An Integrated View of Gene Expression and Solute Profiles of <i>Arabidopsis</i> Tumors: A Genome-Wide Approach

Deeken, Rosalia; Engelmann, Julia C.; Efetova, Marina; Czirjak, Tina; Müller, Tobias; Kaiser, Werner M.; Tietz, Olaf; Krischke, Markus; Mueller, Martin J.; Palme, Klaus; Dandekar, Thomas; Hedrich, Rainer

doi:10.1105/tpc.106.044743

Cited by 102 publications

(176 citation statements)

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“…When reevaluating a transcriptome profiling approach of Agrobacterium tumefaciens infected Arabidopsis stems, 11 cytosolic protein biosynthesis was overrepresented among the upregulated genes in fully developed crown galls (Fischer test χ 2 = 4.7), while genes of plastidic protein biosynthesis were also overrepresented among the downregulated genes (Fischer test χ 2 = 3.7). While reduced plastidic protein biosynthesis reflects the reduction of photosynthetic rates in tumors and galls 2,11 increased cytosolic protein biosynthesis could reflect the induction of host PR protein biosynthesis.…”

Section: A Model Ofmentioning

confidence: 99%

“…12 Although amino acids accumulated in A. tumefaciens induced galls as well, only few genes involved in the TCA cycle or in amino acid biosynthesis were transcriptionally regulated. 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.…”

Section: A Model Ofmentioning

confidence: 99%

“…While reduced plastidic protein biosynthesis reflects the reduction of photosynthetic rates in tumors and galls 2,11 increased cytosolic protein biosynthesis could reflect the induction of host PR protein biosynthesis. Even in the compatible interaction between U. maydis and maize, the pathogen induces a defense reaction, including the strong transcriptional induction of pathogenesis related (PR) genes 3 and it has been shown that ribosomes produce large amounts of PR proteins during pathogen attack.…”

Section: A Model Ofmentioning

confidence: 99%

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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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Section: A Model Ofmentioning

confidence: 99%

Section: A Model Ofmentioning

confidence: 99%

Section: A Model Ofmentioning

confidence: 99%

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A model ofUstilago maydisleaf tumor metabolism

Horst

Doehlemann

Wahl³

et al. 2010

Plant Signaling & Behavior

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“…Raw signal intensity values were computed from the scanned array images using the Affymetrix GeneChip Command Console 3.0. Statistical gene expression analysis was performed analogously to the analysis described by Deeken et al (2006). Data from gene expression microarrays were analyzed using the statistical software R (R Development Core Team; www.R-project.org) and add-on packages for microarray analysis from Bioconductor (Gentleman et al, 2004).…”

Section: Microarray Analysis Data Preprocessing and Differential Gementioning

confidence: 99%

“…Microarray hybridizations, data acquisition, and bioinformatics analysis of the microarray experiments were performed as described (Deeken et al, 2006;Duy et al, 2007) with adaptations (see "Materials and Methods"). For each time-point, T 0 (low-light challenge: time = 0 h, just before transfer to low light), T 6 (6 h), T 24 (24 h), and T 48 (48 h), the fold changes and adjusted P values for genes differentially expressed were calculated from three replicate saul1 mutant samples versus three replicate wild-type samples.…”

Section: Regulatory Events In Saul1 Seedlings Precede the Occurrence mentioning

confidence: 99%

Early Senescence and Cell Death in Arabidopsis saul1 Mutants Involves the PAD4-Dependent Salicylic Acid Pathway

Vogelmann

Drechsel²,

Bergler³

et al. 2012

Plant Physiology

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Age-dependent leaf senescence and cell death in Arabidopsis (Arabidopsis thaliana) requires activation of the transcription factor ORESARA1 (ORE1) and is not initiated prior to a leaf age of 28 d. Here, we investigate the conditional execution of events that regulate early senescence and cell death in senescence-associated ubiquitin ligase1 (saul1) mutants, deficient in the PLANT U-BOX-ARMADILLO E3 ubiquitin ligase SAUL1. In saul1 mutants challenged with low light, the switch of age-dependent cell death was turned on prematurely, as indicated by the accumulation of ORE1 transcripts, induction of the senescence marker gene SENESCENCE-ASSOCIATED GENE12, and cell death. However, ORE1 accumulation by itself was not sufficient to cause saul1 phenotypes, as demonstrated by double mutant analysis. Exposure of saul1 mutants to low light for only 24 h did not result in visible symptoms of senescence; however, the senescence-promoting transcription factor genes WRKY53, WRKY6, and NAC-LIKE ACTIVATED BY AP3/PI were up-regulated, indicating that senescence in saul1 seedlings was already initiated. To resolve the time course of gene expression, microarray experiments were performed at narrow intervals. Differential expression of the genes involved in salicylic acid and defense mechanisms were the earliest events detected, suggesting a central role for salicylic acid in saul1 senescence and cell death. The salicylic acid content increased in low-light-treated saul1 mutants, and application of exogenous salicylic acid was indeed sufficient to trigger saul1 senescence in permissive light conditions. Double mutant analyses showed that PHYTOALEXIN DEFICIENT4 (PAD4) but not NONEXPRESSER OF PR GENES1 (NPR1) is essential for saul1 phenotypes. Our results indicate that saul1 senescence depends on the PAD4-dependent salicylic acid pathway but does not require NPR1 signaling.

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