Genome Comparison of Barley and Maize Smut Fungi Reveals Targeted Loss of RNA Silencing Components and Species-Specific Presence of Transposable Elements

Abstract

Ustilago hordei is a biotrophic parasite of barley (Hordeum vulgare). After seedling infection, the fungus persists in the plant until head emergence when fungal spores develop and are released from sori formed at kernel positions. The 26.1-Mb U. hordei genome contains 7113 protein encoding genes with high synteny to the smaller genomes of the related, maizeinfecting smut fungi Ustilago maydis and Sporisorium reilianum but has a larger repeat content that affected genome evolution at important loci, including mating-type and effector loci. The U. hordei genome encodes components involved in RNA interference and heterochromatin formation, normally involved in genome defense, that are lacking in the U. maydis genome due to clean excision events. These excision events were possibly a result of former presence of repetitive DNA and of an efficient homologous recombination system in U. maydis. We found evidence of repeat-induced point mutations in the genome of U. hordei, indicating that smut fungi use different strategies to counteract the deleterious effects of repetitive DNA. The complement of U. hordei effector genes is comparable to the other two smuts but reveals differences in family expansion and clustering. The availability of the genome sequence will facilitate the identification of genes responsible for virulence and evolution of smut fungi on their respective hosts.

The Transition from a Phytopathogenic Smut Ancestor to an Anamorphic Biocontrol Agent Deciphered by Comparative Whole-Genome Analysis

“…Of the four, U. hordei seems to stand out with over 10% of TEs and repeats. We did not find evidence of a repeat-induced point mutation mechanism as in U. hordei, but, as in S. reilianum, too few available homologous repeats made a comparative analysis difficult to assess mutation rates (Laurie et al, 2012). In general, repeat content in genomes of fungi seems to vary widely and is much higher in the biotrophic rusts and mildews (Spanu, 2012).…”

“…The number of transposable elements and simple repeats found in the P. flocculosa genome is similar to that reported in U. maydis (Table 1; see Supplemental Tables 1 and 2 online). It is 3 times lower than in U. hordei, in which species-specific transposable element families seem to have expanded over time (Laurie et al, 2012). Repetitive elements do not cluster in specific areas of the genome but appear to be randomly scattered (data not shown).…”

“…Comparative genomics has been extensively exploited to unravel specific virulence determinants and their evolution among the phytopathogenic Ustilaginomycetes U. maydis, S. reilianum, and U. hordei (Kämper et al, 2006;Schirawski et al, 2010;Laurie et al, 2012). In this work, the genome release of the closely related fungus P. flocculosa constitutes a new step in the study of Ustilaginomycete fungi evolution and phytopathogenicity-associated traits.…”

“…These genes are missing from the U. maydis genome but are present in U. hordei and S. reilianum (Laurie et al, 2012).…”

“…These observations reinforced the relevance of using phylogenetically related species to improve our understanding into the evolution of pathogenic factors through comparative genomic approaches. Additionally, the recent genome annotation of Sporisorium reilianum (Schirawski et al, 2010) and Ustilago hordei (Laurie et al, 2012) has provided an opportunity to perform comparative analyses that highlight common and divergent features among these closely related pathogens. Of particular interest was the finding that all three fungi share many conserved effectors but also possess sets of species-specific effectors.…”