skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Comparative Genomics of a Plant-Pathogenic Fungus, Pyrenophora tritici-repentis, Reveals Transduplication and the Impact of Repeat Elements on Pathogenicity and Population Divergence

Journal Article · · G3

Pyrenophora tritici-repentis is a necrotrophic fungus causal to the disease tan spot of wheat, whose contribution to crop loss has increased significantly during the last few decades. Pathogenicity by this fungus is attributed to the production of host-selective toxins (HST), which are recognized by their host in a genotype-specific manner. To better understand the mechanisms that have led to the increase in disease incidence related to this pathogen, we sequenced the genomes of three P. tritici-repentis isolates. A pathogenic isolate that produces two known HSTs was used to assemble a reference nuclear genome of approximately 40 Mb composed of 11 chromosomes that encode 12,141 predicted genes. Comparison of the reference genome with those of a pathogenic isolate that produces a third HST, and a nonpathogenic isolate, showed the nonpathogen genome to be more diverged than those of the two pathogens. Examination of gene-coding regions has provided candidate pathogen-specific proteins and revealed gene families that may play a role in a necrotrophic lifestyle. Analysis of transposable elements suggests that their presence in the genome of pathogenic isolates contributes to the creation of novel genes, effector diversification, possible horizontal gene transfer events, identified copy number variation, and the first example of transduplication by DNA transposable elements in fungi. Overall, comparative analysis of these genomes provides evidence that pathogenicity in this species arose through an influx of transposable elements, which created a genetically flexible landscape that can easily respond to environmental changes.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
DOE Contract Number:
AC02-05CH11231
OSTI ID:
1165998
Report Number(s):
LBNL-6824E
Journal Information:
G3, Vol. 3, Issue 1; ISSN 2160-1836
Publisher:
Genetics Society of America
Country of Publication:
United States
Language:
English

References (169)

ProtTest: selection of best-fit models of protein evolution journal January 2005
Genome characterization of Pyrenophora tritici-repentis isolates reveals high plasticity and independent chromosomal location of ToxA and ToxB journal March 2009
Simple sequence repeats and diversity of globally distributed populations of Pyrenophora tritici-repentis journal July 2011
RNA-mediated gene silencing of ToxB in Pyrenophora tritici-repentis: Silencing of ToxB journal October 2011
Population Race Structure of Pyrenophora tritici-repentis Prevalent on Wheat and Noncereal Grasses in the Great Plains journal April 2003
Identification and Characterization of Novel Isolates of Pyrenophora tritici-repentis from Arkansas journal February 2010
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs journal September 1997
Quantification of ToxB gene expression and formation of appressoria by isolates of Pyrenophora tritici-repentis differing in pathogenicity journal August 2008
Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea journal August 2011
Pyrenophora bromi , Causal Agent of Brownspot of Bromegrass, Expresses a Gene Encoding a Protein with Homology and Similar Activity to Ptr ToxB, a Host-Selective Toxin of Wheat journal March 2011
A Combination of Phenotypic and Genotypic Characterization Strengthens Pyrenophora tritici-repentis Race Identification journal June 2007
Homologs of ToxB, a host-selective toxin gene from Pyrenophora tritici-repentis, are present in the genome of sister-species Pyrenophora bromi and other members of the Ascomycota journal March 2008
Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici - repentis journal January 2010
Transcriptional regulation of plant cell wall degradation by filamentous fungi journal September 2005
Diseases under conservation tillage systems journal October 1996
Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis journal September 1989
Automated De Novo Identification of Repeat Sequence Families in Sequenced Genomes journal July 2002
Transposable element contributions to plant gene and genome evolution journal January 2000
Effects of Crop Rotation and Residue Management Practices on Severity of Tan Spot of Winter Wheat journal January 1992
The Impact of Reduced Tillage on Soilborne Plant Pathogens journal September 1998
Chromatin-level regulation of biosynthetic gene clusters journal May 2009
Influence of carbon source on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat journal October 2010
Influence of water activity and temperature on growth and mycotoxin production by isolates of Pyrenophora tritici-repentis from wheat journal May 2009
Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships journal January 2010
Repeat-induced G-C to A-T mutations in Neurospora journal June 1989
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal January 2009
A proteomic evaluation of Pyrenophora tritici-repentis, causal agent of tan spot of wheat, reveals major differences between virulent and avirulent isolates journal March 2009
Tobacco Nectarin V Is a Flavin-Containing Berberine Bridge Enzyme-Like Protein with Glucose Oxidase Activity journal January 2004
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis journal April 2000
GMC oxidoreductases journal February 1992
Advances in the Characterization of the Pyrenophora tritici-repentis —Wheat Interaction journal June 1999
A single gene encodes a selective toxin causal to the development of tan spot of wheat. journal February 1997
Standardization of toxin nomenclature in the Pyrenophora tritici-repentis /wheat interaction journal December 1998
Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction: Research review journal July 2010
Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes journal March 2011
Chromosome evolution in eukaryotes: a multi-kingdom perspective journal December 2005
The Genome of Nectria haematococca: Contribution of Supernumerary Chromosomes to Gene Expansion journal August 2009
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research journal August 2005
Insights into the pathogenicity of Penicillium marneffei journal February 2008
The Fusarium graminearum Genome Reveals a Link Between Localized Polymorphism and Pathogen Specialization journal September 2007
Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence journal July 2004
Fungal transposable elements and genome evolution journal January 1997
Transposable Elements in Filamentous Fungi journal October 2003
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement journal June 2010
Aspergillus Enzymes Involved in Degradation of Plant Cell Wall Polysaccharides journal December 2001
Vistas of tan spot research journal December 1998
The genome sequence of the rice blast fungus Magnaporthe grisea journal April 2005
Engineering evolution to study speciation in yeasts journal March 2003
A Microfluidic System for Large DNA Molecule Arrays journal September 2004
Molecular cloning, expression, and induction of berberine bridge enzyme, an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack. journal November 1991
Obligate biotrophy features unraveled by the genomic analysis of rust fungi journal May 2011
Detection of infection and host responses in susceptible and resistant wheat cultivars to a toxin-producing isolate of Pyrenophora tritici-repentis journal March 1998
The role of lignification as a resistance mechanism in wheat to a toxin-producing isolate of Pyrenophora tritici-repentis journal March 1998
Improved Prediction of Signal Peptides: SignalP 3.0 journal July 2004
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Identification of a Chlorosis-Inducing Toxin from Pyrenophora tritici-repentis and the Chromosomal Location of an Insensitivity Locus in Wheat journal May 2002
A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres journal November 2010
An efficient algorithm for large-scale detection of protein families journal April 2002
Molecular Characterization of Berberine Bridge Enzyme Genes from Opium Poppy journal December 1996
A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens journal July 2010
The importance of the N-terminus for activity of Ptr ToxB, a chlorosis-inducing host-selective toxin produced by Pyrenophora tritici-repentis journal April 2011
The Pfam protein families database journal November 2009
HMMER web server: interactive sequence similarity searching journal May 2011
A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa journal June 2002
Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat journal July 2004
Characterization of the wheat- Stagonospora nodorum disease system: what is the molecular basis of this quantitative necrotrophic disease interaction? journal March 2010
Population Genetic Analysis of a Global Collection of Pyrenophora tritici-repentis , Causal Agent of Tan Spot of Wheat journal October 2005
Emergence of a new disease as a result of interspecific virulence gene transfer journal July 2006
An Iterative Type I Polyketide Synthase PKSN Catalyzes Synthesis of the Decaketide Alternapyrone with Regio-Specific Octa-Methylation journal December 2005
Inheritance of race-specific necrotic and chlorotic reactions induced by Pyrenophora tritici-repentis in hexaploid wheats journal December 1998
Host shifts in fungi caused by climate change? journal April 2011
The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans journal July 2004
Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis journal June 2011
Self versus non-self: fungal cell wall degradation in Trichoderma journal January 2012
Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans journal September 2009
The Functional Role of Pack-MULEs in Rice Inferred from Purifying Selection and Expression Profile journal January 2009
RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences journal November 2008
Dothideomycete–Plant Interactions Illuminated by Genome Sequencing and EST Analysis of the Wheat Pathogen Stagonospora nodorum journal November 2007
Fungal chitinases: diversity, mechanistic properties and biotechnological potential journal December 2011
Transposon-Mediated Expansion and Diversification of a Family of ULP-like Genes journal April 2006
WoLF PSORT: protein localization predictor journal May 2007
Whole-Genome Sequence Assembly for Mammalian Genomes: Arachne 2 journal January 2003
Pack-MULE transposable elements mediate gene evolution in plants journal September 2004
Amplification generates modular diversity at an avirulence locus in the pathogen Phytophthora journal July 2006
Functional characterization and manipulation of the apicidin biosynthetic pathway in Fusarium semitectum journal April 2010
Cloning and Characterization of a Cyclic Peptide Synthetase Gene from Alternaria alternata Apple Pathotype Whose Product Is Involved in AM-Toxin Synthesis and Pathogenicity journal July 2000
The evolutionary fate of MULE-mediated duplications of host gene fragments in rice journal August 2005
Horizontal gene transfer in eukaryotic evolution journal August 2008
BLAT---The BLAST-Like Alignment Tool journal March 2002
Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae: Transcription factor of Bipolaris melanin regulation journal April 2008
Mutational Analysis of β-Glucanase Genes from the Plant-Pathogenic Fungus Cochliobolus carbonum journal December 2001
Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens journal July 2011
Observations on the host range of isolates of Pyrenophora trichostoma journal March 1982
A new method to compute K-mer frequencies and its application to annotate large repetitive plant genomes journal January 2008
Activity of Ptr ToxA fromPyrenophora tritici-repentisrequires host metabolism journal March 1998
Genetics of Tan Necrosis and Extensive Chlorosis in Tan Spot of Wheat Caused by Pyrenophora tritici-repentis journal January 1991
Minireview/ Minisynthèse The wheat/ Pyrenophora tritici-repentis interaction: progress towards an understanding of tan spot disease journal March 2010
The Identification of Two New Races of Pyrenophora tritici-repentis from the Host Center of Diversity Confirms a One-to-One Relationship in Tan Spot of Wheat journal April 2003
Virulence of Pyrenophora tritici-repentis in the countries of the Silk Road journal September 2005
The variability of a Pyrenophora tritici-repentis population as revealed by inter-retrotransposon amplified polymorphism with regard to the Ptr ToxA gene. journal January 2010
Genetic Diversity of the Mating Type and Toxin Production Genes in Pyrenophora tritici-repentis journal May 2010
Mapping short DNA sequencing reads and calling variants using mapping quality scores journal November 2008
SOAP2: an improved ultrafast tool for short read alignment journal June 2009
Chromosome-based molecular characterization of pathogenic and non-pathogenic wheat isolates of Pyrenophora tritici-repentis journal November 2002
Whole-Genome Shotgun Optical Mapping of Deinococcus radiodurans journal September 1999
Pyrenophora teres: profile of an increasingly damaging barley pathogen: Pathogen profile of Pyrenophora teres journal December 2010
The genome of the protist parasite Entamoeba histolytica journal February 2005
Construction of subtractive cDNA library using magnetic beads and PCR. journal February 1995
Green Fluorescent Protein Is Lighting Up Fungal Biology journal May 2001
Real-Time Quantitative Expression Studies of the Zearalenone Biosynthetic Gene Cluster in Fusarium graminearum journal February 2009
Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium journal March 2010
A gene from the fungal plant pathogen Nectria haematococca that encodes the phytoalexin-detoxifying enzyme pisatin demethylase defines a new cytochrome P450 family journal September 1994
Localization of Ptr ToxA Produced by Pyrenophora tritici-repentis Reveals Protein Import into Wheat Mesophyll Cells journal September 2005
The Arg-Gly-Asp–Containing, Solvent-Exposed Loop of Ptr ToxA Is Required for Internalization journal March 2008
A Host-Selective Toxin of Pyrenophora tritici-repentis , Ptr ToxA, Induces Photosystem Changes and Reactive Oxygen Species Accumulation in Sensitive Wheat journal June 2009
Host-selective toxins as agents of cell death in plant-fungus interactions journal July 2001
Characterization of the ToxB Gene from Pyrenophora tritici-repentis journal May 2001
Characterization of the Multiple-Copy Host-Selective Toxin Gene, ToxB , in Pathogenic and Nonpathogenic Isolates of Pyrenophora tritici-repentis journal May 2004
Generation and utilization of chemical-resistant mutants in Pyrenophora tritici-repentis , the causal agent of tan spot of wheat journal January 1994
Review of the epidemiology and economic importance of Pyrenophora semeniperda journal January 2003
Pathogenic and molecular variability among isolates of Pyrenophora tritici-repentis, causal agent of tan spot of wheat in Argentina journal February 2008
Estimating disease losses to the Australian wheat industry journal January 2009
A general method applicable to the search for similarities in the amino acid sequence of two proteins journal March 1970
New developments in pathogenicity and virulence of necrotrophs journal August 2010
Analysis of Transcriptome Changes Induced by Ptr ToxA in Wheat Provides Insights into the Mechanisms of Plant Susceptibility journal September 2009
Host-Selective Toxins of Pyrenophora tritici-repentis Induce Common Responses Associated with Host Susceptibility journal July 2012
Foreword: Integrated plant disease management journal February 2012
Intraspecific genetic diversity of Drechslera tritici-repentis as detected by random amplified polymorphic DNA analysis journal January 2002
Copy Number Variation and Transcriptional Polymorphisms of Phytophthora sojae RXLR Effector Genes Avr1a and Avr3a journal April 2009
Genome evolution in filamentous plant pathogens: why bigger can be better journal May 2012
Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans journal January 2010
Requirement of Host Signaling Mechanisms for the Action of Ptr ToxA in Wheat journal March 2004
The epidemiology of yellow spot of wheat in southern Queensland journal January 1980
Genes for the Biosynthesis of the Fungal Polyketides Hypothemycin from Hypomyces subiculosus and Radicicol from Pochonia chlamydosporia journal June 2008
Small proteins of plant-pathogenic fungi secreted during host colonization journal December 2005
EMBOSS: The European Molecular Biology Open Software Suite journal June 2000
A phylogenomic analysis of the Ascomycota journal October 2006
Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations journal February 2011
Structure of Ptr ToxA: An RGD-Containing Host-Selective Toxin from Pyrenophora tritici-repentis journal October 2005
A multigene phylogeny of the Dothideomycetes using four nuclear loci journal November 2006
A class-wide phylogenetic assessment of Dothideomycetes journal January 2009
The Ascomycota Tree of Life: A Phylum-wide Phylogeny Clarifies the Origin and Evolution of Fundamental Reproductive and Ecological Traits journal April 2009
Multimodular biocatalysts for natural product assembly journal April 2001
Rearrangement of duplicated DNA in specialized cells of Neurospora journal December 1987
Genetic Similarity among Isolates of Pyrenophora tritici-repentis, Causal Agent of Tan Spot of Wheat journal March 2006
Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism journal December 2010
A five-gene phylogeny of Pezizomycotina journal November 2006
Characterization and Disruption of A Gene in the Maize Pathogen Cochliobolus carbonum Encoding a Cellulase Lacking a Cellulose Binding Domain and Hinge Region journal January 1995
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
Fungal Effector Proteins journal September 2009
Host–parasite interactions in tan spot [ Pyrenophora tritici-repentis ] of wheat journal December 2003
Characterization of a Host-Specific Protein Toxin (Ptr ToxB) from Pyrenophora tritici-repentis journal August 1999
Comparative virulence of chlorosis-inducing races of Pyrenophora tritici-repentis journal March 2002
Geographical variation and positive diversifying selection in the host-specific toxin SnToxA journal May 2007
The Origins of Plant Pathogens in Agro-Ecosystems journal September 2008
Crop sequences and tillage practices in relation to diseases of winter wheat in Ontario journal December 1990
Reduction of quinones and phenoxy radicals by extracellular glucose dehydrogenase from Glomerella cingulata suggests a role in plant pathogenicity journal November 2011
Proteinaceous necrotrophic effectors in fungal virulence journal January 2010
Cultivar-Specific Toxicity of Culture Filtrates of Pyrenophora tritici-repentis journal January 1987
Purification of a Cultivar-Specific Toxin from Pyrenophora tritici-repentis, Causal Agent of Tan Spot of Wheat journal January 1990
Purification and Immunological Characterization of Toxic Components from Cultures of Pyrenophora tritici-repentis journal January 1995
Creating and screening Cochliobolus heterostrophus non-ribosomal peptide synthetase mutants journal February 2008
A functional genomics approach to dissect the mode of action of the Stagonospora nodorum effector protein SnToxA in wheat: SnToxA mode of action journal November 2011
Unique aspects of the grass cell wall journal June 2008
HC-toxin journal July 2006
H OST -S ELECTIVE T OXINS AND A VIRULENCE D ETERMINANTS : What's in a Name? journal September 2002
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs journal February 2008
Chapter 9 A Single Molecule System for Whole Genome Analysis book January 2007
A Single Molecule Scaffold for the Maize Genome journal November 2009