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A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora larici-populina (Poplar Leaf Rust)

March 2012 , Volume 25 , Number  3
Pages  279 - 293

Stéphane Hacquard,1 David L. Joly,2 Yao-Cheng Lin,3 Emilie Tisserant,1 Nicolas Feau,2 Christine Delaruelle,1 Valérie Legué,1 Annegret Kohler,1 Philippe Tanguay,2 Benjamin Petre,1 Pascal Frey,1 Yves Van de Peer,3 Pierre Rouzé,3 Francis Martin,1 Richard C. Hamelin,2,4 and Sébastien Duplessis1

1Unité Mixte de Recherche 1136 Institut National de la Recherche Agronomique-Nancy Université, Interactions Arbres/Microorganismes, INRA Nancy, 54280 Champenoux, France; 2Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du PEPS, P.O. Box 10380, Stn. Sainte-Foy, Québec, QC, G1V 4C7, Canada; 3Department of Plant Systems Biology, VIB, Ghent University, 9052 Ghent, Belgium; 4Department of Forest Sciences, Faculty of Forestry, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

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Accepted 26 October 2011.

The obligate biotrophic rust fungus Melampsora larici-populina is the most devastating and widespread pathogen of poplars. Studies over recent years have identified various small secreted proteins (SSP) from plant biotrophic filamentous pathogens and have highlighted their role as effectors in host–pathogen interactions. The recent analysis of the M. larici-populina genome sequence has revealed the presence of 1,184 SSP-encoding genes in this rust fungus. In the present study, the expression and evolutionary dynamics of these SSP were investigated to pinpoint the arsenal of putative effectors that could be involved in the interaction between the rust fungus and poplar. Similarity with effectors previously described in Melampsora spp., richness in cysteines, and organization in large families were extensively detailed and discussed. Positive selection analyses conducted over clusters of paralogous genes revealed fast-evolving candidate effectors. Transcript profiling of selected M. laricipopulina SSP showed a timely coordinated expression during leaf infection, and the accumulation of four candidate effectors in distinct rust infection structures was demonstrated by immunolocalization. This integrated and multifaceted approach helps to prioritize candidate effector genes for functional studies.

© 2012 The American Phytopathological Society