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Host-Induced Gene Silencing in Barley Powdery Mildew Reveals a Class of Ribonuclease-Like Effectors

June 2013 , Volume 26 , Number  6
Pages  633 - 642

Clara Pliego,1 Daniela Nowara,2 Giulia Bonciani,1 Dana M. Gheorghe,1 Ruo Xu,3 Priyanka Surana,4,5 Ehren Whigham,5 Dan Nettleton,5 Adam J. Bogdanove,5 Roger P. Wise,5,6 Patrick Schweizer,2 Laurence V. Bindschedler,7 and Pietro D. Spanu1

1Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, United Kingdom; 2Leibniz-Institute of Plant Genetics and Crop Plant Research, 06466-Gatersleben, Germany; 3Department of Statistics, Iowa State University, Ames, IA, 50011-1210, U.S.A.; 4Bioinformatics and Computational Biology Graduate Program, Iowa State University, Ames, IA 50011-3260, U.S.A.; 5Department of Plant Pathology & Microbiology and Center for Plant Responses to Environmental Stresses, Iowa State University, Ames, IA, 50011-1020, U.S.A.; 6Corn Insects and Crop Genetics Research Unit, U.S. Department of Agriculture-Agricultural Research Service, Iowa State University, Ames, Iowa 50011–1020, U.S.A.; 7Department of Chemistry, University of Reading, Whiteknights Campus, Reading, RG6 6AS, United Kingdom

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Accepted 20 February 2013.

Obligate biotrophic pathogens of plants must circumvent or counteract defenses to guarantee accommodation inside the host. To do so, they secrete a variety of effectors that regulate host immunity and facilitate the establishment of pathogen feeding structures called haustoria. The barley powdery mildew fungus Blumeria graminis f. sp. hordei produces a large number of proteins predicted to be secreted from haustoria. Fifty of these Blumeria effector candidates (BEC) were screened by host-induced gene silencing (HIGS), and eight were identified that contribute to infection. One shows similarity to β-1,3 glucosyltransferases, one to metallo-proteases, and two to microbial secreted ribonucleases; the remainder have no similarity to proteins of known function. Transcript abundance of all eight BEC increases dramatically in the early stages of infection and establishment of haustoria, consistent with a role in that process. Complementation analysis using silencing-insensitive synthetic cDNAs demonstrated that the ribonuclease-like BEC 1011 and 1054 are bona fide effectors that function within the plant cell. BEC1011 specifically interferes with pathogen-induced host cell death. Both are part of a gene superfamily unique to the powdery mildew fungi. Structural modeling was consistent, with BEC1054 adopting a ribonuclease-like fold, a scaffold not previously associated with effector function.

© 2013 The American Phytopathological Society