , Volume 24 , Number  5
Pages  543 - 553

Miaoying Tian,1 Joe Win,2 Elizabeth Savory,1 Alyssa Burkhardt,3 Michael Held,4 Federica Brandizzi,4 and Brad Day1,3,5

1Department of Plant Pathology, Michigan State University, East Lansing, MI 48824, U.S.A.; 2The Sainsbury Laboratory, Norwich, NR4 7UH, United Kingdom; and 3Graduate Program in Cellular and Molecular Biology, 4Department of Energy-Plant Research Laboratory, and 5Graduate Program in Genetics, Michigan State University, East Lansing, MI, U.S.A.

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Accepted 7 January 2011.

Pseudoperonospora cubensis is a biotrophic oomycete pathogen that causes downy mildew of cucurbits, a devastating foliar disease threatening cucurbit production worldwide. We sequenced P. cubensis genomic DNA using 454 pyrosequencing and obtained random genomic sequences covering approximately 14% of the genome, thus providing the first set of useful genomic sequence information for P. cubensis. Using bioinformatics approaches, we identified 32 putative RXLR effector proteins. Interestingly, we also identified 29 secreted peptides with high similarity to RXLR effectors at the N-terminal translocation domain, yet containing an R-to-Q substitution in the first residue of the translocation motif. Among these, a family of QXLR-containing proteins, designated as PcQNE, was confirmed to have a functional signal peptide and was further characterized as being localized in the plant nucleus. Internalization of secreted PcQNE into plant cells requires the QXLR-EER motif. This family has a large number of near-identical copies within the P. cubensis genome, is under diversifying selection at the C-terminal domain, and is upregulated during infection of plants, all of which are common characteristics of characterized oomycete effectors. Taken together, the data suggest that PcQNE are bona fide effector proteins with a QXLR translocation motif, and QXLR effectors are prevalent in P. cubensis. Furthermore, the massive duplication of PcQNE suggests that they might play pivotal roles in pathogen fitness and pathogenicity.

© 2011 The American Phytopathological Society