title: Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts.
abstract: Barley powdery mildew, Blumeria graminis f. sp. hordei (Bgh), is an obligate biotrophic ascomycete fungal pathogen that can grow and reproduce only on living cells of wild or domesticated barley (Hordeum sp.). Domestication and deployment of resistant barley cultivars by humans selected for amplification of Bgh isolates with different virulence combinations. We sequenced the genomes of two European Bgh isolates, A6 and K1, for comparative analysis with the reference genome of isolate DH14. This revealed a mosaic genome structure consisting of large isolate-specific DNA blocks with either high or low SNP densities. Some of the highly polymorphic blocks likely accumulated SNPs for over 10,000 years, well before the domestication of barley. These isolate-specific blocks of alternating monomorphic and polymorphic regions imply an exceptionally large standing genetic variation in the Bgh population and might be generated and maintained by rare outbreeding and frequent clonal reproduction. RNA-sequencing experiments with isolates A6 and K1 during four early stages of compatible and incompatible interactions on leaves of partially immunocompromised Arabidopsis mutants revealed a conserved Bgh transcriptional program during pathogenesis compared with the natural host barley despite ~200 million years of reproductive isolation of these hosts. Transcripts encoding candidate-secreted effector proteins are massively induced in successive waves. A specific decrease in candidate-secreted effector protein transcript abundance in the incompatible interaction follows extensive transcriptional reprogramming of the host transcriptome and coincides with the onset of localized host cell death, suggesting a host-inducible defense mechanism that targets fungal effector secretion or production.
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.
authors.forename: Stéphane
authors.initials: S
authors.lastname: Hacquard
authors.forename: Barbara
authors.initials: B
authors.lastname: Kracher
authors.forename: Takaki
authors.initials: T
authors.lastname: Maekawa
authors.forename: Saskia
authors.initials: S
authors.lastname: Vernaldi
authors.forename: Paul
authors.initials: P
authors.lastname: Schulze-Lefert
authors.forename: Emiel
authors.initials: E
authors.lastname: Ver Loren van Themaat
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000382:microbiology; D001203:Ascomycota / Q000235:genetics* / Q000472:pathogenicity / Q000502:physiology; D016000:Cluster Analysis; D004271:DNA, Fungal / Q000737:chemistry / Q000235:genetics; D015966:Gene Expression Regulation, Fungal; D016681:Genome, Fungal / Q000235:genetics*; D001467:Hordeum / Q000235:genetics / Q000382:microbiology; D058507:Host Specificity; D020411:Oligonucleotide Array Sequence Analysis; D018515:Plant Leaves / Q000235:genetics / Q000382:microbiology; D030821:Plants, Genetically Modified; D020641:Polymorphism, Single Nucleotide; D017422:Sequence Analysis, DNA; D013045:Species Specificity; D059467:Transcriptome / Q000235:genetics*; D014774:Virulence / Q000235:genetics
chemical_list: D004271:DNA, Fungal
keywords: comparative genomics; effector-triggered immunity; fungal genetics; obligate biotrophy; plant–microbe interactions