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Peter S. Solomon - One of the best experts on this subject based on the ideXlab platform.
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PR1-mediated defence via C-terminal peptide release is targeted by a fungal pathogen effector.
The New phytologist, 2020Co-Authors: Yi-chang Sung, Susan Breen, Chen Wang, Megan A. Outram, Bayantes Dagvadorj, Bostjan Kobe, Simon J. Williams, Britta Winterberg, Peter S. SolomonAbstract:The effector SnTox3 from Parastagonospora nodorum elicits a strong necrotic response in susceptible wheat and also interacts with wheat pathogenesis-related protein 1 (TaPR-1), although the function of this interaction in disease is unclear. Here, we dissect TaPR1 function by studying SnTox3-TaPR1 interaction and demonstrate the dual functionality of SnTox3. We utilized site-directed mutagenesis to identify an SnTox3 variant, SnTox3P173S , that was unable to interact with TaPR1 in yeast-two-hybrid assays. Additionally, using recombinant proteins we established a novel protein-mediated phenotyping assay allowing functional studies to be undertaken in wheat. Wheat leaves infiltrated with TaPR1 proteins showed significantly less disease compared to control leaves, correlating with a strong increase in defence gene expression. This activity was dependent on release of the TaCAPE1 peptide embedded within TaPR1 by an unidentified serine protease. The priming activity of TaPR1 was compromised by SnTox3 but not the noninteracting variant SnTox3P173S , and we demonstrate that SnTox3 prevents TaCAPE1 release from TaPR1 in vitro. SnTox3 independently functions to induce necrosis through recognition by Snn3 and also suppresses host defence through a direct interaction with TaPR1 proteins. Importantly, this study also advances our understanding of the role of PR1 proteins in host-microbe interactions as inducers of host defence signalling.
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The crystal structure of SnTox3 from the necrotrophic fungus Parastagonospora nodorum reveals a unique effector fold and insights into Kex2 protease processing of fungal effectors
2020Co-Authors: Megan A. Outram, Peter S. Solomon, Yi-chang Sung, Bayantes Dagvadorj, Sharmin A. Rima, David A. Jones, Daniel J. Ericsson, Jana Sperschneider, Bostjan KobeAbstract:Plant pathogens cause disease through secreted effector proteins, which act to modulate host physiology and promote infection. Typically, the sequences of effectors provide little functional information and further targeted experimentation is required. Here, we utilised a structure/function approach to study SnTox3, an effector from the necrotrophic fungal pathogen Parastagonospora nodorum, which causes cell death in wheat-lines carrying the sensitivity gene Snn3. We developed a workflow for the production of SnTox3 in a heterologous host that enabled crystal structure determination. We show this approach can be successfully applied to effectors from other pathogenic fungi. Complementing this, an in-silico study uncovered the prevalence of an expanded subclass of effectors from fungi. The β-barrel fold of SnTox3 is a novel fold among fungal effectors. We demonstrate that SnTox3 is a pre-pro-protein and that the protease Kex2 removes the pro-domain. Our in-silico studies suggest that Kex2-processed pro-domain (designated here as K2PP) effectors are common in fungi, and we demonstrate this experimentally for effectors from Fusarium oxysporum f sp. lycopersici. We propose that K2PP effectors are highly prevalent among fungal effectors. The identification and classification of K2PP effectors has broad implications for the approaches used to study their function in fungal virulence.
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Assessing the efficacy of CRISPR/Cas9 genome editing in the wheat pathogen Parastagonspora nodorum
Fungal Biology and Biotechnology, 2020Co-Authors: Haseena Khan, Megan C. Mcdonald, Simon J. Williams, Peter S. SolomonAbstract:Background The genome-editing tool CRISPR/Cas9 has revolutionized gene manipulation by providing an efficient method to generate targeted mutations. This technique deploys the Cas9 endonuclease and a guide RNA (sgRNA) which interact to form a Cas9-sgRNA complex that initiates gene editing through the introduction of double stranded DNA breaks. We tested the efficacy of the CRISPR/Cas9 approach as a means of facilitating a variety of reverse genetic approaches in the wheat pathogenic fungus Parastagonospora nodorum . Results Parastagonospora nodorum protoplasts were transformed with the Cas9 protein and sgRNA in the form of a preassembled ribonuclear protein (RNP) complex targeting the Tox3 effector gene. Subsequent screening of the P. nodorum transformants revealed 100% editing of those mutants screened. We further tested the efficacy of RNP complex when co-transformed with a Tox3 -Homology Directed Repair cassette harbouring 1 kb of homologous flanking DNA. Subsequent screening of resulting transformants demonstrated homologous recombination efficiencies exceeding 70%. A further transformation with a Tox3 -Homology Directed Repair cassette harbouring a selectable marker with 50 bp micro-homology flanks was also achieved with 25% homologous recombination efficiency. The success of these homology directed repair approaches demonstrate that CRISPR/Cas9 is amenable to other in vivo DNA manipulation approaches such as the insertion of DNA and generating point mutations. Conclusion These data highlight the significant potential that CRISPR/Cas9 has in expediting transgene-free gene knockouts in Parastagonospora nodorum and also in facilitating other gene manipulation approaches. Access to these tools will significantly decrease the time required to assess the requirement of gene for disease and to undertake functional studies to determine its role.
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Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity.
Frontiers in microbiology, 2020Co-Authors: Mariano Jordi Muria-gonzalez, Yit-heng Chooi, Russell A. Barrow, Oliver Mead, Hui-yeng Y. Yap, Susan Breen, Chen Wang, Peter S. SolomonAbstract:Septoria nodorum blotch is a major disease of wheat caused by the fungus Parastagonospora nodorum. Recent studies have demonstrated that secondary metabolites, including polyketides and non-ribosomal peptides, produced by the pathogen play important roles in disease and development. However, there is currently no knowledge on the composition or biological activity of the volatile organic compounds (VOCs) secreted by P. nodorum. To address this, we undertook a series of growth and phytotoxicity assays and demonstrated that P. nodorum VOCs inhibited bacterial growth, were phytotoxic and suppressed self-growth. Mass spectrometry analysis revealed that 3-methyl-1-butanol, 2-methyl-1-butanol, 2-methyl-1-propanol, and 2-phenylethanol were dominant in the VOC mixture and phenotypic assays using these short chain alcohols confirmed that they were phytotoxic. Further analysis of the VOCs also identified the presence of multiple sesquiterpenes of which four were identified via mass spectrometry and nuclear magnetic resonance as β-elemene, α-cyperone, eudesma-4,11-diene and acora-4,9-diene. Subsequent reverse genetics studies were able to link these molecules to corresponding sesquiterpene synthases in the P. nodorum genome. However, despite extensive testing, these molecules were not involved in either of the growth inhibition or phytotoxicity phenotypes previously observed. Plant assays using mutants of the pathogen lacking the synthetic genes revealed that the identified sesquiterpenes were not required for disease formation on wheat leaves. Collectively, these data have significantly extended our knowledge of the VOCs in fungi and provided the basis for further dissecting the roles of sesquiterpenes in plant disease.
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genomics driven discovery of phytotoxic cytochalasans involved in the virulence of the wheat pathogen Parastagonospora nodorum
ACS Chemical Biology, 2020Co-Authors: Haochen Wei, Peter S. Solomon, Ernest Lacey, Keith A. Stubbs, Alexandre N. Sobolev, Yit-heng ChooiAbstract:The etiology of fungal pathogenesis of grains is critical to global food security. The large number of orphan biosynthetic gene clusters uncovered in fungal plant pathogen genome sequencing project...
Timothy L Friesen - One of the best experts on this subject based on the ideXlab platform.
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A protein kinase-major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat.
The Plant journal : for cell and molecular biology, 2021Co-Authors: Zengcui Zhang, Timothy L Friesen, Robert Brueggeman, Gongjun Shi, Katherine L D Running, Sudeshi Seneviratne, Amanda R Peters Haugrud, Agnes Szabo-hever, Justin D. FarisAbstract:Septoria nodorum blotch (SNB), a disease caused by the necrotrophic fungal pathogen Parastagonospora nodorum, is a threat to wheat production worldwide. Multiple inverse gene-for-gene interactions involving the recognition of necrotrophic effectors (NEs) by wheat sensitivity genes play major roles in causing SNB. One interaction involves the wheat gene Snn3 and the P. nodorum NE SnTox3. Here, we used a map-based strategy to clone the Snn3-D1 gene from Aegilops tauschii, the D-genome progenitor of common wheat. Snn3-D1 contained protein kinase and major sperm protein domains, both of which were essential for function as confirmed by mutagenesis. As opposed to other characterized interactions in this pathosystem, a compatible Snn3-D1-SnTox3 interaction was light independent, and Snn3-D1 transcriptional expression was down-regulated by light and up-regulated by darkness. Snn3-D1 likely emerged in Ae. tauschii due to a ~218 kb insertion that occurred along the west bank of the Caspian Sea. The identification of this new class of NE sensitivity gene combined with the previously cloned sensitivity genes demonstrates that P. nodorum can take advantage of diverse host targets to trigger SNB susceptibility in wheat.
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Parastagonospora nodorum and Related Species in Western Canada: Genetic Variability and Effector Genes.
Phytopathology, 2020Co-Authors: Mohamed Hafez, Timothy L Friesen, Ryan Gourlie, Therese Despins, T. K. Turkington, Reem AboukhaddourAbstract:Parastagonospora nodorum is an important fungal pathogen that causes Septoria nodorum blotch (SNB) in wheat. This pathogen produces several necrotrophic effectors that act as virulence factors; three have been cloned, SnToxA, SnTox1, and SnTox3. In this study, P. nodorum and its sister species P. avenaria f. tritici (Pat1) were isolated from wheat node and grain samples collected from distanced sites in western Canada during 2018. The presence of effector genes and associated haplotypes were determined by PCR and sequence analysis. An internal transcribed spacer-restriction fragment length polymorphism test was developed to distinguish between leaf spotting pathogens (P. nodorum, Pat1, Pyrenophora tritici-repentis, and Bipolaris sorokiniana). P. nodorum was mainly recovered from wheat nodes and to a lesser extent from the grains, while Pat1 was exclusively isolated from grain samples. The effector genes were present in almost all P. nodorum isolates, with the ToxA haplotype 5 (H5) being most prevalent, while a novel ToxA haplotype (denoted here H21) is reported for the first time. In Pat1, only combinations of SnTox1 and SnTox3 genes were present. A ToxA haplotype network was also constructed to assess the evolutionary relationship among globally found haplotypes to date. Finally, cultivars representing wheat development in Canada for the last century were tested for sensitivity to Sn-effectors and to the presence of Tsn1, the ToxA sensitivity gene. Of tested cultivars, 32.9 and 56.9% were sensitive to SnTox1 and SnTox3, respectively, and Tsn1 was present in 59% of the cultivars. In conclusion, P. nodorum and Pat1 were prevalent wheat pathogens in Canada with a potential tissue-specific colonization capacity, while producing necrotrophic effectors to which wheat is sensitive.
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Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States.
PLoS genetics, 2019Co-Authors: Jonathan Richards, Justin D. Faris, Zhaohui Liu, Eva H. Stukenbrock, Jessica Carpenter, Christina Cowger, Timothy L FriesenAbstract:Filamentous fungi rapidly evolve in response to environmental selection pressures in part due to their genomic plasticity. Parastagonospora nodorum, a fungal pathogen of wheat and causal agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing the gain, loss, or functional diversification of virulence determinants, known as effector genes. Whole genome resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat production regions of the United States enabled the examination of effector diversity and genomic regions under selection specific to geographically discrete populations. 1,026,859 SNPs/InDels were used to identify novel loci, as well as SnToxA and SnTox3 as factors in disease. Genes displaying presence/absence variation, predicted effector genes, and genes localized on an accessory chromosome had significantly higher pN/pS ratios, indicating a higher rate of sequence evolution. Population structure analyses indicated two P. nodorum populations corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States (Population 2). Prevalence of SnToxA varied greatly between the two populations which correlated with presence of the host sensitivity gene Tsn1 in the most prevalent cultivars in the corresponding regions. Additionally, 12 and 5 candidate effector genes were observed to be under diversifying selection among isolates from Population 1 and 2, respectively, but under purifying selection or neutrally evolving in the opposite population. Selective sweep analysis revealed 10 and 19 regions that had recently undergone positive selection in Population 1 and 2, respectively, involving 92 genes in total. When comparing genes with and without presence/absence variation, those genes exhibiting this variation were significantly closer to transposable elements. Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection pressures unique to spring and winter wheat production regions by rapid adaptive evolution and various routes of genomic diversification, potentially facilitated through transposable element activity.
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Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States
2019Co-Authors: Jonathan Richards, Justin D. Faris, Zhaohui Liu, Eva H. Stukenbrock, Jessica Carpenter, Christina Cowger, Timothy L FriesenAbstract:Abstract Filamentous fungi rapidly evolve in response to environmental selection pressures, exemplified by their genomic plasticity. Parastagonospora nodorum, a fungal pathogen of wheat and causal agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing the gain, loss, or functional diversification of putative effector genes. Whole genome resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat production regions of the United States enabled the examination of effector diversity and genomic regions under selection specific to geographically discrete populations. A total of 1,026,859 quality SNPs/InDels were identified within the natural population. Implementation of GWAS identified novel loci, as well as SnToxA and SnTox3 as major factors in disease. Genes displaying presence/absence variation and predicted effector genes, as well as genes localized on an accessory chromosome, had significantly higher pN/pS ratios, indicating a greater level of diversifying selection. Population structure analyses indicated two major P. nodorum populations corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States (Population 2). Prevalence of SnToxA varied greatly between the two populations which correlated with presence of the host sensitivity gene Tsn1. Additionally, 12 and 5 candidate effector genes were observed to be diversifying among isolates from Population 1 and Population 2, respectively, but under purifying or neutral selection in the opposite population. Selective sweep analysis revealed 10 and 19 regions of positive selection from Population 1 and Population 2, respectively, with 92 genes underlying population-specific selective sweeps. Also, genes exhibiting presence/absence variation were significantly closer to transposable elements. Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection pressures unique to spring and winter wheat production regions by various routes of genomic diversification, potentially facilitated through transposable element activity. Author Summary Parastagonospora nodorum is an economically important pathogen of wheat, employing proteinaceous effector molecules to cause disease. Recognition of effectors by host susceptibility genes often leads to the elicitation of programmed cell death. However, little is known on the correlation between effector diversity and the spatial distribution of host resistance/susceptibility or the genomic mechanisms of diversification. This research presents the genome resequencing of 197 P. nodorum isolates collected from spring, winter, and durum wheat production regions of the United States, enabling the investigation of genome dynamics and evolution. Results illustrate local adaptation to host resistance or susceptibility, as evidenced by population-specific evolution of predicted effector genes and positively selected selective sweeps. Predicted effector genes, genes exhibiting presence/absence variation, and genes residing on an accessory chromosome, were found to be diversifying more rapidly. Additionally, transposable elements were predicted to play a role in the maintenance or elimination of genes. A GWAS approach identified the previously reported SnToxA and SnTox3 as well as novel virulence candidates, as major elicitors of disease on winter wheat. These results highlight the flexibility of the P. nodorum genome in response to population-specific selection pressures and illustrates the utility of whole genome resequencing for the identification of putative virulence mechanisms.
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Genetics of Variable Disease Expression Conferred by Inverse Gene-For-Gene Interactions in the Wheat-Parastagonospora nodorum Pathosystem.
Plant physiology, 2019Co-Authors: Amanda R. Peters Haugrud, Timothy L Friesen, Zengcui Zhang, Jonathan Richards, Justin D. FarisAbstract:The wheat-Parastagonospora nodorum pathosystem involves the recognition of pathogen-secreted necrotrophic effectors (NEs) by corresponding wheat NE sensitivity genes. This inverse gene-for-gene recognition leads to necrotrophic effector-triggered susceptibility and ultimately septoria nodorum blotch disease. Here, we used multiple pathogen isolates to individually evaluate the effects of the host gene-NE interactions Tan spot necrosis1-Stagonospora nodorum ToxinA (Tsn1-SnToxA), Stagonospora nodorum necrosis1-Stagonospora nodorum Toxin1 (Snn1-SnTox1), and Stagonospora nodorum necrosis3-B genome homeolog1-Stagonospora nodorum Toxin3 (Snn3-B1-SnTox3), alone and in various combinations, to determine the relative importance of these interactions in causing disease. Genetic analysis of a recombinant inbred wheat population inoculated separately with three P. nodorum isolates, all of which produce all three NEs, indicated that the Tsn1-SnToxA and Snn3-B1-SnTox3 interactions contributed to disease caused by all four isolates, but their effects varied and ranged from epistatic to additive. The Snn1-SnTox1 interaction was associated with increased disease for one isolate, but for other isolates, there was evidence that this interaction inhibited the expression of other host gene-NE interactions. RNA sequencing analysis in planta showed that SnTox1 was differentially expressed between these three isolates after infection. Further analysis of NE gene-knockout isolates showed that the effect of some interactions could be masked or inhibited by other compatible interactions, and the regulation of this occurs at the level of NE gene transcription. Collectively, these results show that the inverse gene-for-gene interactions leading to necrotrophic effector-triggered susceptibility in the wheat-P. nodorum pathosystem vary in their effects depending on the genetic backgrounds of the pathogen and host, and interplay among the interactions is complex and intricately regulated.
Kar-chun Tan - One of the best experts on this subject based on the ideXlab platform.
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Septoria nodorum blotch of wheat: disease management and resistance breeding in the face of shifting disease dynamics and a changing environment.
Phytopathology, 2020Co-Authors: Rowena C. Downie, Min Lin, Andrea Ficke, Morten Lillemo, Richard P. Oliver, Kar-chun Tan, Beatrice Corsi, H. Phan, James CockramAbstract:The fungus Parastagonospora nodorum is a narrow host range necrotrophic fungal pathogen that causes Septoria nodorum blotch (SNB) of cereals, most notably wheat. Although commonly observed on wheat seedlings, P. nodorum infection has the greatest effect on the adult crop. It results in leaf blotch, which limits photosynthesis and thus crop growth and yield. It can also affect the wheat ear, resulting in glume blotch which directly affects grain quality. Reports of P. nodorum fungicide resistance, the increasing use of reduced tillage agronomic practices and high evolutionary potential of the pathogen, combined with changes in climate and agricultural environments, mean that genetic resistance to SNB remains a high priority in many regions of wheat cultivation. In this review, we summarise current information on P. nodorum population structure and its implication for improved SNB management. We then review recent advances in the genetics of host resistance to P. nodorum and the necrotrophic effectors it secretes during infection, integrating the genomic positions of these genetic loci using the recently released wheat reference genome assembly. Finally, we discuss the genetic and genomic tools now available for SNB resistance breeding and consider future opportunities and challenges in crop health management using the wheat-P. nodorum interaction as a model.
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Genetic mapping using a wheat multi-founder population reveals a locus on chromosome 2A controlling resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum
Theoretical and Applied Genetics, 2020Co-Authors: Min Lin, Andrea Ficke, James Cockram, Kar-chun Tan, Beatrice Corsi, Morten LillemoAbstract:Key message A locus on wheat chromosome 2A was found to control field resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum . Abstract The necrotrophic fungal pathogen Parastagonospora nodorum is the causal agent of Septoria nodorum leaf blotch and glume blotch, which are common wheat ( Triticum aestivum L.) diseases in humid and temperate areas. Susceptibility to Septoria nodorum leaf blotch can partly be explained by sensitivity to corresponding P. nodorum necrotrophic effectors (NEs). Susceptibility to glume blotch is also quantitative; however, the underlying genetics have not been studied in detail. Here, we genetically map resistance/susceptibility loci to leaf and glume blotch using an eight-founder wheat multiparent advanced generation intercross population. The population was assessed in six field trials across two sites and 4 years. Seedling infiltration and inoculation assays using three P. nodorum isolates were also carried out, in order to compare quantitative trait loci (QTL) identified under controlled conditions with those identified in the field. Three significant field resistance QTL were identified on chromosomes 2A and 6A, while four significant seedling resistance QTL were detected on chromosomes 2D, 5B and 7D. Among these, QSnb.niab - 2A.3 for field resistance to both leaf blotch and glume blotch was detected in Norway and the UK. Colocation with a QTL for seedling reactions against culture filtrate from a Norwegian P. nodorum isolate indicated the QTL could be caused by a novel NE sensitivity. The consistency of this QTL for leaf blotch at the seedling and adult plant stages and culture filtrate infiltration was confirmed by haplotype analysis. However, opposite effects for the leaf blotch and glume blotch reactions suggest that different genetic mechanisms may be involved.
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Genetic mapping using a wheat multi-founder population reveals a locus on chromosome 2A controlling resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik, 2020Co-Authors: Min Lin, Andrea Ficke, James Cockram, Kar-chun Tan, Beatrice Corsi, Morten LillemoAbstract:A locus on wheat chromosome 2A was found to control field resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum. The necrotrophic fungal pathogen Parastagonospora nodorum is the causal agent of Septoria nodorum leaf blotch and glume blotch, which are common wheat (Triticum aestivum L.) diseases in humid and temperate areas. Susceptibility to Septoria nodorum leaf blotch can partly be explained by sensitivity to corresponding P. nodorum necrotrophic effectors (NEs). Susceptibility to glume blotch is also quantitative; however, the underlying genetics have not been studied in detail. Here, we genetically map resistance/susceptibility loci to leaf and glume blotch using an eight-founder wheat multiparent advanced generation intercross population. The population was assessed in six field trials across two sites and 4 years. Seedling infiltration and inoculation assays using three P. nodorum isolates were also carried out, in order to compare quantitative trait loci (QTL) identified under controlled conditions with those identified in the field. Three significant field resistance QTL were identified on chromosomes 2A and 6A, while four significant seedling resistance QTL were detected on chromosomes 2D, 5B and 7D. Among these, QSnb.niab-2A.3 for field resistance to both leaf blotch and glume blotch was detected in Norway and the UK. Colocation with a QTL for seedling reactions against culture filtrate from a Norwegian P. nodorum isolate indicated the QTL could be caused by a novel NE sensitivity. The consistency of this QTL for leaf blotch at the seedling and adult plant stages and culture filtrate infiltration was confirmed by haplotype analysis. However, opposite effects for the leaf blotch and glume blotch reactions suggest that different genetic mechanisms may be involved.
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A specific fungal transcription factor controls effector gene expression and orchestrates the establishment of the necrotrophic pathogen lifestyle on wheat
Scientific Reports, 2019Co-Authors: Darcy A. B. Jones, Peter S. Solomon, Richard P. Oliver, Kasia Rybak, Shao Yu Lin, Evan John, Huyen T. T. Phan, Karam B. Singh, Kar-chun TanAbstract:The fungus Parastagonospora nodorum infects wheat through the use of necrotrophic effector (NE) proteins that cause host-specific tissue necrosis. The Zn_2Cys_6 transcription factor PnPf2 positively regulates NE gene expression and is required for virulence on wheat. Little is known about other downstream targets of PnPf2. We compared the transcriptomes of the P . nodorum wildtype and a strain deleted in PnPf2 ( pf2-69 ) during in vitro growth and host infection to further elucidate targets of PnPf2 signalling. Gene ontology enrichment analysis of the differentially expressed (DE) genes revealed that genes associated with plant cell wall degradation and proteolysis were enriched in down-regulated DE gene sets in pf2-69 compared to SN15. In contrast, genes associated with redox control, nutrient and ion transport were up-regulated in the mutant. Further analysis of the DE gene set revealed that PnPf2 positively regulates twelve genes that encode effector-like proteins. Two of these genes encode proteins with homology to previously characterised effectors in other fungal phytopathogens. In addition to modulating effector gene expression, PnPf2 may play a broader role in the establishment of a necrotrophic lifestyle by orchestrating the expression of genes associated with plant cell wall degradation and nutrient assimilation.
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Pan-Parastagonospora Comparative Genome Analysis-Effector Prediction and Genome Evolution.
Genome biology and evolution, 2018Co-Authors: Robert A. Syme, Timothy L Friesen, Richard P. Oliver, Kar-chun Tan, Bruce A. Mcdonald, Kasia Rybak, James K. HaneAbstract:We report a fungal pan-genome study involving Parastagonospora spp., including 21 isolates of the wheat (Triticum aestivum) pathogen Parastagonospora nodorum, 10 of the grass-infecting Parastagonospora avenae, and 2 of a closely related undefined sister species. We observed substantial variation in the distribution of polymorphisms across the pan-genome, including repeat-induced point mutations, diversifying selection and gene gains and losses. We also discovered chromosome-scale inter and intraspecific presence/absence variation of some sequences, suggesting the occurrence of one or more accessory chromosomes or regions that may play a role in host-pathogen interactions. The presence of known pathogenicity effector loci SnToxA, SnTox1, and SnTox3 varied substantially among isolates. Three P. nodorum isolates lacked functional versions for all three loci, whereas three P. avenae isolates carried one or both of the SnTox1 and SnTox3 genes, indicating previously unrecognized potential for discovering additional effectors in the P. nodorum-wheat pathosystem. We utilized the pan-genomic comparative analysis to improve the prediction of pathogenicity effector candidates, recovering the three confirmed effectors among our top-ranked candidates. We propose applying this pan-genomic approach to identify the effector repertoire involved in other host-microbe interactions involving necrotrophic pathogens in the Pezizomycotina.
Morten Lillemo - One of the best experts on this subject based on the ideXlab platform.
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Septoria nodorum blotch of wheat: disease management and resistance breeding in the face of shifting disease dynamics and a changing environment.
Phytopathology, 2020Co-Authors: Rowena C. Downie, Min Lin, Andrea Ficke, Morten Lillemo, Richard P. Oliver, Kar-chun Tan, Beatrice Corsi, H. Phan, James CockramAbstract:The fungus Parastagonospora nodorum is a narrow host range necrotrophic fungal pathogen that causes Septoria nodorum blotch (SNB) of cereals, most notably wheat. Although commonly observed on wheat seedlings, P. nodorum infection has the greatest effect on the adult crop. It results in leaf blotch, which limits photosynthesis and thus crop growth and yield. It can also affect the wheat ear, resulting in glume blotch which directly affects grain quality. Reports of P. nodorum fungicide resistance, the increasing use of reduced tillage agronomic practices and high evolutionary potential of the pathogen, combined with changes in climate and agricultural environments, mean that genetic resistance to SNB remains a high priority in many regions of wheat cultivation. In this review, we summarise current information on P. nodorum population structure and its implication for improved SNB management. We then review recent advances in the genetics of host resistance to P. nodorum and the necrotrophic effectors it secretes during infection, integrating the genomic positions of these genetic loci using the recently released wheat reference genome assembly. Finally, we discuss the genetic and genomic tools now available for SNB resistance breeding and consider future opportunities and challenges in crop health management using the wheat-P. nodorum interaction as a model.
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Genetic Structure of the Norwegian Parastagonospora nodorum Population.
Frontiers in microbiology, 2020Co-Authors: Min Lin, Andrea Ficke, James Cockram, Morten LillemoAbstract:The necrotrophic fungal pathogen Parastagonospora nodorum causes Septoria nodorum blotch (SNB), which is one of the dominating leaf blotch diseases of wheat in Norway. A total of 165 P. nodorum isolates were collected from three wheat growing regions in Norway from 2015 to 2017. These isolates, as well as nine isolates from other countries, were analyzed for genetic variation using 20 simple sequence repeat (SSR) markers. Genetic analysis of the isolate collection indicated that the P. nodorum pathogen population infecting Norwegian spring and winter wheat underwent regular sexual reproduction and exhibited a high level of genetic diversity, with no genetic subdivisions between sampled locations, years or host cultivars. A high frequency of the presence of necrotrophic effector (NE) gene SnToxA was found in Norwegian P. nodorum isolates compared to other parts of Europe, and we hypothesize that the SnToxA gene is the major virulence factor among the three known P. nodorum NE genes (SnToxA, SnTox1, and SnTox3) in the Norwegian pathogen population. While the importance of SNB has declined in much of Europe, Norway has remained as a P. nodorum hotspot, likely due at least in part to local adaptation of the pathogen population to ToxA sensitive Norwegian spring wheat cultivars.
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Genetic mapping using a wheat multi-founder population reveals a locus on chromosome 2A controlling resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum
Theoretical and Applied Genetics, 2020Co-Authors: Min Lin, Andrea Ficke, James Cockram, Kar-chun Tan, Beatrice Corsi, Morten LillemoAbstract:Key message A locus on wheat chromosome 2A was found to control field resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum . Abstract The necrotrophic fungal pathogen Parastagonospora nodorum is the causal agent of Septoria nodorum leaf blotch and glume blotch, which are common wheat ( Triticum aestivum L.) diseases in humid and temperate areas. Susceptibility to Septoria nodorum leaf blotch can partly be explained by sensitivity to corresponding P. nodorum necrotrophic effectors (NEs). Susceptibility to glume blotch is also quantitative; however, the underlying genetics have not been studied in detail. Here, we genetically map resistance/susceptibility loci to leaf and glume blotch using an eight-founder wheat multiparent advanced generation intercross population. The population was assessed in six field trials across two sites and 4 years. Seedling infiltration and inoculation assays using three P. nodorum isolates were also carried out, in order to compare quantitative trait loci (QTL) identified under controlled conditions with those identified in the field. Three significant field resistance QTL were identified on chromosomes 2A and 6A, while four significant seedling resistance QTL were detected on chromosomes 2D, 5B and 7D. Among these, QSnb.niab - 2A.3 for field resistance to both leaf blotch and glume blotch was detected in Norway and the UK. Colocation with a QTL for seedling reactions against culture filtrate from a Norwegian P. nodorum isolate indicated the QTL could be caused by a novel NE sensitivity. The consistency of this QTL for leaf blotch at the seedling and adult plant stages and culture filtrate infiltration was confirmed by haplotype analysis. However, opposite effects for the leaf blotch and glume blotch reactions suggest that different genetic mechanisms may be involved.
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Genetic mapping using a wheat multi-founder population reveals a locus on chromosome 2A controlling resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik, 2020Co-Authors: Min Lin, Andrea Ficke, James Cockram, Kar-chun Tan, Beatrice Corsi, Morten LillemoAbstract:A locus on wheat chromosome 2A was found to control field resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum. The necrotrophic fungal pathogen Parastagonospora nodorum is the causal agent of Septoria nodorum leaf blotch and glume blotch, which are common wheat (Triticum aestivum L.) diseases in humid and temperate areas. Susceptibility to Septoria nodorum leaf blotch can partly be explained by sensitivity to corresponding P. nodorum necrotrophic effectors (NEs). Susceptibility to glume blotch is also quantitative; however, the underlying genetics have not been studied in detail. Here, we genetically map resistance/susceptibility loci to leaf and glume blotch using an eight-founder wheat multiparent advanced generation intercross population. The population was assessed in six field trials across two sites and 4 years. Seedling infiltration and inoculation assays using three P. nodorum isolates were also carried out, in order to compare quantitative trait loci (QTL) identified under controlled conditions with those identified in the field. Three significant field resistance QTL were identified on chromosomes 2A and 6A, while four significant seedling resistance QTL were detected on chromosomes 2D, 5B and 7D. Among these, QSnb.niab-2A.3 for field resistance to both leaf blotch and glume blotch was detected in Norway and the UK. Colocation with a QTL for seedling reactions against culture filtrate from a Norwegian P. nodorum isolate indicated the QTL could be caused by a novel NE sensitivity. The consistency of this QTL for leaf blotch at the seedling and adult plant stages and culture filtrate infiltration was confirmed by haplotype analysis. However, opposite effects for the leaf blotch and glume blotch reactions suggest that different genetic mechanisms may be involved.
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Molecular mapping of adult plant resistance to Parastagonospora nodorum leaf blotch in bread wheat lines ‘Shanghai-3/Catbird’ and ‘Naxos’
Theoretical and Applied Genetics, 2014Co-Authors: Morten LillemoAbstract:Key message The field resistance to Parastagonospora nodorum leaf blotch in SHA3/CBRD is based on many genes with minor effects. Abstract Parastagonospora nodorum leaf blotch is a severe wheat disease in Norway and other regions with humid and rainy climate. It causes grain shriveling and reduced yield in years of epidemics. Shanghai-3/Catbird (SHA3/CBRD), a CIMMYT breeding line, was observed to be resistant to P. nodorum leaf blotch in the field. The objective of the current study was to map the genetic factors related to its resistance. A recombinant inbred line population from a cross between SHA3/CBRD and the susceptible German spring cv. Naxos was tested in field trials over 4 years (2010, 2011, 2012 and 2013) with natural infection supplied with mist irrigation. Leaf blotch severity was scored together with plant height, heading date and maturity date in these trials. A testing data set was also available from other field trials with the same population. Totally, two major and six minor QTL were detected for leaf blotch resistance. The major QTL on chromosome 3BL with resistance contributed by Naxos was consistent across all environments and explained up to 12 % of the phenotypic variation. Another major QTL on 3B with resistance from SHA3/CBRD was significant in 2010, 2013 and the testing data set and explained up to 12 % of the phenotypic variation. Minor QTL were detected on 1B, 3AS, 5BS, 5BL, 7A and 7B. The 5BS QTL was likely caused by Snn3 - B1 , with sensitivity contributed by Naxos. The 5BL QTL mapped to the Tsn1 region, but was likely caused by other mechanisms since both parents were insensitive to ToxA.
Richard P. Oliver - One of the best experts on this subject based on the ideXlab platform.
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Septoria nodorum blotch of wheat: disease management and resistance breeding in the face of shifting disease dynamics and a changing environment.
Phytopathology, 2020Co-Authors: Rowena C. Downie, Min Lin, Andrea Ficke, Morten Lillemo, Richard P. Oliver, Kar-chun Tan, Beatrice Corsi, H. Phan, James CockramAbstract:The fungus Parastagonospora nodorum is a narrow host range necrotrophic fungal pathogen that causes Septoria nodorum blotch (SNB) of cereals, most notably wheat. Although commonly observed on wheat seedlings, P. nodorum infection has the greatest effect on the adult crop. It results in leaf blotch, which limits photosynthesis and thus crop growth and yield. It can also affect the wheat ear, resulting in glume blotch which directly affects grain quality. Reports of P. nodorum fungicide resistance, the increasing use of reduced tillage agronomic practices and high evolutionary potential of the pathogen, combined with changes in climate and agricultural environments, mean that genetic resistance to SNB remains a high priority in many regions of wheat cultivation. In this review, we summarise current information on P. nodorum population structure and its implication for improved SNB management. We then review recent advances in the genetics of host resistance to P. nodorum and the necrotrophic effectors it secretes during infection, integrating the genomic positions of these genetic loci using the recently released wheat reference genome assembly. Finally, we discuss the genetic and genomic tools now available for SNB resistance breeding and consider future opportunities and challenges in crop health management using the wheat-P. nodorum interaction as a model.
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A specific fungal transcription factor controls effector gene expression and orchestrates the establishment of the necrotrophic pathogen lifestyle on wheat
Scientific Reports, 2019Co-Authors: Darcy A. B. Jones, Peter S. Solomon, Richard P. Oliver, Kasia Rybak, Shao Yu Lin, Evan John, Huyen T. T. Phan, Karam B. Singh, Kar-chun TanAbstract:The fungus Parastagonospora nodorum infects wheat through the use of necrotrophic effector (NE) proteins that cause host-specific tissue necrosis. The Zn_2Cys_6 transcription factor PnPf2 positively regulates NE gene expression and is required for virulence on wheat. Little is known about other downstream targets of PnPf2. We compared the transcriptomes of the P . nodorum wildtype and a strain deleted in PnPf2 ( pf2-69 ) during in vitro growth and host infection to further elucidate targets of PnPf2 signalling. Gene ontology enrichment analysis of the differentially expressed (DE) genes revealed that genes associated with plant cell wall degradation and proteolysis were enriched in down-regulated DE gene sets in pf2-69 compared to SN15. In contrast, genes associated with redox control, nutrient and ion transport were up-regulated in the mutant. Further analysis of the DE gene set revealed that PnPf2 positively regulates twelve genes that encode effector-like proteins. Two of these genes encode proteins with homology to previously characterised effectors in other fungal phytopathogens. In addition to modulating effector gene expression, PnPf2 may play a broader role in the establishment of a necrotrophic lifestyle by orchestrating the expression of genes associated with plant cell wall degradation and nutrient assimilation.
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Pan-Parastagonospora Comparative Genome Analysis-Effector Prediction and Genome Evolution.
Genome biology and evolution, 2018Co-Authors: Robert A. Syme, Timothy L Friesen, Richard P. Oliver, Kar-chun Tan, Bruce A. Mcdonald, Kasia Rybak, James K. HaneAbstract:We report a fungal pan-genome study involving Parastagonospora spp., including 21 isolates of the wheat (Triticum aestivum) pathogen Parastagonospora nodorum, 10 of the grass-infecting Parastagonospora avenae, and 2 of a closely related undefined sister species. We observed substantial variation in the distribution of polymorphisms across the pan-genome, including repeat-induced point mutations, diversifying selection and gene gains and losses. We also discovered chromosome-scale inter and intraspecific presence/absence variation of some sequences, suggesting the occurrence of one or more accessory chromosomes or regions that may play a role in host-pathogen interactions. The presence of known pathogenicity effector loci SnToxA, SnTox1, and SnTox3 varied substantially among isolates. Three P. nodorum isolates lacked functional versions for all three loci, whereas three P. avenae isolates carried one or both of the SnTox1 and SnTox3 genes, indicating previously unrecognized potential for discovering additional effectors in the P. nodorum-wheat pathosystem. We utilized the pan-genomic comparative analysis to improve the prediction of pathogenicity effector candidates, recovering the three confirmed effectors among our top-ranked candidates. We propose applying this pan-genomic approach to identify the effector repertoire involved in other host-microbe interactions involving necrotrophic pathogens in the Pezizomycotina.
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Novel sources of resistance to Septoria nodorum blotch in the Vavilov wheat collection identified by genome-wide association studies
Theoretical and Applied Genetics, 2018Co-Authors: Huyen T. T. Phan, Richard P. Oliver, Eiko Furuki, Kasia Rybak, Stefania Bertazzoni, Eric Dinglasan, Lee T. Hickey, Kar-chun TanAbstract:Key message The fungus Parastagonospora nodorum causes Septoria nodorum blotch (SNB) of wheat. A genetically diverse wheat panel was used to dissect the complexity of SNB and identify novel sources of resistance. Abstract The fungus Parastagonospora nodorum is the causal agent of Septoria nodorum blotch (SNB) of wheat. The pathosystem is mediated by multiple fungal necrotrophic effector–host sensitivity gene interactions that include SnToxA– Tsn1 , SnTox1– Snn1, and SnTox3– Snn3 . A P. nodorum strain lacking SnToxA , SnTox1, and SnTox3 ( toxa13 ) retained wild-type-like ability to infect some modern wheat cultivars, suggesting evidence of other effector-mediated susceptibility gene interactions or the lack of host resistance genes. To identify genomic regions harbouring such loci, we examined a panel of 295 historic wheat accessions from the N. I. Vavilov Institute of Plant Genetic Resources in Russia, which is comprised of genetically diverse landraces and breeding lines registered from 1920 to 1990. The wheat panel was subjected to effector bioassays, infection with P. nodorum wild type (SN15) and toxa13 . In general, SN15 was more virulent than toxa13. Insensitivity to all three effectors contributed significantly to resistance against SN15, but not toxa13 . Genome-wide association studies using phenotypes from SN15 infection detected quantitative trait loci (QTL) on chromosomes 1BS ( Snn1 ), 2DS, 5AS, 5BS ( Snn3 ), 3AL, 4AL, 4BS, and 7AS. For toxa13 infection, a QTL was detected on 5AS (similar to SN15), plus two additional QTL on 2DL and 7DL. Analysis of resistance phenotypes indicated that plant breeders may have inadvertently selected for effector insensitivity from 1940 onwards. We identify accessions that can be used to develop bi-parental mapping populations to characterise resistance-associated alleles for subsequent introgression into modern bread wheat to minimise the impact of SNB.
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Novel sources of resistance to Septoria nodorum blotch in the Vavilov wheat collection identified by genome-wide association studies.
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik, 2018Co-Authors: H. Phan, Richard P. Oliver, Eiko Furuki, Kasia Rybak, Stefania Bertazzoni, Eric Dinglasan, Lee T. Hickey, Kar-chun TanAbstract:The fungus Parastagonospora nodorum causes Septoria nodorum blotch (SNB) of wheat. A genetically diverse wheat panel was used to dissect the complexity of SNB and identify novel sources of resistance. The fungus Parastagonospora nodorum is the causal agent of Septoria nodorum blotch (SNB) of wheat. The pathosystem is mediated by multiple fungal necrotrophic effector-host sensitivity gene interactions that include SnToxA-Tsn1, SnTox1-Snn1, and SnTox3-Snn3. A P. nodorum strain lacking SnToxA, SnTox1, and SnTox3 (toxa13) retained wild-type-like ability to infect some modern wheat cultivars, suggesting evidence of other effector-mediated susceptibility gene interactions or the lack of host resistance genes. To identify genomic regions harbouring such loci, we examined a panel of 295 historic wheat accessions from the N. I. Vavilov Institute of Plant Genetic Resources in Russia, which is comprised of genetically diverse landraces and breeding lines registered from 1920 to 1990. The wheat panel was subjected to effector bioassays, infection with P. nodorum wild type (SN15) and toxa13. In general, SN15 was more virulent than toxa13. Insensitivity to all three effectors contributed significantly to resistance against SN15, but not toxa13. Genome-wide association studies using phenotypes from SN15 infection detected quantitative trait loci (QTL) on chromosomes 1BS (Snn1), 2DS, 5AS, 5BS (Snn3), 3AL, 4AL, 4BS, and 7AS. For toxa13 infection, a QTL was detected on 5AS (similar to SN15), plus two additional QTL on 2DL and 7DL. Analysis of resistance phenotypes indicated that plant breeders may have inadvertently selected for effector insensitivity from 1940 onwards. We identify accessions that can be used to develop bi-parental mapping populations to characterise resistance-associated alleles for subsequent introgression into modern bread wheat to minimise the impact of SNB.
