The host-parasite physiology of the maize smut fungus, Ustilago maydis II. Translocation of 14C-labelled assimilates in smutted maize plants

Billett, E. Ellen; Burnett, J. H.

doi:10.1016/0048-4059(78)90023-1

Cited by 32 publications

(17 citation statements)

References 21 publications

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“…Feeding experiments witb^C Oj have shown altered translocation patterns in beans infected with rust (Livne & Daly, 1966), maize infected witb smut (Billett & Burnett, 1978) and barley infected witb mildew (Edwards, 1971). Similar experiments witb pea infected witb mildew combined with furtber measurements of sucrose in tbe apoplast could give a clearer picture of any altered source-sink relations in this system.…”

Section: Resultsmentioning

confidence: 79%

Effect of powdery mildew infection on concentrations of apoplastic sugars in pea leaves

Aked

Hall

1993

New Phytologist

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SUMMARYIntercellular washing fluid (IWF) was extracted by centrifugation from healthy and mildew-infected pea leaves. The level of cytoplasmic contamination of the IWF was estimated to be 0-3 "o for healthy leaves and 0-7 % in mildew-infected leaves as assessed by the presence of malate dehydrogenase activity. The IWF was analyzed for sugars using gas liquid chromatography and the glucose oxidase assay. Changes in the concentrations of glucose, fructose and sucrose showed different trends over an infection time course. Glucose and sucrose concentrations fluctuated over the 7 d period following infection but almost always showed higher levels in infected tissues than in the controls. Fructose concentrations were low and showed a greater increase over 7 d in infected compared to healthy leaves. The pattern of efflux of sucrose from pre-loaded healthy and mildew-infected pea leaf discs suggests that the plasma membranes of cells from infected pea leaves might be more leaky than those of healthy pea leaves. The implications of apoplastic sugar levels for nutritional aspects of the plant-pathogen interaction are discussed.

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Section: Resultsmentioning

confidence: 79%

Effect of powdery mildew infection on concentrations of apoplastic sugars in pea leaves

Aked

Hall

1993

New Phytologist

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“…We also observed that nit2 (nitrogen catabolic enzyme regulatory protein) and snf1 (sucrose nonfermenting 1), the nitrogen and carbon catabolite de-repressors (Nadal et al, 2010;Horst et al, 2012), have increased transcript levels during tumor formation compared to early biotrophic growth (Supplemental Data Sets 3 and 4), indicating that carbon and nitrogen sources may be limiting. Previous studies indicated that tumor tissue is a strong sink tissue with an efficient supply of organic nutrients from systemic source leaves (Billet and Burnett, 1978;Doehlemann et al, 2008b;Horst et al, 2008;Horst et al, 2010). Metabolome profiling of U. maydis infected tissue revealed that free hexoses and amino acids are highly abundant in tumor tissue, and even reach the levels of juvenile sink tissue (Horst et al, 2010).…”

Section: General Changes In Fungal Metabolism Throughout the Infectiomentioning

confidence: 99%

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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“…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][3][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.…”

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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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The host-parasite physiology of the maize smut fungus, Ustilago maydis II. Translocation of 14C-labelled assimilates in smutted maize plants

Cited by 32 publications

References 21 publications

Effect of powdery mildew infection on concentrations of apoplastic sugars in pea leaves

Effect of powdery mildew infection on concentrations of apoplastic sugars in pea leaves

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

A model ofUstilago maydisleaf tumor metabolism

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