A genome-based analysis of amino acid metabolism in the biotrophic plant pathogen Ustilago maydis

McCann, Michael P.; Snetselaar, Karen M.

doi:10.1016/j.fgb.2008.05.006

Cited by 26 publications

(17 citation statements)

References 133 publications

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“…Little is known about the regulatory mechanisms of NCR in basidiomycetes. It has been demonstrated that basidiomycetes possess genes coding for GATA factors homologous to Nit2/AreA but lack orthologs of the negative acting factors known from yeast and filamentous fungi (32,59,87).…”

Section: Discussionmentioning

confidence: 99%

“…Ustilago maydis has the genetic setup to synthesize every proteinogenic amino acid (59) and is capable of utilizing a plethora of nitrogen sources, e.g., inorganic N, such as nitrate and ammonium, as well as organic nitrogen sources, such as biogenic amino acids and nucleobases (34). We assessed the role of um10417 in nitrogen utilization by cultivating SG200, SG200-⌬um10417, and SG200-⌬N-um10417 sporidia in the presence of different inorganic and organic nitrogen sources.…”

Section: Ustilago Maydismentioning

confidence: 99%

“…Nevertheless, the underlying regulatory mechanisms have remained elusive. The genes coding for nitrate reductase (nar1), nitrite reductase (nir1), and a putative nitrate transporter (nrt) are located in one gene cluster in U. maydis (59), suggesting their coordinated regulation. Thus, the transcriptional response of nar1 and nrt in SG200 and Nit2-deficient SG200 was assessed in response to different nitrogen regimens by RNA blot analysis.…”

Section: Ustilago Maydismentioning

confidence: 99%

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The Ustilago maydis Nit2 Homolog Regulates Nitrogen Utilization and Is Required for Efficient Induction of Filamentous Growth

et al. 2012

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Nitrogen catabolite repression (NCR) is a regulatory strategy found in microorganisms that restricts the utilization of complex and unfavored nitrogen sources in the presence of favored nitrogen sources. In fungi, this concept has been best studied in yeasts and filamentous ascomycetes, where the GATA transcription factors Gln3p and Gat1p (in yeasts) and Nit2/AreA (in ascomycetes) constitute the main positive regulators of NCR. The reason why functional Nit2 homologs of some phytopathogenic fungi are required for full virulence in their hosts has remained elusive. We have identified the Nit2 homolog in the basidiomycetous phytopathogen Ustilago maydis and show that it is a major, but not the exclusive, positive regulator of nitrogen utilization. By transcriptome analysis of sporidia grown on artificial media devoid of favored nitrogen sources, we show that only a subset of nitrogen-responsive genes are regulated by Nit2, including the Gal4-like transcription factor Ton1 (a target of Nit2). Ustilagic acid biosynthesis is not under the control of Nit2, while nitrogen starvation-induced filamentous growth is largely dependent on functional Nit2. nit2 deletion mutants show the delayed initiation of filamentous growth on maize leaves and exhibit strongly compromised virulence, demonstrating that Nit2 is required to efficiently initiate the pathogenicity program of U. maydis.

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Section: Discussionmentioning

confidence: 99%

Section: Ustilago Maydismentioning

confidence: 99%

Section: Ustilago Maydismentioning

confidence: 99%

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The Ustilago maydis Nit2 Homolog Regulates Nitrogen Utilization and Is Required for Efficient Induction of Filamentous Growth

et al. 2012

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“…The importance of nitrogen availability in biotrophic associations is further corroborated by the observation that nitrogen fertilizers generally increase the susceptibility of plants to biotrophs, whereas they decrease the susceptibility of plants to necrotrophs (Snoeijers et al, 2000;Dordas, 2008;Ballini et al, 2013). Indeed, U. maydis is known to grow on various nitrogen sources and has the ability to generate all proteinogenic amino acids (Holliday, 1961;McCann and Snetselaar, 2008).…”

Section: Nitrogen Transportersmentioning

confidence: 98%

The Biotrophic Development of Ustilago maydis Studied by RNA-Seq Analysis

et al. 2018

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The corn smut fungus Ustilago maydis is a model organism for elucidating host colonization strategies of biotrophic fungi. Here we performed an in depth transcriptional profiling of the entire plant-associated development of U. maydis wild-type strains. In our analysis we focused on fungal metabolism, nutritional strategies, secreted effectors and regulatory networks. Secreted proteins were enriched in three distinct expression modules corresponding to stages on the plant surface, establishment of biotrophy and induction of tumors. These modules are likely the key determinants for U. maydis virulence. With respect to nutrient utilization, we observed that expression of several nutrient transporters was tied to these virulence modules rather than being controlled by nutrient availability. We show that oligopeptide transporters likely involved in nitrogen assimilation are important virulence factors. By measuring the intramodular connectivity of transcription factors, we identified the potential drivers for the virulence modules. While known components of the b-mating type cascade emerged as inducers for the plant surface and biotrophy module, we identified a set of yet uncharacterized transcription factors as likely responsible for expression of the tumor module. We demonstrate a crucial role for leaf tumor formation and effector gene expression for one of these transcription factors.

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“…11 This difference in crown galls and U. maydis induced tumors may relate to the different nitrogen acquisition strategies of the two pathogens: While A. tumefaciens synthesizes opines for its nitrogen supply, U. maydis most likely takes up amino acids provided in the phloem sap and by the host cells as a nitrogen source. Despite the fact that U. maydis possesses a complete set of genes to synthesize all proteinogenic AA de novo, 15 the increased activity of the TCA cycle and induced AA biosynthesis in U. maydis induced tumors could reflect an elevated rate of interconversion between the different AA in the host cells, which could represent the main route for U. Shown is the number of genes in the respective mapman BiNs 13 that are either induced, repressed or unchanged in maize tumor cells at 4.5 days post infection with U. maydis compared to uninfected control leaves.…”

Section: A Model Ofmentioning

confidence: 99%

A model ofUstilago maydisleaf tumor metabolism

Horst

Doehlemann

Wahl³

et al. 2010

Plant Signaling & Behavior

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Extensive progress has been made in the last years in unraveling molecular mechanisms of plant-pathogen interactions. Although the main research focus lies on defense and counter-defense mechanisms, some plant-pathogen interactions have been characterized on the physiological level. Only a few studies have focused on the nutrient acquisition strategies of phytopathogens. In a previous study, we analyzed how local infection of maize leaves by the tumorinducing fungus Ustilago maydis affects whole plant physiology and were able to show that carbon and nitrogen assimilates are rerouted to the tumor. While the sink strength of infected emerging young leaves increases with tumor development, systemic source leaves exhibit elevated export of assimilates and delayed senescence to compensate for the altered sink-source balance. Here we provide new experimental data on the metabolization of these assimilates in the tumor and propose a model on their utilization in the infected tissue.Biotrophic plant pathogens depend on living host tissue and need to be able to compete with host cells for the acquisition of nutrients.1 It was shown that by inducing tumors on maize (Zea mays) leaves, the biotrophic basidiomycete fungus Ustilago maydis establishes a strong sink organ for carbohydrates 2-4 and amino acids. 5 These assimilates are provided by systemic source leaves, which exhibit increased productivity and increased export rates compared to comparable leaves of non-infected maize plants. To address how assimilates are metabolized in tumors, we conducted maize transcriptomics at different time points post infection and performed additional physiological analyses on developed tumors that were inspired by the transcript profiling approach. In brief, phenylpropanoid-, AA-, cell wall biosynthesis and enzymes of the TCA cycle are transcriptionally induced in tumors, while sucrose biosynthesis is repressed.3 At the same time, tumor metabolism is characterized by reduced photosynthesis and an accumulation of soluble sugars, i.e., hexoses which are generated via cleavage of sucrose by cell wall and vacuolar invertases.2 In addition, a plasmamembrane-associated sucrose synthase (Sus1) 6 is six-fold induced in tumors. Thus, we propose that sucrose imported from systemic leaves into tumor tissue serves the following main functions in host and pathogen metabolism: (1) provision of building blocks for cell wall biosynthesis of the tumor cell, which is channeled by SUS1, (2) generation of hexoses in the tumor-cell vacuole to build up osmotic pressure for tumor cell-expansion (see Fig. 2) and (3) feeding of U. maydis, which will most likely proceed via the high affinity sucrose transporter SRT1 that can outcompete host sucrose transporters based on its low K M for sucrose and will enable the pathogen to retrieve most of the sucrose.

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A genome-based analysis of amino acid metabolism in the biotrophic plant pathogen Ustilago maydis

Cited by 26 publications

References 133 publications

The Ustilago maydis Nit2 Homolog Regulates Nitrogen Utilization and Is Required for Efficient Induction of Filamentous Growth

The Ustilago maydis Nit2 Homolog Regulates Nitrogen Utilization and Is Required for Efficient Induction of Filamentous Growth

The Biotrophic Development of Ustilago maydis Studied by RNA-Seq Analysis

A model ofUstilago maydisleaf tumor metabolism

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