Gene erosion and genome expansion in a group of highly host-specialized fungal phytopathogens

Abstract

Due to their comparatively small genome size and short generation time, fungi are exquisite model systems to study eukaryotic genome evolution. Powdery mildew (PM) fungi present an exceptional case where their strict host dependency (a lifestyle termed obligate biotrophy) is associated with some of the largest fungal genomes sequenced so far (>100 Mbp). This size expansion is largely due to the pervasiveness of transposable elements (TEs), which can cover more than 70% of these genomes, and is associated with the loss of multiple conserved ascomycete genes (CAGs) required for a free-living lifestyle. To date, little is known about the mechanisms that drove this expansion, and information on ancestral PM genomes is lacking. We report the genome analysis of the early-diverged PM species Parauncinula polyspora that in contrast to most other PMs reproduces exclusively sexually. The P. polyspora genome is surprisingly small (<30 Mb) and sparsely equipped with TEs (<10%), despite the conserved absence of a common defense mechanism (RIP) involved in constraining repetitive elements. The genome still harbors the majority of the CAGs that are absent in the genomes of the recently evolved PMs. We speculate that TE spread might have been limited by its unique reproduction strategy and host features and further hypothesize that the loss of CAGs may promote the evolutionary isolation and host niche specialization of PM fungi. Limitations associated with this evolutionary trajectory might have been in part counteracted by the evolution of plastic, TE-rich genomes and/or the expansion of gene families encoding secreted virulence proteins. Genome evolution | Plant pathogen | Fungal genomics | Transposable elements | Repeat-Induced Point MutationCorrespondence: panstruga@bio1.rwth-aachen.de

The emergence of the multi‐species NIP1 effector in Rhynchosporium was accompanied by high rates of gene duplications and losses

“…However, the consistent patterns among species, broad independence from assembly contiguity (N50) and sequencing depth suggest that Rhynchosporium genomes exhibit indeed substantial size differences. In other fungi, rapid evolution of genome size was found among closely related species and may be correlated with important changes in fungal lifestyles (Albertin and Marullo, ; Sipos et al, ; Frantzeskakis et al, ). Intra‐specific analyses of fungal genomes showed substantial genome size and gene content variation (Plissonneau et al, , ; Syme et al, ).…”