Host-Selective Toxins of Pyrenophora tritici-repentis Induce Common Responses Associated with Host Susceptibility

Pyrenophora tritici-repentis (Ptr), a necrotrophic fungus and the causal agent of tan spot of wheat, produces one or a combination of host-selective toxins (HSTs) necessary for disease development. The two most studied toxins produced by Ptr, Ptr ToxA (ToxA) and Ptr ToxB (ToxB), are proteins that cause necrotic or chlorotic symptoms respectively. Investigation of host responses induced by HSTs provides better insight into the nature of the host susceptibility. Microarray analysis of ToxA has provided evidence that it can elicit responses similar to those associated with defense. In order to evaluate whether there are consistent host responses associated with susceptibility, a similar analysis of ToxB-induced changes in the same sensitive cultivar was conducted. Comparative analysis of ToxA- and ToxB-induced transcriptional changes showed that similar groups of genes encoding WRKY transcription factors, RLKs, PRs, components of the phenylpropanoid and jasmonic acid pathways are activated. ROS accumulation and photosystem dysfunction proved to be common mechanism-of-action for these toxins. Despite similarities in defense responses, transcriptional and biochemical responses as well as symptom development occur more rapidly for ToxA compared to ToxB, which could be explained by differences in perception as well as by differences in activation of a specific process, for example, ethylene biosynthesis in ToxA treatment. Results of this study suggest that perception of HSTs will result in activation of defense responses as part of a susceptible interaction and further supports the hypothesis that necrotrophic fungi exploit defense responses in order to induce cell death.

• Publication year

  2012

• Venue

  PLoS ONE

• Publication date

  2012-07-06

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1371/journal.pone.0040240PMID 22792250PMCID 3391247
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat.

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  2011cited by this paper
• Reactive oxygen species during plant-microorganism early interactions.

  2010cited by this paper
• Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction.

  2010cited by this paper
• The ubiquitin-proteasome system regulates plant hormone signaling.

  2010cited by this paper
• Inhibition of photosynthesis and modification of the wheat leaf proteome by Ptr ToxB: A host‐specific toxin from the fungal pathogen Pyrenophora tritici‐repentis

  2010influential reference
• Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum

  2010cited by this paper
• Minireview/ Minisynthèse The wheat/Pyrenophora tritici-repentis interaction: progress towards an understanding of tan spot disease

  2010cited by this paper
• Biotic stress globally downregulates photosynthesis genes.

  2010cited by this paper
• NB-LRR proteins: pairs, pieces, perception, partners, and pathways.

  2010cited by this paper
• A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens

  2010cited by this paper
• Estimating disease losses to the Australian wheat industry

  2009cited by this paper
• Hormone (Dis)harmony Moulds Plant Health and Disease

  2009cited by this paper
• Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence

  2009cited by this paper
• Evolutionary History and Stress Regulation of Plant Receptor-Like Kinase/Pelle Genes

  2009cited by this paper
• A host-selective toxin of Pyrenophora tritici-repentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat.

  2009cited by this paper
• Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis.

  2009cited by this paper
• Evolutionary History and Stress Regulation of Plant Receptor-Like Kinase/Pelle Genes1[W][OA]

  2009cited by this paper
• Analysis of transcriptome changes induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility.

  2009cited by this paper
• Phenotypic analysis of Arabidopsis mutants: trypan blue stain for fungi, oomycetes, and dead plant cells.

  2008cited by this paper
• GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis

  2008cited by this paper
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  2008cited by this paper
• Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster.

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• Unraveling the Tapestry of Networks Involving Reactive Oxygen Species in Plants

  2008cited by this paper
• Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death.

  2008cited by this paper
• Phytopathogen type III effector weaponry and their plant targets.

  2008cited by this paper
• The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization.

  2008cited by this paper
• BMC Bioinformatics BioMed Central

  2008cited by this paper
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  2007cited by this paper
• Characterization of the Interaction of a Novel Stagonospora nodorum Host-Selective Toxin with a Wheat Susceptibility Gene1[W]

  2007cited by this paper
• Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade.

  2007cited by this paper
• A Combination of Phenotypic and Genotypic Characterization Strengthens Pyrenophora tritici-repentis Race Identification.

  2007cited by this paper
• Transcriptome analysis of trichothecene-induced gene expression in barley.

  2007cited by this paper
• Plant disease susceptibility conferred by a “resistance” gene

  2007influential reference
• Reactive Oxygen Species Signaling in Response to Pathogens1

  2006cited by this paper
• affylmGUI: a graphical user interface for linear modeling of single channel microarray data

  2006cited by this paper
• Saccharin-induced protection against powdery mildew in barley: effects on growth and phenylpropanoid metabolism

  2006cited by this paper
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  2005cited by this paper
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  2005cited by this paper
• Structure of Ptr ToxA: An RGD-Containing Host-Selective Toxin from Pyrenophora tritici-repentisw⃞

  2005cited by this paper
• Forensic pathology of canadian bread wheat: the case of tan spot.

  2005cited by this paper
• A practical false discovery rate approach to identifying patterns of differential expression in microarray data

  2005influential reference
• Characterization of the ToxB gene from North African and Canadian isolates of Pyrenophora tritici-repentis

  2005cited by this paper
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  2005cited by this paper
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  2005influential reference
• Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat

  2004cited by this paper
• GOstat: find statistically overrepresented Gene Ontologies within a group of genes.

  2004cited by this paper
• Ptr ToxA requires multiple motifs for complete activity.

  2004cited by this paper
• Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments

  2004cited by this paper
• Characterization of the multiple-copy host-selective toxin gene, ToxB, in pathogenic and nonpathogenic isolates of Pyrenophora tritici-repentis.

  2004cited by this paper
• An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants

  2004cited by this paper
• Host–parasite interactions in tan spot [Pyrenophora tritici-repentis] of wheat

  2003cited by this paper
• The Identification of Two New Races of Pyrenophora tritici-repentis from the Host Center of Diversity Confirms a One-to-One Relationship in Tan Spot of Wheat.

  2003cited by this paper
• The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes.

  2003cited by this paper
• Tan spot of wheat (Triticum aestivum L.) infection at different stages of crop development and inoculum type

  2003cited by this paper
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  2002cited by this paper
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  2002cited by this paper
• Host-selective toxins and avirulence determinants: what's in a name?

  2002cited by this paper
• Ethylene Biosynthesis and Signaling Networks Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001768.

  2002cited by this paper
• Nonphytotoxic Aluminum-Peat Complexes Suppress Phytophthora parasitica.

  2001cited by this paper
• Characterization of the ToxB gene from Pyrenophora tritici-repentis.

  2001cited by this paper
• In silico prediction of protein-protein interactions in human macrophages

  2001influential reference
• The complexity of disease signaling in Arabidopsis.

  2001cited by this paper
• Plant cell walls: wall-associated kinases and cell expansion.

  2001cited by this paper
• Heterologous expression of functional Ptr ToxA.

  2000cited by this paper
• The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea.

  2000cited by this paper
• Characterization of a Host-Specific Protein Toxin (Ptr ToxB) from Pyrenophora tritici-repentis

  1999cited by this paper
• Genetic Analysis of Sensitivity to a Pyrenophora tritici-repentis Necrosis-Inducing Toxin in Durum and Common Wheat.

  1999cited by this paper
• Polygalacturonase and polygalacturonase inhibitor protein: gene isolation and transcription in Glycine max-Heterodera glycines interactions.

  1999cited by this paper
• Phenylpropanoid biosynthesis and its regulation.

  1998cited by this paper
• Isolation and Mode of Action of Ptr Chlorosis Toxin From Pyrenophora Tritici-Repentis

  1998cited by this paper
• Activity of Ptr ToxA fromPyrenophora tritici-repentisrequires host metabolism

  1998cited by this paper
• Polygalacturonases: many genes in search of a function.

  1998cited by this paper
• INHERITANCE OF RACE-SPECIFIC NECROTIC AND CHLOROTIC REACTIONS INDUCED BY PYRENOPHORA TRITICI-REPENTIS IN HEXAPLOID WHEATS

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• Induced chlorophyll degradation by a chlorosis toxin from Pyrenophora tritici-repentis

  1998cited by this paper
• Standardization of toxin nomenclature in the Pyrenophora tritici-repentis/wheat interaction

  1998cited by this paper
• Vistas of tan spot research

  1998cited by this paper
• Molecular Genetics of Host-Specific Toxins in Plant Disease

  1998cited by this paper
• The jasmonate pathway is involved differentially in the regulation of different defence responses in tobacco cells

  1997cited by this paper
• Structural and Physical Properties of a Necrosis-Inducing Toxin from Pyrenophora tritici-repentis.

  1997cited by this paper
• A single gene encodes a selective toxin causal to the development of tan spot of wheat.

  1997cited by this paper
• Host-selective toxins: agents of compatibility.

  1996cited by this paper
• Chromosomal location of a gene conditioning insensitivity in wheat to a necrosis-inducing culture filtrate from Pyrenophora tritici-repentis

  1996cited by this paper
• Cloning, expression and occurrence of the gene encoding the Ptr necrosis toxin from Pyrenophora tritici-repentis.

  1996cited by this paper
• A gene for resistance to a necrosis-inducing isolate of Pyrenophora tritici-repentis located on 5BL of Triticum aestivum cv. Chinese Spring.

  1996cited by this paper
• Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis.

  1995cited by this paper
• Stress-Induced Phenylpropanoid Metabolism.

  1995cited by this paper
• Identification of a new race in Pyrenophora tritici-repentis: implications for the current pathotype classification system

  1995cited by this paper
• Evidence of a host-specific chlorosis toxin from Pyrenophora tritici-repentis, the causal agent of tan spot of wheat.

  1995cited by this paper
• JIPs and RIPs: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens.

  1994cited by this paper
• JIP60, a methyl jasmonate-induced ribosome-inactivating protein involved in plant stress reactions.

  1994cited by this paper
• Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid.

  1993cited by this paper
• A methyl jasmonate‐induced shift in the length of the 5′ untranslated region impairs translation of the plastid rbcL transcript in barley.

  1993cited by this paper
• Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures.

  1992cited by this paper
• Compendium of Wheat Diseases

  1991cited by this paper
• Genetics of tan necrosis and extensive chlorosis in tan spot of wheat caused by Pyrenophora tritici-repentis.

  1991cited by this paper
• Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat.

  1990cited by this paper
• Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis

  1989cited by this paper
• Resistance to powdery mildew in wheat: a review of its use in agriculture and breeding programmes

  1984cited by this paper

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