Plant Cell Advance Online Publication
Published on May 13, 2005; 10.1105/tpc.105.031807
Received February 23, 2005
Returned for revision April 7, 2005
Accepted April 18, 2005
Differential Recognition of Highly Divergent Downy Mildew Avirulence Gene Alleles by RPP1 Resistance Genes from Two Arabidopsis Lines
Anne P. Rehmany 1*, Anna Gordon 1, Laura E. Rose 2, Rebecca L. Allen 1, Miles R. Armstrong 3, Stephen C. Whisson 3, Sophien Kamoun 4, Brett M. Tyler 5, Paul R. J. Birch 3, and Jim L. Beynon 1
1 Warwick HRI, University of Warwick, Wellesbourne, Warwick CV35 9EF, United Kingdom
2 Department of Evolutionary Biology, University of Munich, 82152 Planegg-Martinsried, Germany
3 Plant Pathogen Interactions Programme, Scottish Crop Research Institute, Invergowrie, Dundee DD2 5DA, United Kingdom
4 Department of Plant Pathology, Ohio State University, Ohio Agricultural Research and Development Center, Wooster, Ohio 44691
5 Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061
* To whom correspondence should be addressed. E-mail: anne.rehmany{at}warwick.ac.uk.
The perception of downy mildew avirulence (Arabidopsis thaliana Recognized [ATR]) gene products by matching Arabidopsis thaliana resistance (Recognition of Peronospora parasitica [RPP]) gene products triggers localized cell death (a hypersensitive response) in the host plant, and this inhibits pathogen development. The oomycete pathogen, therefore, is under selection pressure to alter the form of these gene products to prevent detection. That the pathogen maintains these genes indicates that they play a positive role in pathogen survival. Despite significant progress in cloning plant RPP genes and characterizing essential plant components of resistance signaling pathways, little progress has been made in identifying the oomycete molecules that trigger them. Concluding a map-based cloning effort, we have identified an avirulence gene, ATR1NdWsB, that is detected by RPP1 from the Arabidopsis accession Niederzenz in the cytoplasm of host plant cells. We report the cloning of six highly divergent alleles of ATR1NdWsB from eight downy mildew isolates and demonstrate that the ATR1NdWsB alleles are differentially recognized by RPP1 genes from two Arabidopsis accessions (Niederzenz and Wassilewskija). RPP1-Nd recognizes a single allele of ATR1NdWsB; RPP1-WsB also detects this allele plus three additional alleles with divergent sequences. The Emco5 isolate expresses an allele of ATR1NdWsB that is recognized by RPP1-WsB, but the isolate evades detection in planta. Although the Cala2 isolate is recognized by RPP1-WsA, the ATR1NdWsB allele from Cala2 is not, demonstrating that RPP1-WsA detects a novel ATR gene product. Cloning of ATR1NdWsB has highlighted the presence of a highly conserved novel amino acid motif in avirulence proteins from three different oomycetes. The presence of the motif in additional secreted proteins from plant pathogenic oomycetes and its similarity to a host-targeting signal from malaria parasites suggest a conserved role in pathogenicity.
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