Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis

By J. Kämper, R. Kahmann, M. Bölker, Li‐Jun Ma, Thomas Brefort, B. Saville, F. Banuett, J. Kronstad, S. Gold, O. Müller and 70 more. Nature, 2006

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Ustilago maydis is a ubiquitous pathogen of maize and a well-established model organism for the study of plant–microbe interactions. This basidiomycete fungus does not use aggressive virulence strategies to kill its host. U. maydis belongs to the group of biotrophic parasites (the smuts) that depend on living tissue for proliferation and development. Here we report the genome sequence for a member of this economically important group of biotrophic fungi. The 20.5-million-base U. maydis genome assembly contains 6,902 predicted protein-encoding genes and lacks pathogenicity signatures found in the genomes of aggressive pathogenic fungi, for example a battery of cell-wall-degrading enzymes. However, we detected unexpected genomic features responsible for the pathogenicity of this organism. Specifically, we found 12 clusters of genes encoding small secreted proteins with unknown function. A significant fraction of these genes exists in small gene families. Expression analysis showed that most of the genes contained in these clusters are regulated together and induced in infected tissue. Deletion of individual clusters altered the virulence of U. maydis in five cases, ranging from a complete lack of symptoms to hypervirulence. Despite years of research into the mechanism of pathogenicity in U. maydis, no ‘true’ virulence factors had been previously identified. Thus, the discovery of the secreted protein gene clusters and the functional demonstration of their decisive role in the infection process illuminate previously unknown mechanisms of pathogenicity operating in biotrophic fungi. Genomic analysis is, similarly, likely to open up new avenues for the discovery of virulence determinants in other pathogens.

Subfields: Molecular Biology, Plant Science

View Paper: https://www.semanticscholar.org/paper/0c45686419a4463f2a896ba5f84b7696a65fefd1

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Citations in the corpus

Poplar and Pathogen Interactions: Insights from Populus Genome-Wide Analyses of Resistance and Defense Gene Families and Gene Expression Profiling (2009, background): “As an obligate biotroph, M. larici-populina is not easily cultured and studied in a laboratory setting, unlike other model leaf fungal pathogens such as M. grisea and Ustilago maydis (Dean et al., 2005; Kämper et al., 2006).”
Plant immunity: towards an integrated view of plant–pathogen interactions (2010, background): “Such generalized identification of fungal effector genes has been restricted by the lack of conserved motifs to aid genome interrogation, but genome analysis of several fungal pathogens predicts that they have complex and diversified secretome”
Obligate biotrophy features unraveled by the genomic analysis of rust fungi (2011, background): “The size of these proteomes is similar to the symbiotic basidiomycete Laccaria bicolor (14), but strikingly larger than the corn smut fungi Ustilago maydis and Sporisorium reilianum, two nonobligate pathogenic biotrophs that encode only approximately 6,500 proteins (15, 16).”
Influence of carbon and nitrogen concentration on itaconic acid production by the smut fungus Ustilago maydis (2014, background): “Ustilago maydis is best known for its pathogenicity toward maize (Zea mays), from which it derives its common name "corn smut" [18].”