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Title: Broadly conserved fungal effector BEC1019 suppresses host cell death and enhances pathogen virulence in powdery mildew of barley (Hordeum vulgare L.)

item WHIGHAM, EHREN - Iowa State University
item QI, SHAN - Cornell University
item MISTRY, DIVYA - Iowa State University
item SURANA, PRIYANKA - Iowa State University
item XU, RUO - Iowa State University
item Fuerst, Gregory
item PLIEGO, CLARA - Imperial College
item BINDSCHEDLER, LAURENCE - University Of London
item SPANU, PIETRO - Imperial College
item DICKERSON, JULIE - Iowa State University
item INNES, ROGER - Indiana University
item NETTLETON, DAN - Iowa State University
item BOGDANOVE, ADAM - Cornell University
item Wise, Roger

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/9/2015
Publication Date: 4/30/2015
Citation: Whigham, E., Qi, S., Mistry, D., Surana, P., Xu, R., Fuerst, G.S., Pliego, C., Bindschedler, L., Spanu, P., Dickerson, J., Innes, R.W., Nettleton, D., Bogdanove, A.J., Wise, R.P. 2015. Broadly conserved fungal effector BEC1019 suppresses host cell death and enhances pathogen virulence in powdery mildew of barley (Hordeum vulgare L.). Molecular Plant-Microbe Interactions. 28(9): 968-983. DOI:

Interpretive Summary: Crop loss caused by disease remains one of the greatest challenges in agriculture in both developed and developing countries. Pathogenic fungi, viruses, bacteria, insects, and nematodes parasitize agronomic and horticultural crops, as well as commercial and recreational forests. Certain pathogens, like powdery mildews, require living host tissue to survive. This requirement means host defenses must be overcome throughout the pathogen’s entire life cycle. Commonly, pathogens use small molecules, called effectors, to suppress, modify, or evade host defense. Genomic and proteogenomic studies have identified nearly 500 candidate secreted effector proteins from the powdery mildew fungus that infects barley. Here we show that silencing one effector, BEC1019, results in significantly less fungal growth than a control interaction. In addition, BEC1019 is able to suppress cell death induced by a bacterial effector when delivered by the Xanthomonas type III secretion system. Copies of this gene (orthologs) are found in 97 fungal species spread across the fungal kingdom. In addition to several major plant pathogens, orthologs are found in pathogens of animals and free-living fungi like baker’s yeast. Such broad conservation suggests study of this effector could have implications for both medicine and agriculture. Because common themes govern all plant-pathogen interactions, this finding provides new knowledge of broad significance to plant scientists, and to growers who utilize disease resistance to protect their crops. This will be used to develop new ways to combat diseases of crop plants, most notable cereal grains, which are our most important food sources.

Technical Abstract: The interaction of barley, Hordeum vulgare L., with the biotrophic powdery mildew fungus, Blumeria graminis f. sp. hordei, is an ideal model to address fundamental questions in host resistance and susceptibility. Effector proteins secreted by B. graminis act to inhibit, induce, or accelerate host processes to allow colonization and nutrient acquisition by the pathogen. Previous research identified a collection of novel effectors secreted by B. graminis that contribute to pathogen virulence. Blumeria effector candidate (BEC) 1019, a predicted metalloprotease, is expressed in haustorial feeding structures, and Host-Induced-Gene-Silencing. Silencing of BEC1019 restricts haustorial development in compatible interactions. Here we show that Barley Stripe Mosaic Virus-Induced Gene Silencing of BEC1019 significantly reduces the accumulation of fungal biomass in infected barley leaves. Delivery of BEC1019 to the host cell cytoplasm via Xanthomonas type III secretion suppresses cultivar non-specific hypersensitive reaction (HR) induced by Xanthomonas oryzae pv. oryzicola, as well as cultivar specific HR induced by the AvrPphB effector from Pseudomonas syringae pv. phaseolicola. Site-directed mutagenesis of BEC1019 implicates a conserved ETVIC motif as required for suppression of HR. Orthologs of BEC1019 are present in 97 of 241 sequenced fungal genomes, including plant pathogens Magnaporthe oryzae (rice blast) and Fusarium graminearum (Fusarium head blight of barley and wheat), as well as the human pathogens Candida albicans and Aspergillus fumigatus. The C. albicans ortholog phenocopies BEC1019 in the Xanthomonas type III secretion assay. Random Forest analysis identified amino acid residues flanking the ETVIC motif that are predictive of plant parasitism. BEC1019 represents a new class of biotrophic effector remarkable for its broad conservation.