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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    ABSTRACT: The “hemibiotrophic” fungus Zymoseptoria tritici causes Septoria tritici blotch disease of wheat (Triticum aestivum). Pathogen reproduction on wheat occurs without cell penetration, suggesting dynamic and intimate intercellular communication occurs between fungus and plant throughout the disease cycle. We used deep RNA sequencing and metabolomics to investigate the physiology of plant and pathogen throughout an asexual reproductive cycle of Z. tritici on wheat leaves. Over 3,000 pathogen genes, >7,000 wheat genes and >300 metabolites were differentially regulated. Intriguingly, individual fungal chromosomes contributed unequally to the overall gene expression changes. Early transcriptional down regulation of putative host defense genes was detected in inoculated leaves. There was little evidence for fungal nutrient acquisition from the plant throughout symptomless colonization by Z. tritici, which may instead be utilizing lipid and fatty acid stores for growth. However the fungus then subsequently manipulated specific plant carbohydrates, including fructan metabolites, during the switch to necrotrophic growth and reproduction. This switch coincided with increased expression of jasmonic acid (JA) biosynthesis genes and large scale activation of other plant “defense” responses. Fungal genes encoding putative secondary metabolite clusters and secreted effector proteins were identified with distinct infection phase-specific expression patterns, although functional analysis suggested many have overlapping / redundant functions in virulence. The pathogenic lifestyle of Z. tritici on wheat revealed through this study, involving initial defense suppression by a slow growing extracellular and nutritionally limited pathogen, followed by defense (hyper-) activation during reproduction, reveals a subtle modification on the conceptual definition of hemibiotrophic plant infection. http://www.plantphysiol.org/content/early/2015/01/16/pp.114.255927.full.pdf+html
    Plant physiology 01/2015; 167(3). DOI:10.1104/pp.114.255927 · 6.84 Impact Factor
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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.
    Frontiers in Plant Science 09/2014; 5:372. DOI:10.3389/fpls.2014.00372 · 3.95 Impact Factor
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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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    ABSTRACT: Background Cochliobolus heterostrophus is a dothideomycete that causes Southern Corn Leaf Blight disease. There are two races, race O and race T that differ by the absence (race O) and presence (race T) of ~ 1.2-Mb of DNA encoding genes responsible for the production of T-toxin, which makes race T much more virulent than race O. The presence of repetitive elements in fungal genomes is considered to be an important source of genetic variability between different species. Results A detailed analysis of class I and II TEs identified in the near complete genome sequence of race O was performed. In total in race O, 12 new families of transposons were identified. In silico evidence of recent activity was found for many of the transposons and analyses of expressed sequence tags (ESTs) demonstrated that these elements were actively transcribed. Various potentially active TEs were found near coding regions and may modify the expression and structure of these genes by acting as ectopic recombination sites. Transposons were found on scaffolds carrying polyketide synthase encoding genes, responsible for production of T-toxin in race T. Strong evidence of ectopic recombination was found, demonstrating that TEs can play an important role in the modulation of genome architecture of this species. The Repeat Induced Point mutation (RIP) silencing mechanism was shown to have high specificity in C. heterostrophus, acting only on transposons near coding regions. Conclusions New families of transposons were identified. In C. heterostrophus, the RIP silencing mechanism is efficient and selective. The co-localization of effector genes and TEs, therefore, exposes those genes to high rates of point mutations. This may accelerate the rate of evolution of these genes, providing a potential advantage for the host. Additionally, it was shown that ectopic recombination promoted by TEs appears to be the major event in the genome reorganization of this species and that a large number of elements are still potentially active. So, this study provides information about the potential impact of TEs on the evolution of C. heterostrophus. Electronic supplementary material The online version of this article (doi:10.1186/1471-2164-15-536) contains supplementary material, which is available to authorized users.
    BMC Genomics 06/2014; 15(1):536. DOI:10.1186/1471-2164-15-536 · 3.99 Impact Factor
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