Abstract
BackgroundPowdery mildews are biotrophic pathogenic fungi infecting a number of economically important plants. The grass powdery mildew, Blumeria graminis, has become a model organism to study host specialization of obligate biotrophic fungal pathogens. We resolved the large-scale genomic architecture of B. graminis forma specialis hordei (Bgh) to explore the potential influence of its genome organization on the co-evolutionary process with its host plant, barley (Hordeum vulgare).ResultsThe near-chromosome level assemblies of the Bgh reference isolate DH14 and one of the most diversified isolates, RACE1, enabled a comparative analysis of these haploid genomes, which are highly enriched with transposable elements (TEs). We found largely retained genome synteny and gene repertoires, yet detected copy number variation (CNV) of secretion signal peptide-containing protein-coding genes (SPs) and locally disrupted synteny blocks. Genes coding for sequence-related SPs are often locally clustered, but neither the SPs nor the TEs reside preferentially in genomic regions with unique features. Extended comparative analysis with different host-specific B. graminis formae speciales revealed the existence of a core suite of SPs, but also isolate-specific SP sets as well as congruence of SP CNV and phylogenetic relationship. We further detected evidence for a recent, lineage-specific expansion of TEs in the Bgh genome.ConclusionsThe characteristics of the Bgh genome (largely retained synteny, CNV of SP genes, recently proliferated TEs and a lack of significant compartmentalization) are consistent with a “one-speed” genome that differs in its architecture and (co-)evolutionary pattern from the “two-speed” genomes reported for several other filamentous phytopathogens.
Highlights
Powdery mildews are biotrophic pathogenic fungi infecting a number of economically important plants
Whilst a short-read-based genome is available for DH14 [11], enabling direct comparison with the newly established long read-based assembly, isolate RACE1 was chosen because of its exceptionally high coding sequence divergence compared to a collection of 15 other B. graminis forma specialis hordei (Bgh) isolates from different geographic origins, including DH14 [9]
Rather we found that the Secreted protein (SP) count follows the scaffold size (Additional file 9: Figure S8B), which is in line with the results of a χ2-test that did not detect a significant deviation between the SP frequency per scaffold and the underlying genome fraction per scaffold (p = 0.21)
Summary
Powdery mildews are biotrophic pathogenic fungi infecting a number of economically important plants. Powdery mildews (Ascomycota, Erysiphales) are ubiquitous fungal plant pathogens in temperate regions of the world [1] They thrive on the basis of an obligate biotrophic lifestyle, i.e., by retrieving nutrients from living plant cells for Frantzeskakis et al BMC Genomics (2018) 19:381 specialis (f.sp.) is capable of infecting the respective host plant species belonging to the grasses (Poaceae) family, including cereals [8]. These genomes harbor an abundance of candidate secreted effector protein (CSEP)-coding genes, which were deemed to be crucial for successful pathogenesis [12, 13] Isolatespecific variants of these powdery mildew CSEPs are recognized by matching intracellular immune receptors, encoded by barley or wheat R genes, which are present only in particular genotypes of these cereal hosts [9, 14, 15]. Comparative sequence analysis of multiple isolates of both barley and wheat powdery mildew pathogens, B. graminis f.sp. hordei (Bgh) and B. graminis f.sp. tritici (Bgt), revealed that at least their genomes are characterized by an ancient haplotype mosaic composed of isolatespecific DNA blocks, suggesting exceptionally rare outbreeding and dominant clonal reproduction of the haploid fungus in nature [12, 19]
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