A chromosome-level genome assembly of Thecaphora frezzii, cause of peanut smut, reveals the largest genome of the true smut fungi.

Peanut smut, caused by the fungus Thecaphora frezzii, is a significant disease of peanuts in Argentina. Infected plants have seeds replaced by a mass of dark teliospores, reducing yield and seed quality. Following successful in vitro culture of the fungus in its haploid stage, we produced a chromosome-level genome assembly of the species. We compare this genome to those of 49 other species of true smut fungi, or Ustilaginomycetes, including species of medical, agricultural, and industrial importance, some of which are known as pathogens and others only as saprotrophic yeasts. At almost 39 Mb, T. frezzii has the largest genome of the smut fungi sequenced to date with the most repetitive content. While sharing some core effectors with well-studied Ustilago species and their close allies, T. frezzii possesses a large proportion of predicted effectors unique to the species or genus, suggesting a unique infection strategy. Comparisons among the 50 smut genomes also show that the 14 smut species observed only as yeasts have generally smaller genomes with low repeat content, supporting the hypothesis that some smut fungi are adapted to saprotrophic growth as yeasts. This high quality, annotated genome for T. frezzii will be a valuable resource for investigating the population dynamics and evolution of an economically important pathogen and for illuminating an understudied clade of smut fungi.