Article

Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea.

Institute of Biological Environmental and Rural Sciences, Aberystwyth University, Penglais Campus, Aberystwyth, UK.
The Plant Journal (Impact Factor: 6.82). 06/2009; 59(5):723-37. DOI: 10.1111/j.1365-313X.2009.03912.x
Source: PubMed

ABSTRACT The mechanisms by which biotrophic and hemi-biotrophic fungal pathogens simultaneously subdue plant defences and sequester host nutrients are poorly understood. Using metabolite fingerprinting, we show that Magnaporthe grisea, the causal agent of rice blast disease, dynamically re-programmes host metabolism during plant colonization. Identical patterns of metabolic change occurred during M. grisea infections in barley, rice and Brachypodium distachyon. Targeted metabolite profiling by GC-MS confirmed the modulation of a conserved set of metabolites. In pre-symptomatic tissues, malate and polyamines accumulated, rather than being utilized to generate defensive reactive oxygen species, and the levels of metabolites associated with amelioration of redox stress in various cellular compartments increased dramatically. The activity of NADP-malic enzyme and generation of reactive oxygen species were localized to pathogen penetration sites, and both appeared to be suppressed in compatible interactions. Early diversion of the shikimate pathway to produce quinate was observed, as well as accumulation of non-polymerized lignin precursors. These data are consistent with modulation of defensive phenylpropanoid metabolism by M. grisea and the inability of susceptible hosts to mount a hypersensitive reaction or produce lignified papillae (both involving reactive oxygen species) to restrict pathogen invasion. Rapid proliferation of M. grisea hyphae in plant tissue after 3 days was associated with accelerated nutrient acquisition and utilization by the pathogen. Conversion of photoassimilate into mannitol and glycerol for carbon sequestration and osmolyte production appear to drive hyphal growth. Taken together, our results suggest that fungal pathogens deploy a common metabolic re-programming strategy in diverse host species to suppress plant defence and colonize plant tissue.

Download full-text

Full-text

Available from: David P Enot, Jun 22, 2015
1 Follower
 · 
159 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Soybean germplasm exhibits various levels of resistance to Fusarium tucumaniae, the main causal agent of sudden death syndrome (SDS) of soybean in Argentina. In this study, two soybean genotypes, one susceptible (NA 4613) and one partially resistant (DM 4670) to SDS infection, were inoculated with F. tucumaniae. Disease symptoms were scored at 7, 10, 14, and 25 days post-inoculation (dpi). The greatest difference in the area under the disease progress curve (AUDPC) values among genotypes was observed at 25 dpi. In order to detect early metabolic markers that could potentially discriminate between susceptible and resistant genotypes, gas chromatography-mass spectrometry (GC-MS) analyses of root samples were performed. These analyses show higher levels of several amino acids and the polyamine cadaverine in the inoculated than in the uninoculated susceptible cultivar at 7 dpi. Principal component analysis (PCA) revealed that the metabolic profile of roots harvested at the earliest time points from the inoculated susceptible genotype was clearly differentiated from the rest of the samples. Furthermore, variables associated with the first principal component were mainly amino acids. Taken together, the results indicate that the pathogen induced the susceptible plant to accumulate amino acids in roots at early time points after infection, suggesting that GC-MS-based metabolomics could be used for the rapid characterization of cultivar response to SDS.
    Journal of Experimental Botany 10/2014; DOI:10.1093/jxb/eru432 · 5.79 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Many defense mechanisms contribute to the plant immune system against pathogen, involving the regulation of different processes of the primary and secondary metabolism. At the same time, pathogens have evolved mechanisms to hijack the plant defense in order to establish the infection and proliferate. Localization and timing of the host response is essential to understand defense mechanisms and resistance to pathogens (Rico et al. 2011). Imaging technics, such as fluorescence imaging and thermography, are a very valuable tool providing spatial and temporal information about a series of plant processes. In this study, bean plants challenged with two pathovars of Pseudomonas syringae have been investigated. P. syringae pv. phaseolicola 1448A and P. syringae pv. tomato DC3000 elicit a compatible and incompatible interaction in bean, respectively. Both types of host-pathogen interaction triggered different changes in the activity of photosynthesis and the secondary metabolism. We conclude that the combined analysis of leaf temperature, chlorophyll fluorescence and green fluorescence emitted by phenolics allows to discriminate compatible from incompatible P. syringae - P. vulgaris interactions in very early times of the infection, prior to the development of symptoms. These can constitute disease signatures that would allow an early identification of emerging plagues in crops.
    Physiologia Plantarum 05/2014; DOI:10.1111/ppl.12237 · 3.26 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Growth is a complex trait that adapts to the prevailing conditions by integrating many internal and external signals. Understanding the molecular origin of this variation remains a challenging issue. In this study, natural variation of shoot growth under mannitol-induced stress was analyzed by standard quantitative trait locus mapping methods in a RIL population derived from a cross between Col-0 and Cvi-0 Arabidopsis thaliana accessions. Cloning of a major QTL specific to mannitol condition lead to the identification of EGM1 and EGM2, a pair of tandem-duplicated genes encoding receptor-like kinases potentially involved in the signaling of mannitol-associated stress responses. Using different genetic approaches, we identified two non-synonymous mutations in EGM2[Cvi] allele shared by at least ten accessions from different origin, likely responsible for a specific tolerance to mannitol. We have shown that the enhanced shoot growth phenotype contributed by the Cvi-allele is not linked to generic osmotic properties but instead to some specific chemical structure of mannitol itself. This result raised the question of the function of such a gene in A. thaliana, a species which does not synthesize mannitol. Our findings suggest that the RLK encoded by EGM genes could be activated by mannitol produced by pathogens such as fungi and contribute to plant defense response whenever mannitol is present. This article is protected by copyright. All rights reserved.
    The Plant Journal 01/2014; DOI:10.1111/tpj.12454 · 6.82 Impact Factor