Broadly Conserved Fungal Effector BEC1019 Suppresses Host Cell Death and Enhances Pathogen Virulence in Powdery Mildew of Barley (Hordeum vulgare L.).
The interaction of barley, Hordeum vulgare L., with the powdery mildew fungus Blumeria graminis f. sp. hordei is a well-developed model to investigate resistance and susceptibility to obligate biotrophic pathogens. The 130-Mb Blumeria genome encodes approximately 540 predicted effectors that are hypothesized to suppress or induce host processes to promote colonization. Blumeria effector candidate (BEC)1019, a single-copy gene encoding a putative, secreted metalloprotease, is expressed in haustorial feeding structures, and host-induced gene silencing of BEC1019 restricts haustorial development in compatible interactions. Here, we show that Barley stripe mosaic virus-induced gene silencing of BEC1019 significantly reduces fungal colonization of barley epidermal cells, demonstrating that BEC1019 plays a central role in virulence. In addition, delivery of BEC1019 to the host cytoplasm via Xanthomonas type III secretion suppresses cultivar nonspecific hypersensitive reaction (HR) induced by Xanthomonas oryzae pv. oryzicola, as well as cultivar-specific HR induced by AvrPphB from Pseudomonas syringae pv. phaseolicola. BEC1019 homologs are present in 96 of 241 sequenced fungal genomes, including plant pathogens, human pathogens, and free-living nonpathogens. Comparative analysis revealed variation at several amino acid positions that correlate with fungal lifestyle and several highly conserved, noncorrelated motifs. Site-directed mutagenesis of one of these, ETVIC, compromises the HR-suppressing activity of BEC1019. We postulate that BEC1019 represents an ancient, broadly important fungal protein family, members of which have evolved to function as effectors in plant and animal hosts.
1 Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, 50011, U.S.A.;
Ehren
E
Whigham
2 Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, New York, 14853, U.S.A.;
Shan
S
Qi
3 Bioinformatics and Computational Biology, Iowa State University;
Divya
D
Mistry
1 Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, 50011, U.S.A.;|3 Bioinformatics and Computational Biology, Iowa State University;
Priyanka
P
Surana
4 Department of Statistics, Iowa State University;
Ruo
R
Xu
1 Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, 50011, U.S.A.;|5 Corn Insects and Crop Genetics Research, USDA-Agricultural Research Service, Iowa State University;
Gregory
G
Fuerst
6 Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, U. K.;
Clara
C
Pliego
7 School of Biological Sciences, Royal Holloway University of London (RHUL), Egham, Surrey, TW20 0EX, U. K.;
Laurence V
LV
Bindschedler
6 Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, U. K.;
Pietro D
PD
Spanu
3 Bioinformatics and Computational Biology, Iowa State University;|8 Department of Electrical and Computer Engineering, Iowa State University;
Julie A
JA
Dickerson
9 Department of Biology, Indiana University, Bloomington, IN, 47405, U.S.A.
Roger W
RW
Innes
4 Department of Statistics, Iowa State University;
Dan
D
Nettleton
2 Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, New York, 14853, U.S.A.;
Adam J
AJ
Bogdanove
1 Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, 50011, U.S.A.;|3 Bioinformatics and Computational Biology, Iowa State University;|5 Corn Insects and Crop Genetics Research, USDA-Agricultural Research Service, Iowa State University;
Roger P
RP
Wise
D000595:Amino Acid Sequence; D001203:Ascomycota / Q000235:genetics / Q000378:metabolism / Q000472:pathogenicity*; D017124:Conserved Sequence; D015966:Gene Expression Regulation, Fungal / Q000502:physiology; D020868:Gene Silencing; D001467:Hordeum / Q000382:microbiology*; D008969:Molecular Sequence Data; D010802:Phylogeny; D010935:Plant Diseases / Q000382:microbiology*; D018515:Plant Leaves; D010942:Plant Viruses; D014774:Virulence; D014974:Xanthomonas / Q000378:metabolism