Kämper, J. et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444, 97-101

Philipps University of Marburg, Marburg, Hesse, Germany
Nature (Impact Factor: 41.46). 12/2006; 444(7115):97-101. DOI: 10.1038/nature05248
Source: PubMed


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.

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    • "This identified 16 putative regions (Fig. 10; Table VI). In contrast to observations made for the plant pathogenic fungus U. maydis (Kämper et al., 2006), none of the putative physical clusters were predominantly composed of small secreted proteins. Instead, many of the clustered genes had functions (IPR) related to metabolic processes, and in particular secondary metabolism . "
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    • "Puccinia graminis f. sp. tritici features a remarkably large genome of 89 Mb, which is more than four times larger than the related genome of the basidiomycete smut fungus Ustilago maydis (Kämper et al., 2006). Innovation of gene content has been attributed to large sets of lineage-specific expanded gene families, which are thought to drive adaptation and pathogen-associated processes (Duplessis et al., 2011; Raffaele and Kamoun, 2012). "
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    ABSTRACT: Plant pathogens cause severe losses to crop plants and threaten global food production. One striking example is the wheat stem rust fungus, Puccinia graminis f. sp. tritici, which can rapidly evolve new virulent pathotypes in response to resistant host lines. Like several other filamentous fungal and oomycete plant pathogens, its genome features expanded gene families that have been implicated in host-pathogen interactions, possibly encoding effector proteins that interact directly with target host defense proteins. Previous efforts to understand virulence largely relied on the prediction of secreted, small and cysteine-rich proteins as candidate effectors and thus delivered an overwhelming number of candidates. Here, we implement an alternative analysis strategy that uses the signal of adaptive evolution as a line of evidence for effector function, combined with comparative information and expression data. We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families. In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving. One of our top candidates has recently been shown to induce genotype-specific hypersensitive cell death in wheat. This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification. Our system can be applied to a wide range of pathogens and will give insight into host-pathogen dynamics, ultimately leading to progress in strategies for disease control.
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    • "Repetitive sequences generally represent 3 to 20% of the sequenced genomes of fungi; in Pyrenophora tritici-repentis [30] and Setosphaeria turcica [29] 16% and 12.96%, respectively, of the sequenced genome correspond to repetitive sequences. However, some sequenced genomes such as that of Ustilago maydis have low repetitive sequence content, with only 1.1% [31]. In contrast, other fungal genomes with unusual sizes display a large number of repetitive sequences: 85% of the genome of Blumeria graminis, estimated at 174 Mb, is represented by repetitive sequences, the largest percentage found to this point in fungi [32]. "
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