title: Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen.
abstract: Disease-resistance genes encoding intracellular nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are key components of the plant innate immune system and typically detect the presence of isolate-specific avirulence (AVR) effectors from pathogens. NLR genes define the fastest-evolving gene family of flowering plants and are often arranged in gene clusters containing multiple paralogs, contributing to copy number and allele-specific NLR variation within a host species. Barley mildew resistance locus a (Mla) has been subject to extensive functional diversification, resulting in allelic resistance specificities each recognizing a cognate, but largely unidentified, AVRagene of the powdery mildew fungus, Blumeria graminis f. sp. hordei (Bgh). We applied a transcriptome-wide association study among 17 Bgh isolates containing different AVRagenes and identified AVRa1and AVRa13, encoding candidate-secreted effectors recognized by Mla1 and Mla13 alleles, respectively. Transient expression of the effector genes in barley leaves or protoplasts was sufficient to trigger Mla1 or Mla13 allele-specific cell death, a hallmark of NLR receptor-mediated immunity. AVRa1and AVRa13are phylogenetically unrelated, demonstrating that certain allelic MLA receptors evolved to recognize sequence-unrelated effectors. They are ancient effectors because corresponding loci are present in wheat powdery mildew. AVRA1recognition by barley MLA1 is retained in transgenic Arabidopsis, indicating that AVRA1directly binds MLA1 or that its recognition involves an evolutionarily conserved host target of AVRA1Furthermore, analysis of transcriptome-wide sequence variation among the Bgh isolates provides evidence for Bgh population structure that is partially linked to geographic isolation.
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne D-50829, Germany.
authors.forename: Xunli
authors.initials: X
authors.lastname: Lu
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne D-50829, Germany.
authors.forename: Barbara
authors.initials: B
authors.lastname: Kracher
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne D-50829, Germany.
authors.forename: Isabel M L
authors.initials: IM
authors.lastname: Saur
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne D-50829, Germany.
authors.forename: Saskia
authors.initials: S
authors.lastname: Bauer
authors.affiliation: Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Bentley, Perth, WA 6102, Australia.
authors.forename: Simon R
authors.initials: SR
authors.lastname: Ellwood
authors.affiliation: Corn Insects and Crop Genetics Research, Agricultural Research Service, US Department of Agriculture, Ames, IA 50011-1020; Department of Plant Pathology and Microbiology, Center for Plant Responses to Environmental Stresses, Iowa State University, Ames, IA 50011-1020.
authors.forename: Roger
authors.initials: R
authors.lastname: Wise
authors.affiliation: Faculty of Agriculture, Ehime University, Matsuyama, Ehime 790-8566, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Yaeno
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne D-50829, Germany; schlef@mpipz.mpg.de maekawa@mpipz.mpg.de.
authors.forename: Takaki
authors.initials: T
authors.lastname: Maekawa
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne D-50829, Germany; schlef@mpipz.mpg.de maekawa@mpipz.mpg.de.
authors.forename: Paul
authors.initials: P
authors.lastname: Schulze-Lefert
mesh_terms: D000483:Alleles; D017360:Arabidopsis / Q000235:genetics; D001203:Ascomycota / Q000235:genetics* / Q000276:immunology* / Q000472:pathogenicity; D001483:Base Sequence; D016923:Cell Death; D060467:Disease Resistance / Q000276:immunology; D020869:Gene Expression Profiling; D015966:Gene Expression Regulation, Fungal; D056726:Genetic Association Studies; D016681:Genome, Fungal; D005838:Genotype; D001467:Hordeum / Q000276:immunology* / Q000382:microbiology*; D054884:Host-Pathogen Interactions / Q000276:immunology; D010641:Phenotype; D059828:Plant Cells; D010935:Plant Diseases / Q000276:immunology* / Q000382:microbiology*; D018515:Plant Leaves / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics*; D030821:Plants, Genetically Modified; D020641:Polymorphism, Single Nucleotide; D011971:Receptors, Immunologic / Q000235:genetics; D059467:Transcriptome; D037521:Virulence Factors / Q000737:chemistry / Q000235:genetics
chemical_list: C433105:MLA1 protein, Hordeum vulgare; D010940:Plant Proteins; D011971:Receptors, Immunologic; D037521:Virulence Factors
keywords: R genes; association analysis; avirulence effectors; plant-microbe interactions; powdery mildew