Maize Tumors Caused by
            <i>Ustilago maydis</i>
            Require Organ-Specific Genes in Host and Pathogen

Skibbe, David S.; Doehlemann, Gunther; Fernandes, John; Walbot, Virginia

doi:10.1126/science.1185775

Cited by 192 publications

(194 citation statements)

References 18 publications

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“…The mutant strains lacking the mitochondrial carrier CIC1 or one of two gene members of the FG3_54 cluster (FGSG_ 10992 or FGSG_10995) also displayed reduced virulence on florets (Figure 6; see Supplemental Figure 17 online), while the mutant strains lacking the CWDEs (CbhC1 and Eng1) or another member of the FG3_54 SMB cluster NPS9 didn't reduce virulence on florets significantly. In line with organ specificity of virulence genes demonstrated in the Ustilago maydis-maize system (Skibbe et al, 2010), the three genes required for coleoptile infection but not for floret infection might represent virulence genes specific to coleoptile infection.…”

Section: Discussionmentioning

confidence: 99%

In Planta Stage-Specific Fungal Gene Profiling Elucidates the Molecular Strategies of Fusarium graminearum Growing inside Wheat Coleoptiles

et al. 2012

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The ascomycete Fusarium graminearum is a destructive fungal pathogen of wheat (Triticum aestivum). To better understand how this pathogen proliferates within the host plant, we tracked pathogen growth inside wheat coleoptiles and then examined pathogen gene expression inside wheat coleoptiles at 16, 40, and 64 h after inoculation (HAI) using laser capture microdissection and microarray analysis. We identified 344 genes that were preferentially expressed during invasive growth in planta. Gene expression profiles for 134 putative plant cell wall-degrading enzyme genes suggest that there was limited cell wall degradation at 16 HAI and extensive degradation at 64 HAI. Expression profiles for genes encoding reactive oxygen species (ROS)-related enzymes suggest that F. graminearum primarily scavenges extracellular ROS before a later burst of extracellular ROS is produced by F. graminearum enzymes. Expression patterns of genes involved in primary metabolic pathways suggest that F. graminearum relies on the glyoxylate cycle at an early stage of plant infection. A secondary metabolite biosynthesis gene cluster was specifically induced at 64 HAI and was required for virulence. Our results indicate that F. graminearum initiates infection of coleoptiles using covert penetration strategies and switches to overt cellular destruction of tissues at an advanced stage of infection.

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Section: Discussionmentioning

confidence: 99%

In Planta Stage-Specific Fungal Gene Profiling Elucidates the Molecular Strategies of Fusarium graminearum Growing inside Wheat Coleoptiles

et al. 2012

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“…Further support for the occurrence of tissue-specific infection strategies of phytopathological fungi is lent by the recent discovery that Ustilago maydis-induced tumor formation on different organs of the maize (Zea mays) plant is associated with organ-specific gene expression in maize (and U. maydis), including differences in transcript levels of defense genes (Skibbe et al, 2010). Rice root infection by M. oryzae must rely on adapted plant transcriptional reprogramming, allowing the Transcript accumulation fold change of infected relative to noninfected tissue at 2, 4, and 6 DAI for roots and 3 and 4 DAI for leaves.…”

Section: Discussionmentioning

confidence: 99%

Tissue-Adapted Invasion Strategies of the Rice Blast Fungus Magnaporthe oryzae

et al. 2010

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Magnaporthe oryzae causes rice blast, the most serious foliar fungal disease of cultivated rice (Oryza sativa). During hemibiotrophic leaf infection, the pathogen simultaneously combines biotrophic and necrotrophic growth. Here, we provide cytological and molecular evidence that, in contrast to leaf tissue infection, the fungus adopts a uniquely biotrophic infection strategy in roots for a prolonged period and spreads without causing a loss of host cell viability. Consistent with a biotrophic lifestyle, intracellularly growing hyphae of M. oryzae are surrounded by a plant-derived membrane. Global, temporal gene expression analysis used to monitor rice responses to progressive root infection revealed a rapid but transient induction of basal defense-related gene transcripts, indicating perception of the pathogen by the rice root. Early defense gene induction was followed by suppression at the onset of intracellular fungal growth, consistent with the biotrophic nature of root invasion. By contrast, during foliar infection, the vast majority of these transcripts continued to accumulate or increased in abundance. Furthermore, induction of necrotrophy-associated genes during early tissue penetration, previously observed in infected leaves, was not seen in roots. Collectively, our results not only report a global characterization of transcriptional root responses to a biotrophic fungal pathogen but also provide initial evidence for tissue-adapted fungal infection strategies.

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“…The establishment of the biotrophic interface during infection involves complex signaling between the pathogen and the host cells to suppress plant defense pathways or to guarantee the supply of nutrients provided by the host. The infection process requires precise timing and tight control of gene expression not only to ensure the correct temporal and spatial expression of various pathogenicity factors but also to adapt fungal development to the changing environment during disease progression (Skibbe et al, 2010). In the smut fungus Ustilago maydis, pathogenic and sexual development is tightly linked to cell cycle control .…”

Section: Introductionmentioning

confidence: 99%

TheUstilago maydisClp1 Protein Orchestrates Pheromone andb-Dependent Signaling Pathways to Coordinate the Cell Cycle and Pathogenic Development

et al. 2010

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Regulation of the cell cycle and morphogenetic switching during pathogenic and sexual development in Ustilago maydis is orchestrated by a concerted action of the a and b mating-type loci. Activation of either mating-type locus triggers the G2 cell cycle arrest that is a prerequisite for the formation of the infectious dikaryon; this cell cycle arrest is released only after penetration of the host plant. Here, we show that bW, one of the two homeodomain transcription factors encoded by the b mating-type locus, and the zinc-finger transcription factor Rbf1, a master regulator for pathogenic development, interact with Clp1 (clampless 1), a protein required for the distribution of nuclei during cell division of the dikaryon. In addition, we identify Cib1, a previously undiscovered bZIP transcription factor required for pathogenic development, as a Clp1-interacting protein. Clp1 interaction with bW blocks b-dependent functions, such as the b-dependent G2 cell cycle arrest and dimorphic switching. The interaction of Clp1 with Rbf1 results in the repression of the a-dependent pheromone pathway, conjugation tube formation, and the a-induced G2 cell cycle arrest. The concerted interaction of Clp1 with Rbf1 and bW coordinates a-and b-dependent cell cycle control and ensures cell cycle release and progression at the onset of biotrophic development.

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Maize Tumors Caused by Ustilago maydis Require Organ-Specific Genes in Host and Pathogen

Cited by 192 publications

References 18 publications

In Planta Stage-Specific Fungal Gene Profiling Elucidates the Molecular Strategies of Fusarium graminearum Growing inside Wheat Coleoptiles

In Planta Stage-Specific Fungal Gene Profiling Elucidates the Molecular Strategies of Fusarium graminearum Growing inside Wheat Coleoptiles

Tissue-Adapted Invasion Strategies of the Rice Blast Fungus Magnaporthe oryzae

TheUstilago maydisClp1 Protein Orchestrates Pheromone andb-Dependent Signaling Pathways to Coordinate the Cell Cycle and Pathogenic Development

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