Nutrition acquisition strategies during fungal infection of plants

Divon, Hege H.; Fluhr, Robert

doi:10.1111/j.1574-6968.2006.00504.x

Cited by 205 publications

(176 citation statements)

References 75 publications

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“…At 170 to 240 HAI, abundant fungal growth became visible on the surface of the lesions, and some were sporulating ( Figure 1B). The sporulation stage is considered to be the end stage of an infection cycle (Divon and Fluhr, 2007).…”

Section: F Graminearum Hyphae Inside Coleoptiles At 16 40 and 64 Hmentioning

confidence: 99%

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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: F Graminearum Hyphae Inside Coleoptiles At 16 40 and 64 Hmentioning

confidence: 99%

“…We also don't know whether or when F. graminearum produces toxic secondary metabolites, other than DON, that compromise the host. Finally, pathogens must establish nutrient acquisition from the host (Divon and Fluhr, 2007), but we have few insights into the metabolic adjustments that allow F. graminearum to grow in planta.…”

Section: Introductionmentioning

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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“…Thus, pathogens have evolved distinct lifestyles, including biotrophy, hemibiotrophy, and necrotrophy, that allow them to succeed (Solomon et al, 2003;Divon and Fluhr, 2007). However, the molecular mechanisms underlying the central metabolic aspects of plant-pathogen interactions are poorly understood.…”

Section: Introductionmentioning

confidence: 99%

“…The competition for a N source between the pathogen and its host is a dynamic and complex process. Not only are pathogen infection and colonization affected by the N status but so are host N metabolism and translocation per se altered or manipulated during pathogen attack (Divon and Fluhr, 2007;Snoeijers et al, 2000). Therefore, understanding how plants trade off the essential nutrients for balancing basal defense with growth and development has recently attracted much attention (Berger et al, 2007;Spoel et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Amino Acid Homeostasis Modulates Salicylic Acid–Associated Redox Status and Defense Responses inArabidopsis

et al. 2010

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The tight association between nitrogen status and pathogenesis has been broadly documented in plant–pathogen interactions. However, the interface between primary metabolism and disease responses remains largely unclear. Here, we show that knockout of a single amino acid transporter, LYSINE HISTIDINE TRANSPORTER1 (LHT1), is sufficient for Arabidopsis thaliana plants to confer a broad spectrum of disease resistance in a salicylic acid–dependent manner. We found that redox fine-tuning in photosynthetic cells was causally linked to the lht1 mutant-associated phenotypes. Furthermore, the enhanced resistance in lht1 could be attributed to a specific deficiency of its main physiological substrate, Gln, and not to a general nitrogen deficiency. Thus, by enabling nitrogen metabolism to moderate the cellular redox status, a plant primary metabolite, Gln, plays a crucial role in plant disease resistance.

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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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Nutrition acquisition strategies during fungal infection of plants

Cited by 205 publications

References 75 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

Amino Acid Homeostasis Modulates Salicylic Acid–Associated Redox Status and Defense Responses inArabidopsis

A model ofUstilago maydisleaf tumor metabolism

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