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

Abstract

Ustilago maydis is an important fungal pathogen of maize, causing corn smut. It is well adapted to its host and proliferates in living plant tissue without inducing a defence response. The genome sequence of U. maydis has now been determined, the first for a biotrophic plant parasite. Several gene clusters that encode secreted proteins of unknown function were identified: genome-wide expression analysis shows that the clustered genes are upregulated during disease. Mutations in these gene clusters frequently affect virulence, ranging from complete loss of pathogenicity to hypervirulence. Ustilago maydis is a ubiquitous pathogen of maize and a well-established model organism for the study of plant–microbe interactions1. 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 development2. 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 factors3 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.