Abstract
Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew fungi present an exceptional case because of their strict host dependency (termed obligate biotrophy) and the atypical size of their genomes (>100 Mb). This size expansion is largely due to the pervasiveness of transposable elements on 70% of the genome and is associated with the loss of multiple conserved ascomycete genes required for a free-living lifestyle. To date, little is known about the mechanisms that drove these changes, and information on ancestral powdery mildew genomes is lacking. We report genome analysis of the early-diverged and exclusively sexually reproducing powdery mildew fungus Parauncinula polyspora, which we performed on the basis of a natural leaf epiphytic metapopulation sample. In contrast to other sequenced species of this taxonomic group, the assembled P. polyspora draft genome is surprisingly small (<30 Mb), has a higher content of conserved ascomycete genes, and is sparsely equipped with transposons (<10%), despite the conserved absence of a common defense mechanism involved in constraining repetitive elements. We speculate that transposable element spread might have been limited by this pathogen's unique reproduction strategy and host features and further hypothesize that the loss of conserved ascomycete genes may promote the evolutionary isolation and host niche specialization of powdery mildew fungi. Limitations associated with this evolutionary trajectory might have been in part counteracted by the evolution of plastic, transposon-rich genomes and/or the expansion of gene families encoding secreted virulence proteins.IMPORTANCE Powdery mildew fungi are widespread and agronomically relevant phytopathogens causing major yield losses. Their genomes have disproportionately large numbers of mobile genetic elements, and they have experienced a significant loss of highly conserved fungal genes. In order to learn more about the evolutionary history of this fungal group, we explored the genome of an Asian oak tree pathogen, Parauncinula polyspora, a species that diverged early during evolution from the remaining powdery mildew fungi. We found that the P. polyspora draft genome is comparatively compact, has a low number of protein-coding genes, and, despite the absence of a dedicated genome defense system, lacks the massive proliferation of repetitive sequences. Based on these findings, we infer an evolutionary trajectory that shaped the genomes of powdery mildew fungi.
Highlights
IMPORTANCE Powdery mildew fungi are widespread and agronomically relevant phytopathogens causing major yield losses
Among the filtered contigs of the first population, we identified a scaffold of extremely deep coverage (2,384ϫ) that is identical to the deposited nucleotide sequence of the internal transcribed spacer (ITS) region for the P. polyspora specimen voucher MUMH4928
Since the fungus is a pathogen of a tree species (Quercus serrata) that is native to eastern Asia, its propagation in pure culture would represent a formidable task
Summary
IMPORTANCE Powdery mildew fungi are widespread and agronomically relevant phytopathogens causing major yield losses. Different laboratories have successfully managed to tackle technical challenges associated with the advanced genomic analysis of these pathogens: e.g., bottlenecks in extracting high-molecular-weight DNA [15] or in assembling complex repetitive genomes to the chromosome (arm) level [12, 16] Based on these methodological improvements, new information was provided on the population structure [13, 17], genome architecture [12, 13, 16, 18, 19], and evolution [20] of some of the species and their specialized forms The presented analysis of the P. polyspora genome gives unexpected insights into the evolutionary history of PM fungi and provides broad suggestions on how TE inflation can affect the genomes of fungal phytopathogens
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