Publications by authors named "Kim E Hammond-Kosack"

75 Publications

Take-All Disease: New Insights into an Important Wheat Root Pathogen.

Trends Plant Sci 2021 Mar 19. Epub 2021 Mar 19.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, UK. Electronic address:

Take-all disease, caused by the fungal root pathogen Gaeumannomyces tritici, is considered to be the most important root disease of wheat worldwide. Here we review the advances in take-all research over the last 15 years, focusing on the identification of new sources of genetic resistance in wheat relatives and the role of the microbiome in disease development. We also highlight recent breakthroughs in the molecular interactions between G. tritici and wheat, including genome and transcriptome analyses. These new findings will aid the development of novel control strategies against take-all disease. In light of this growing understanding, the G. tritici-wheat interaction could provide a model study system for root-infecting fungal pathogens of cereals.
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http://dx.doi.org/10.1016/j.tplants.2021.02.009DOI Listing
March 2021

Functional evaluation of a homologue of plant rapid alkalinisation factor (RALF) peptides in Fusarium graminearum.

Fungal Biol 2020 Sep 16;124(9):753-765. Epub 2020 Jun 16.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, AL5 2JQ, UK. Electronic address:

The cereal infecting fungus Fusarium graminearum is predicted to possess a single homologue of plant RALF (rapid alkalinisation factor) peptides. Fusarium mutant strains lacking FgRALF were generated and found to exhibit wildtype virulence on wheat and Arabidopsis floral tissue. Arabidopsis lines constitutively overexpressing FgRALF exhibited no obvious change in susceptibility to F. graminearum leaf infection. In contrast transient virus-mediated over-expression (VOX) of FgRALF in wheat prior to F. graminearum infection, slightly increased the rate of fungal colonisation of floral tissue. Ten putative Feronia (FER) receptors of RALF peptide were identified bioinformatically in hexaploid wheat (Triticum aestivum). Transient silencing of two wheat FER homoeologous genes prior to F. graminearum inoculation did not alter the subsequent interaction outcome. Collectively, our VOX results show that the fungal RALF peptide may be a minor contributor in F. graminearum virulence but results from fungal gene deletion experiments indicate potential functional redundancy within the F. graminearum genome. We demonstrate that virus-mediated over-expression is a useful tool to provide novel information about gene/protein function when results from gene deletion/disruption experimentation were uninformative.
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http://dx.doi.org/10.1016/j.funbio.2020.05.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7487784PMC
September 2020

Proteinaceous effector discovery and characterization in filamentous plant pathogens.

Mol Plant Pathol 2020 10 7;21(10):1353-1376. Epub 2020 Aug 7.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, UK.

The complicated interplay of plant-pathogen interactions occurs on multiple levels as pathogens evolve to constantly evade the immune responses of their hosts. Many economically important crops fall victim to filamentous pathogens that produce small proteins called effectors to manipulate the host and aid infection/colonization. Understanding the effector repertoires of pathogens is facilitating an increased understanding of the molecular mechanisms underlying virulence as well as guiding the development of disease control strategies. The purpose of this review is to give a chronological perspective on the evolution of the methodologies used in effector discovery from physical isolation and in silico predictions, to functional characterization of the effectors of filamentous plant pathogens and identification of their host targets.
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http://dx.doi.org/10.1111/mpp.12980DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7488470PMC
October 2020

Genome Sequence of Fusarium graminearum Strain CML3066, Isolated from a Wheat Spike in Southern Brazil.

Microbiol Resour Announc 2020 May 7;9(19). Epub 2020 May 7.

Rothamsted Research, Harpenden, Hertfordshire, United Kingdom

is a global fungal pathogen of wheat and other small grains, causing head blight (FHB) disease, also known as wheat scab. We report here the annotated genome of a deoxynivalenol/15-acetyl-deoxynivalenol-producing Brazilian strain called CML3066, isolated from FHB-symptomatic wheat spikes collected in 2009.
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http://dx.doi.org/10.1128/MRA.00157-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7206484PMC
May 2020

PHI-Nets: A Network Resource for Ascomycete Fungal Pathogens to Annotate and Identify Putative Virulence Interacting Proteins and siRNA Targets.

Front Microbiol 2019 6;10:2721. Epub 2019 Dec 6.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, United Kingdom.

Interactions between proteins underlie all aspects of complex biological mechanisms. Therefore, methodologies based on complex network analyses can facilitate identification of promising candidate genes involved in phenotypes of interest and put this information into appropriate contexts. To facilitate discovery and gain additional insights into globally important pathogenic fungi, we have reconstructed computationally inferred interactomes using an interolog and domain-based approach for 15 diverse Ascomycete fungal species, across nine orders, specifically , , f. sp. , , , , , f. sp. , , , , , , , and . Network cartography analysis was associated with functional patterns of annotated genes linked to the disease-causing ability of each pathogen. In addition, for the best annotated organism, namely , the distribution of annotated genes with respect to network structure was profiled using a random walk with restart algorithm, which suggested possible co-location of virulence-related genes in the protein-protein interaction network. In a second 'use case' study involving two networks, namely and , previously identified small silencing plant RNAs were mapped to their targets. The phenotypic network analysis implicates eight targets and 35 predicted interacting proteins as prime candidate virulence genes for further testing. All 15 networks have been made accessible for download at www.phi-base.org providing a rich resource for major crop plant pathogens.
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http://dx.doi.org/10.3389/fmicb.2019.02721DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908471PMC
December 2019

PHI-base: the pathogen-host interactions database.

Nucleic Acids Res 2020 01;48(D1):D613-D620

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden AL5 2JQ, UK.

The pathogen-host interactions database (PHI-base) is available at www.phi-base.org. PHI-base contains expertly curated molecular and biological information on genes proven to affect the outcome of pathogen-host interactions reported in peer reviewed research articles. PHI-base also curates literature describing specific gene alterations that did not affect the disease interaction phenotype, in order to provide complete datasets for comparative purposes. Viruses are not included, due to their extensive coverage in other databases. In this article, we describe the increased data content of PHI-base, plus new database features and further integration with complementary databases. The release of PHI-base version 4.8 (September 2019) contains 3454 manually curated references, and provides information on 6780 genes from 268 pathogens, tested on 210 hosts in 13,801 interactions. Prokaryotic and eukaryotic pathogens are represented in almost equal numbers. Host species consist of approximately 60% plants (split 50:50 between cereal and non-cereal plants), and 40% other species of medical and/or environmental importance. The information available on pathogen effectors has risen by more than a third, and the entries for pathogens that infect crop species of global importance has dramatically increased in this release. We also briefly describe the future direction of the PHI-base project, and some existing problems with the PHI-base curation process.
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http://dx.doi.org/10.1093/nar/gkz904DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7145647PMC
January 2020

Ensembl Genomes 2020-enabling non-vertebrate genomic research.

Nucleic Acids Res 2020 01;48(D1):D689-D695

European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK.

Ensembl Genomes (http://www.ensemblgenomes.org) is an integrating resource for genome-scale data from non-vertebrate species, complementing the resources for vertebrate genomics developed in the context of the Ensembl project (http://www.ensembl.org). Together, the two resources provide a consistent set of interfaces to genomic data across the tree of life, including reference genome sequence, gene models, transcriptional data, genetic variation and comparative analysis. Data may be accessed via our website, online tools platform and programmatic interfaces, with updates made four times per year (in synchrony with Ensembl). Here, we provide an overview of Ensembl Genomes, with a focus on recent developments. These include the continued growth, more robust and reproducible sets of orthologues and paralogues, and enriched views of gene expression and gene function in plants. Finally, we report on our continued deeper integration with the Ensembl project, which forms a key part of our future strategy for dealing with the increasing quantity of available genome-scale data across the tree of life.
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http://dx.doi.org/10.1093/nar/gkz890DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6943047PMC
January 2020

sRNA Profiling Combined With Gene Function Analysis Reveals a Lack of Evidence for Cross-Kingdom RNAi in the Wheat - Pathosystem.

Front Plant Sci 2019 4;10:892. Epub 2019 Jul 4.

Biointeractions and Crop Protection, Rothamsted Research, Harpenden, United Kingdom.

Cross-kingdom small RNA (sRNA) silencing has recently emerged as a mechanism facilitating fungal colonization and disease development. Here we characterized RNAi pathways in , a major fungal pathogen of wheat, and assessed their contribution to pathogenesis. Computational analysis of fungal sRNA and host mRNA sequencing datasets was used to define the global sRNA populations in and predict their mRNA targets in wheat. 389 -induced sRNA loci were identified. sRNAs generated from some of these loci were predicted to target wheat mRNAs including those potentially involved in pathogen defense. However, molecular approaches failed to validate targeting of selected wheat mRNAs by fungal sRNAs. Mutant strains of carrying deletions of genes encoding key components of RNAi such as Dicer-like (DCL) and Argonaute (AGO) proteins were generated, and virulence bioassays suggested that these are dispensable for full infection of wheat. Nonetheless, our results did suggest the existence of non-canonical DCL-independent pathway(s) for sRNA biogenesis in . dsRNA targeting essential fungal genes applied or generated from an RNA virus vector in a procedure known as HIGS (Host-Induced Gene Silencing) was ineffective in preventing growth or disease. We also demonstrated that is incapable of dsRNA uptake. Collectively, our data suggest that RNAi approaches for gene function analyses in this fungal species and potentially also as a control measure may not be as effective as has been demonstrated for some other plant pathogenic fungi.
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http://dx.doi.org/10.3389/fpls.2019.00892DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6620828PMC
July 2019

Non-canonical fungal G-protein coupled receptors promote Fusarium head blight on wheat.

PLoS Pathog 2019 04 1;15(4):e1007666. Epub 2019 Apr 1.

Biointeractions and Crop Protection, Rothamsted Research, Hertfordshire, United Kingdom.

Fusarium Head Blight (FHB) is the number one floral disease of cereals and poses a serious health hazard by contaminating grain with the harmful mycotoxin deoxynivalenol (DON). Fungi adapt to fluctuations in their environment, coordinating development and metabolism accordingly. G-protein coupled receptors (GPCRs) communicate changes in the environment to intracellular G-proteins that direct the appropriate biological response, suggesting that fungal GPCR signalling may be key to virulence. Here we describe the expansion of non-classical GPCRs in the FHB causing pathogen, Fusarium graminearum, and show that class X receptors are highly expressed during wheat infection. We identify class X receptors that are required for FHB disease on wheat, and show that the absence of a GPCR can cause an enhanced host response that restricts the progression of infection. Specific receptor sub-domains are required for virulence. These non-classical receptors physically interact with intracellular G-proteins and are therefore bona fide GPCRs. Disrupting a class X receptor is shown to dysregulate the transcriptional coordination of virulence traits during infection. This amounts to enhanced wheat defensive responses, including chitinase and plant cell wall biosynthesis, resulting in apoplastic and vascular occlusions that impede infection. Our results show that GPCR signalling is important to FHB disease establishment.
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http://dx.doi.org/10.1371/journal.ppat.1007666DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6459559PMC
April 2019

The adaptation of to DMI Fungicides Is Mediated by Major Transcriptome Modifications in Response to Azole Fungicide, Including the Overexpression of a PDR Transporter (FcABC1).

Front Microbiol 2018 26;9:1385. Epub 2018 Jun 26.

Earth and Life Institute, Applied Microbiology, Phytopathology, Université Catholique de Louvain, Louvain-la-Neuve, Belgium.

is a fungal pathogen causing economically important diseases on a variety of crops. Fungicides can be applied to control this species with triazoles being the most efficient molecules. strains resistant to these molecules have been reported, but the underlying resistance mechanisms remain unknown. In this study, a tebuconazole-adapted strain was developed with a level of fitness similar to its parental strain. The adapted strain showed cross-resistance to all demethylation inhibitors (DMIs), but not to other classes of fungicides tested. RNA-Seq analysis revealed high transcriptomic differences between the resistant strain and its parental strain after tebuconazole treatment. Among these changes, ABC1 (FCUL_06717), a pleiotropic drug resistance transporter, had a 30-fold higher expression level upon tebuconazole treatment in the adapted strains as compared to the wild-type strain. The implication of this transporter in triazole resistance was subsequently confirmed in field strains harboring distinct levels of sensitivity to triazoles. is present in other species/genera, including in which it is known to be necessary for azole resistance. No difference in sequences, including the surrounding regions, were found when comparing the resistant strain to the wild-type strain. is therefore capable to adapt to triazole pressure by overexpressing a drug resistance transporter when submitted to triazoles and the same mechanism is anticipated to occur in other species.
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http://dx.doi.org/10.3389/fmicb.2018.01385DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6028722PMC
June 2018

: A Viral Vector for Protein Expression in Cereals.

Plant Physiol 2018 08 7;177(4):1352-1367. Epub 2018 Jun 7.

Biointeractions and Crop Protection, Rothamsted Research, Harpenden AL5 2JQ, United Kingdom

Rapid and cost-effective virus-derived transient expression systems for plants are invaluable in elucidating gene function and are particularly useful in plant species for which transformation-based methods are unavailable or are too time and labor demanding, such as wheat () and maize (). The virus-mediated overexpression (VOX) vectors based on and described previously for these species are incapable of expressing free recombinant proteins of more than 150 to 250 amino acids, are not suited for high-throughput screens, and have other limitations. In this study, we report the development of a VOX vector based on a monopartite single-stranded positive sense RNA virus, (genus ). In this vector, PV101, the gene of interest was inserted downstream of the duplicated subgenomic promoter of the viral coat protein gene, and the corresponding protein was expressed in its free form. The vector allowed the expression of a 239-amino acid-long GFP in both virus-inoculated and upper uninoculated (systemic) leaves of wheat and maize and directed the systemic expression of a larger approximately 600-amino acid protein, GUSPlus, in maize. Moreover, we demonstrated that PV101 can be used for in planta expression and functional analysis of apoplastic pathogen effector proteins such as the host-specific toxin ToxA of Therefore, this VOX vector opens possibilities for functional genomics studies in two important cereal crops.
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http://dx.doi.org/10.1104/pp.17.01679DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6084670PMC
August 2018

Inter-genome comparison of the Quorn fungus Fusarium venenatum and the closely related plant infecting pathogen Fusarium graminearum.

BMC Genomics 2018 Apr 19;19(1):269. Epub 2018 Apr 19.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK.

Background: The soil dwelling saprotrophic non-pathogenic fungus Fusarium venenatum, routinely used in the commercial fermentation industry, is phylogenetically closely related to the globally important cereal and non-cereal infecting pathogen F. graminearum. This study aimed to sequence, assemble and annotate the F. venenatum (strain A3/5) genome, and compare this genome with F. graminearum.

Results: Using shotgun sequencing, a 38,660,329 bp F. venenatum genome was assembled into four chromosomes, and a 78,618 bp mitochondrial genome. In comparison to F. graminearum, the predicted gene count of 13,946 was slightly lower. The F. venenatum centromeres were found to be 25% smaller compared to F. graminearum. Chromosome length was 2.8% greater in F. venenatum, primarily due to an increased abundance of repetitive elements and transposons, but not transposon diversity. On chromosome 3 a major sequence rearrangement was found, but its overall gene content was relatively unchanged. Unlike homothallic F. graminearum, heterothallic F. venenatum possessed the MAT1-1 type locus, but lacked the MAT1-2 locus. The F. venenatum genome has the type A trichothecene mycotoxin TRI5 cluster, whereas F. graminearum has type B. From the F. venenatum gene set, 786 predicted proteins were species-specific versus NCBI. The annotated F. venenatum genome was predicted to possess more genes coding for hydrolytic enzymes and species-specific genes involved in the breakdown of polysaccharides than F. graminearum. Comparison of the two genomes reduced the previously defined F. graminearum-specific gene set from 741 to 692 genes. A comparison of the F. graminearum versus F. venenatum proteomes identified 15 putative secondary metabolite gene clusters (SMC), 109 secreted proteins and 38 candidate effectors not found in F. venenatum. Five of the 15 F. graminearum-specific SMCs that were either absent or highly divergent in the F. venenatum genome showed increased in planta expression. In addition, two predicted F. graminearum transcription factors previously shown to be required for fungal virulence on wheat plants were absent or exhibited high sequence divergence.

Conclusions: This study identifies differences between the F. venenatum and F. graminearum genomes that may contribute to contrasting lifestyles, and highlights the repertoire of F. graminearum-specific candidate genes and SMCs potentially required for pathogenesis.
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http://dx.doi.org/10.1186/s12864-018-4612-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5907747PMC
April 2018

Elite UK winter wheat cultivars differ in their ability to support the colonization of beneficial root-infecting fungi.

J Exp Bot 2018 05;69(12):3103-3115

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, Hertfordshire, UK.

In numerous countries, Gaeumannomyces species, within the Magnaporthaceae family, have previously been implicated in the suppression of take-all root disease in wheat. A UK arable isolate collection (n=47) was gathered and shown to contain Gaeumannomyces hyphopodioides and an unnamed Magnaporthaceae species. A novel seedling pot bioassay revealed that both species had a similar ability to colonize cereal roots; however, rye (Secale cereale) was only poorly colonized by the Magnaporthaceae species. To evaluate the ability of 40 elite UK winter wheat cultivars to support soil inoculum of beneficial soil-dwelling fungi, two field experiments were carried out using a naturally infested arable site in south-east England. The elite cultivars grown in the first wheat situation differed in their ability to support G. hyphopodioides inoculum, measured by colonization on Hereward as the subsequent wheat in a seedling soil core bioassay. In addition, the root colonization ability of G. hyphopodioides was influenced by the choice of the second wheat cultivar. Nine cultivars supported the colonization of the beneficial root fungus. Our findings provide evidence of complex host genotype-G. hyphopodioides interactions occurring under field conditions. This new knowledge could provide an additional soil-based crop genetic management strategy to help combat take-all root disease.
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http://dx.doi.org/10.1093/jxb/ery136DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5972604PMC
May 2018

Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici.

Nat Genet 2018 03 12;50(3):368-374. Epub 2018 Feb 12.

Biointeractions and Crop Protection, Rothamsted Research, Harpenden, UK.

Deployment of fast-evolving disease-resistance genes is one of the most successful strategies used by plants to fend off pathogens. In gene-for-gene relationships, most cloned disease-resistance genes encode intracellular nucleotide-binding leucine-rich-repeat proteins (NLRs) recognizing pathogen-secreted isolate-specific avirulence (Avr) effectors delivered to the host cytoplasm. This process often triggers a localized hypersensitive response, which halts further disease development . Here we report the map-based cloning of the wheat Stb6 gene and demonstrate that it encodes a conserved wall-associated receptor kinase (WAK)-like protein, which detects the presence of a matching apoplastic effector and confers pathogen resistance without a hypersensitive response . This report demonstrates gene-for-gene disease resistance controlled by this class of proteins in plants. Moreover, Stb6 is, to our knowledge, the first cloned gene specifying resistance to Zymoseptoria tritici, an important foliar fungal pathogen affecting wheat and causing economically damaging septoria tritici blotch (STB) disease.
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http://dx.doi.org/10.1038/s41588-018-0051-xDOI Listing
March 2018

Sharing mutants and experimental information prepublication using FgMutantDb (https://scabusa.org/FgMutantDb).

Fungal Genet Biol 2018 06 3;115:90-93. Epub 2018 Feb 3.

National Small Grains Germplasm Research Facility, USDA-ARS, Aberdeen, ID, United States.

There is no comprehensive storage for generated mutants of Fusarium graminearum or data associated with these mutants. Instead, researchers relied on several independent and non-integrated databases. FgMutantDb was designed as a simple spreadsheet that is accessible globally on the web that will function as a centralized source of information on F. graminearum mutants. FgMutantDb aids in the maintenance and sharing of mutants within a research community. It will serve also as a platform for disseminating prepublication results as well as negative results that often go unreported. Additionally, the highly curated information on mutants in FgMutantDb will be shared with other databases (FungiDB, Ensembl, PhytoPath, and PHI-base) through updating reports. Here we describe the creation and potential usefulness of FgMutantDb to the F. graminearum research community, and provide a tutorial on its use. This type of database could be easily emulated for other fungal species.
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http://dx.doi.org/10.1016/j.fgb.2018.01.002DOI Listing
June 2018

Ensembl Genomes 2018: an integrated omics infrastructure for non-vertebrate species.

Nucleic Acids Res 2018 01;46(D1):D802-D808

The European Molecular Biology Laboratory, The European Bioinformatics Institute, The Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SD, UK.

Ensembl Genomes (http://www.ensemblgenomes.org) is an integrating resource for genome-scale data from non-vertebrate species, complementing the resources for vertebrate genomics developed in the Ensembl project (http://www.ensembl.org). Together, the two resources provide a consistent set of programmatic and interactive interfaces to a rich range of data including genome sequence, gene models, transcript sequence, genetic variation, and comparative analysis. This paper provides an update to the previous publications about the resource, with a focus on recent developments and expansions. These include the incorporation of almost 20 000 additional genome sequences and over 35 000 tracks of RNA-Seq data, which have been aligned to genomic sequence and made available for visualization. Other advances since 2015 include the release of the database in Resource Description Framework (RDF) format, a large increase in community-derived curation, a new high-performance protein sequence search, additional cross-references, improved annotation of non-protein-coding genes, and the launch of pre-release and archival sites. Collectively, these changes are part of a continuing response to the increasing quantity of publicly-available genome-scale data, and the consequent need to archive, integrate, annotate and disseminate these using automated, scalable methods.
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http://dx.doi.org/10.1093/nar/gkx1011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5753204PMC
January 2018

A review of wheat diseases-a field perspective.

Mol Plant Pathol 2018 06 26;19(6):1523-1536. Epub 2017 Dec 26.

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.

Wheat is one of the primary staple foods throughout the planet. Significant yield gains in wheat production over the past 40 years have resulted in a steady balance of supply versus demand. However, predicted global population growth rates and dietary changes mean that substantial yield gains over the next several decades will be needed to meet this escalating demand. A key component to meeting this challenge is better management of fungal incited diseases, which can be responsible for 15%-20% yield losses per annum. Prominent diseases of wheat that currently contribute to these losses include the rusts, blotches and head blight/scab. Other recently emerged or relatively unnoticed diseases, such as wheat blast and spot blotch, respectively, also threaten grain production. This review seeks to provide an overview of the impact, distribution and management strategies of these diseases. In addition, the biology of the pathogens and the molecular basis of their interaction with wheat are discussed.
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http://dx.doi.org/10.1111/mpp.12618DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638159PMC
June 2018

RNAi as an emerging approach to control Fusarium head blight disease and mycotoxin contamination in cereals.

Pest Manag Sci 2018 Apr 22;74(4):790-799. Epub 2017 Nov 22.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, UK.

Fusarium graminearum is a major fungal pathogen of cereals worldwide, causing seedling, stem base and floral diseases, including Fusarium head blight (FHB). In addition to yield and quality losses, FHB contaminates cereal grain with mycotoxins, including deoxynivalenol, which are harmful to human, animal and ecosystem health. Currently, FHB control is only partially effective due to several intractable problems. RNA interference (RNAi) is a natural mechanism that regulates gene expression. RNAi has been exploited in the development of new genomic tools that allow the targeted silencing of genes of interest in many eukaryotes. Host-induced gene silencing (HIGS) is a transgenic technology used to silence fungal genes in planta during attempted infection and thereby reduces disease levels. HIGS relies on the host plant's ability to produce mobile small interfering RNA molecules, generated from long double-stranded RNA, which are complementary to targeted fungal genes. These molecules are transferred from the plant to invading fungi via an uncharacterised mechanism, to cause gene silencing. Here, we describe recent advances in RNAi-mediated control of plant pathogenic fungi, highlighting the key advantages and disadvantages. We then discuss the developments and implications of combining HIGS with other methods of disease control. © 2017 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
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http://dx.doi.org/10.1002/ps.4748DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5873435PMC
April 2018

A spatial temporal analysis of the Fusarium graminearum transcriptome during symptomless and symptomatic wheat infection.

Mol Plant Pathol 2017 12 8;18(9):1295-1312. Epub 2017 Aug 8.

Department of Biointeractions and Crop Protection, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.

Fusarium head blight of wheat is one of the most serious and hazardous crop diseases worldwide. Here, a transcriptomic investigation of Fusarium graminearum reveals a new model for symptomless and symptomatic wheat infection. The predicted metabolic state and secretome of F. graminearum were distinct within symptomless and symptomatic wheat tissues. Transcripts for genes involved in the biosynthesis of the mycotoxin, deoxynivalenol, plus other characterized and putative secondary metabolite clusters increased in abundance in symptomless tissue. Transcripts encoding for genes of distinct groups of putative secreted effectors increased within either symptomless or symptomatic tissue. Numerous pathogenicity-associated gene transcripts and transcripts representing PHI-base mutations that impacted on virulence increased in symptomless tissue. In contrast, hydrolytic carbohydrate-active enzyme (CAZyme) and lipase gene transcripts exhibited a different pattern of expression, resulting in elevated transcript abundance during the development of disease symptoms. Genome-wide comparisons with existing datasets confirmed that, within the wheat floral tissue, at a single time point, different phases of infection co-exist, which are spatially separated and reminiscent of both early and late infection. This study provides novel insights into the combined spatial temporal coordination of functionally characterized and hypothesized virulence strategies.
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http://dx.doi.org/10.1111/mpp.12564DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5697668PMC
December 2017

Annotation of Fusarium graminearum (PH-1) Version 5.0.

Genome Announc 2017 Jan 12;5(2). Epub 2017 Jan 12.

Rothamsted Research, Harpenden, Herts, United Kingdom.

Fusarium graminearum floral infections are a major risk to the global supply of safe cereal grains. We report updates to the PH-1 reference genome and significant improvements to the annotation. Changes include introduction of legacy annotation identifiers, new gene models, secretome and effectorP predictions, and inclusion of extensive untranslated region (UTR) annotations.
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http://dx.doi.org/10.1128/genomeA.01479-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5256205PMC
January 2017

PHI-base: a new interface and further additions for the multi-species pathogen-host interactions database.

Nucleic Acids Res 2017 01 3;45(D1):D604-D610. Epub 2016 Dec 3.

Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK

The pathogen-host interactions database (PHI-base) is available at www.phi-base.org PHI-base contains expertly curated molecular and biological information on genes proven to affect the outcome of pathogen-host interactions reported in peer reviewed research articles. In addition, literature that indicates specific gene alterations that did not affect the disease interaction phenotype are curated to provide complete datasets for comparative purposes. Viruses are not included. Here we describe a revised PHI-base Version 4 data platform with improved search, filtering and extended data display functions. A PHIB-BLAST search function is provided and a link to PHI-Canto, a tool for authors to directly curate their own published data into PHI-base. The new release of PHI-base Version 4.2 (October 2016) has an increased data content containing information from 2219 manually curated references. The data provide information on 4460 genes from 264 pathogens tested on 176 hosts in 8046 interactions. Prokaryotic and eukaryotic pathogens are represented in almost equal numbers. Host species belong ∼70% to plants and 30% to other species of medical and/or environmental importance. Additional data types included into PHI-base 4 are the direct targets of pathogen effector proteins in experimental and natural host organisms. The curation problems encountered and the future directions of the PHI-base project are briefly discussed.
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http://dx.doi.org/10.1093/nar/gkw1089DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5210566PMC
January 2017

Pseudomonas spp. diversity is negatively associated with suppression of the wheat take-all pathogen.

Sci Rep 2016 08 23;6:29905. Epub 2016 Aug 23.

Department of AgroEcology, Rothamsted Research, Harpenden, AL5 2JQ, UK.

Biodiversity and ecosystem functioning research typically shows positive diversity- productivity relationships. However, local increases in species richness can increase competition within trophic levels, reducing the efficacy of intertrophic level population control. Pseudomonas spp. are a dominant group of soil bacteria that play key roles in plant growth promotion and control of crop fungal pathogens. Here we show that Pseudomonas spp. richness is positively correlated with take-all disease in wheat and with yield losses of ~3 t/ha in the field. We modeled the interactions between Pseudomonas and the take-all pathogen in abstract experimental microcosms, and show that increased bacterial genotypic richness escalates bacterial antagonism and decreases the ability of the bacterial community to inhibit growth of the take-all pathogen. Future work is required to determine the generality of these negative biodiversity effects on different media and directly at infection zones on root surfaces. However, the increase in competition between bacteria at high genotypic richness and the potential loss of fungal biocontrol activity highlights an important mechanism to explain the negative Pseudomonas diversity-wheat yield relationship we observed in the field. Together our results suggest that the effect of biodiversity on ecosystem functioning can depend on both the function and trophic level of interest.
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http://dx.doi.org/10.1038/srep29905DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4993996PMC
August 2016

The genome of the emerging barley pathogen Ramularia collo-cygni.

BMC Genomics 2016 08 9;17:584. Epub 2016 Aug 9.

Crop Protection Team, Crop and Soil Systems Group, SRUC, West Mains Road, Edinburgh, EH9 3JG, UK.

Background: Ramularia collo-cygni is a newly important, foliar fungal pathogen of barley that causes the disease Ramularia leaf spot. The fungus exhibits a prolonged endophytic growth stage before switching life habit to become an aggressive, necrotrophic pathogen that causes significant losses to green leaf area and hence grain yield and quality.

Results: The R. collo-cygni genome was sequenced using a combination of Illumina and Roche 454 technologies. The draft assembly of 30.3 Mb contained 11,617 predicted gene models. Our phylogenomic analysis confirmed the classification of this ascomycete fungus within the family Mycosphaerellaceae, order Capnodiales of the class Dothideomycetes. A predicted secretome comprising 1053 proteins included redox-related enzymes and carbohydrate-modifying enzymes and proteases. The relative paucity of plant cell wall degrading enzyme genes may be associated with the stealth pathogenesis characteristic of plant pathogens from the Mycosphaerellaceae. A large number of genes associated with secondary metabolite production, including homologs of toxin biosynthesis genes found in other Dothideomycete plant pathogens, were identified.

Conclusions: The genome sequence of R. collo-cygni provides a framework for understanding the genetic basis of pathogenesis in this important emerging pathogen. The reduced complement of carbohydrate-degrading enzyme genes is likely to reflect a strategy to avoid detection by host defences during its prolonged asymptomatic growth. Of particular interest will be the analysis of R. collo-cygni gene expression during interactions with the host barley, to understand what triggers this fungus to switch from being a benign endophyte to an aggressive necrotroph.
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http://dx.doi.org/10.1186/s12864-016-2928-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4979122PMC
August 2016

Publishing FAIR Data: An Exemplar Methodology Utilizing PHI-Base.

Front Plant Sci 2016 12;7:641. Epub 2016 May 12.

Center for Plant Biotechnology and Genomics, Universidad Politécnica de Madrid Madrid, Spain.

Pathogen-Host interaction data is core to our understanding of disease processes and their molecular/genetic bases. Facile access to such core data is particularly important for the plant sciences, where individual genetic and phenotypic observations have the added complexity of being dispersed over a wide diversity of plant species vs. the relatively fewer host species of interest to biomedical researchers. Recently, an international initiative interested in scholarly data publishing proposed that all scientific data should be "FAIR"-Findable, Accessible, Interoperable, and Reusable. In this work, we describe the process of migrating a database of notable relevance to the plant sciences-the Pathogen-Host Interaction Database (PHI-base)-to a form that conforms to each of the FAIR Principles. We discuss the technical and architectural decisions, and the migration pathway, including observations of the difficulty and/or fidelity of each step. We examine how multiple FAIR principles can be addressed simultaneously through careful design decisions, including making data FAIR for both humans and machines with minimal duplication of effort. We note how FAIR data publishing involves more than data reformatting, requiring features beyond those exhibited by most life science Semantic Web or Linked Data resources. We explore the value-added by completing this FAIR data transformation, and then test the result through integrative questions that could not easily be asked over traditional Web-based data resources. Finally, we demonstrate the utility of providing explicit and reliable access to provenance information, which we argue enhances citation rates by encouraging and facilitating transparent scholarly reuse of these valuable data holdings.
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http://dx.doi.org/10.3389/fpls.2016.00641DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4922217PMC
July 2016

The trans-kingdom identification of negative regulators of pathogen hypervirulence.

FEMS Microbiol Rev 2016 Jan 13;40(1):19-40. Epub 2015 Oct 13.

Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK

Modern society and global ecosystems are increasingly under threat from pathogens, which cause a plethora of human, animal, invertebrate and plant diseases. Of increasing concern is the trans-kingdom tendency for increased pathogen virulence that is beginning to emerge in natural, clinical and agricultural settings. The study of pathogenicity has revealed multiple examples of convergently evolved virulence mechanisms. Originally described as rare, but increasingly common, are interactions where a single gene deletion in a pathogenic species causes hypervirulence. This review utilised the pathogen-host interaction database (www.PHI-base.org) to identify 112 hypervirulent mutations from 37 pathogen species, and subsequently interrogates the trans-kingdom, conserved, molecular, biochemical and cellular themes that cause hypervirulence. This study investigates 22 animal and 15 plant pathogens including 17 bacterial and 17 fungal species. Finally, the evolutionary significance and trans-kingdom requirement for negative regulators of hypervirulence and the implication of pathogen hypervirulence and emerging infectious diseases on society are discussed.
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http://dx.doi.org/10.1093/femsre/fuv042DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4703069PMC
January 2016

Host to a Stranger: Arabidopsis and Fusarium Ear Blight.

Trends Plant Sci 2015 Oct;20(10):651-663

Plant Biology and Crop Science, Rothamsted Research, Harpenden AL5 2JQ, UK. Electronic address:

Fusarium ear blight (FEB) is a devastating fungal disease of cereal crops. Outbreaks are sporadic and current control strategies are severely limited. This review highlights the use of Arabidopsis to study plant-FEB interactions. Use of this pathosystem has identified natural variation in Fusarium susceptibility in Arabidopsis, and native plant genes and signalling processes modulating the interaction. Recent breakthroughs include the identification of plant- and insect-derived small molecules which increase disease resistance, and the use of a host-induced gene silencing (HIGS) construct to silence an important Fusarium gene to prevent infection. Arabidopsis has also been used to study other fungi that cause cereal diseases. These findings offer the potential for translational research in cereals which could yield much-needed novel control strategies.
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http://dx.doi.org/10.1016/j.tplants.2015.06.011DOI Listing
October 2015

Using the pathogen-host interactions database (PHI-base) to investigate plant pathogen genomes and genes implicated in virulence.

Front Plant Sci 2015 6;6:605. Epub 2015 Aug 6.

Department of Plant Biology and Crop Science, Rothamsted Research Harpenden, UK.

New pathogen-host interaction mechanisms can be revealed by integrating mutant phenotype data with genetic information. PHI-base is a multi-species manually curated database combining peer-reviewed published phenotype data from plant and animal pathogens and gene/protein information in a single database.
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http://dx.doi.org/10.3389/fpls.2015.00605DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4526803PMC
August 2015

The completed genome sequence of the pathogenic ascomycete fungus Fusarium graminearum.

BMC Genomics 2015 Jul 22;16:544. Epub 2015 Jul 22.

Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK.

Background: Accurate genome assembly and gene model annotation are critical for comparative species and gene functional analyses. Here we present the completed genome sequence and annotation of the reference strain PH-1 of Fusarium graminearum, the causal agent of head scab disease of small grain cereals which threatens global food security. Completion was achieved by combining (a) the BROAD Sanger sequenced draft, with (b) the gene predictions from Munich Information Services for Protein Sequences (MIPS) v3.2, with (c) de novo whole-genome shotgun re-sequencing, (d) re-annotation of the gene models using RNA-seq evidence and Fgenesh, Snap, GeneMark and Augustus prediction algorithms, followed by (e) manual curation.

Results: We have comprehensively completed the genomic 36,563,796 bp sequence by replacing unknown bases, placing supercontigs within their correct loci, correcting assembly errors, and inserting new sequences which include for the first time complete AT rich sequences such as centromere sequences, subtelomeric regions and the telomeres. Each of the four F. graminearium chromosomes was found to be submetacentric with respect to centromere positioning. The position of a potential neocentromere was also defined. A preferentially higher frequency of genetic recombination was observed at the end of the longer arm of each chromosome. Within the genome 1529 gene models have been modified and 412 new gene models predicted, with a total gene call of 14,164. The re-annotation impacts upon 69 entries held within the Pathogen-Host Interactions database (PHI-base) which stores information on genes for which mutant phenotypes in pathogen-host interactions have been experimentally tested, of which 59 are putative transcription factors, 8 kinases, 1 ATP citrate lyase (ACL1), and 1 syntaxin-like SNARE gene (GzSYN1). Although the completed F. graminearum contains very few transposon sequences, a previously unrecognised and potentially active gypsy-type long-terminal-repeat (LTR) retrotransposon was identified. In addition, each of the sub-telomeres and centromeres contained either a LTR or MarCry-1_FO element. The full content of the proposed ancient chromosome fusion sites has also been revealed and investigated. Regions with high recombination previously noted to be rich in secretome encoding genes were also found to be rich in tRNA sequences. This study has identified 741 F. graminearum species specific genes and provides the first complete genome assembly for a Sordariomycetes species.

Conclusions: This fully completed F. graminearum PH-1 genome and manually curated annotation, available at Ensembl Fungi, provides the optimum resource to perform interspecies comparative analyses and gene function studies.
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http://dx.doi.org/10.1186/s12864-015-1756-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4511438PMC
July 2015

Whole-genome analysis of Fusarium graminearum insertional mutants identifies virulence associated genes and unmasks untagged chromosomal deletions.

BMC Genomics 2015 Apr 3;16:261. Epub 2015 Apr 3.

Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK.

Background: Identifying pathogen virulence genes required to cause disease is crucial to understand the mechanisms underlying the pathogenic process. Plasmid insertion mutagenesis of fungal protoplasts is frequently used for this purpose in filamentous ascomycetes. Post transformation, the mutant population is screened for loss of virulence to a specific plant or animal host. Identifying the insertion event has previously met with varying degrees of success, from a cleanly disrupted gene with minimal deletion of nucleotides at the insertion point to multiple-copy insertion events and large deletions of chromosomal regions. Currently, extensive mutant collections exist in laboratories globally where it was hitherto impossible to identify all the affected genes.

Results: We used a whole-genome sequencing (WGS) approach using Illumina HiSeq 2000 technology to investigate DNA tag insertion points and chromosomal deletion events in mutagenised, reduced virulence F. graminearum isolates identified in disease tests on wheat (Triticum aestivum). We developed the FindInsertSeq workflow to localise the DNA tag insertions to the nucleotide level. The workflow was tested using four mutants showing evidence of single and multi-copy insertions in DNA blot analysis. FindInsertSeq was able to identify both single and multi-copy concatenation insertion sites. By comparing sequencing coverage, unexpected molecular recombination events such as large tagged and untagged chromosomal deletions, and DNA amplification were observed in three of the analysed mutants. A random data sampling approach revealed the minimum genome coverage required to survey the F. graminearum genome for alterations.

Conclusions: This study demonstrates that whole-genome re-sequencing to 22x fold genome coverage is an efficient tool to characterise single and multi-copy insertion mutants in the filamentous ascomycete Fusarium graminearum. In some cases insertion events are accompanied with large untagged chromosomal deletions while in other cases a straight-forward insertion event could be confirmed. The FindInsertSeq analysis workflow presented in this study enables researchers to efficiently characterise insertion and deletion mutants.
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http://dx.doi.org/10.1186/s12864-015-1412-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4404607PMC
April 2015