Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella graminicola

Wittenberg, Alexander H.  J.; van der Lee, Theo A.  J.; Ben M'Barek, Sarrah; Ware, Sarah B.; Goodwin, Stephen B.; Kilian, Andrzej; Visser, Richard G.  F.; Kema, Gert H.  J.; Schouten, Henk J.

doi:10.1371/journal.pone.0005863

Title: Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella graminicola

Journal Article · 10 June 2009 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0005863 · OSTI ID:1627374

Wittenberg, Alexander H. J. ^[1]; van der Lee, Theo A. J. ^[2]; Ben M'Barek, Sarrah ^[3]; Ware, Sarah B. ^[3]; Goodwin, Stephen B. ^[4]; Kilian, Andrzej ^[5]; Visser, Richard G. F. ^[6]; Kema, Gert H. J. ^[2]; Schouten, Henk J. ^[2]

Wageningen Univ. (Netherlands). Research Centre. Plant Research International B.V.; Wageningen Univ. (Netherlands). Dept. of Plant Sciences. Lab. of Plant Breeding. Graduate School of Experimental Plant Sciences; DOE/OSTI
Wageningen Univ. (Netherlands). Research Centre. Plant Research International B.V.
Wageningen Univ. (Netherlands). Research Centre. Plant Research International B.V.; Wageningen Univ. (Netherlands). Research Centre. Dept. of Plant Sciences. Lab. of Phytopathology. Graduate School Experimental Plant Sciences
Purdue Univ., West Lafayette, IN (United States). U.S. Dept. of Agriculture (USDA). Agricultural Research Service (ARS). Crop Production and Pest Control Research Unit. Dept. of Botany and Plant Pathology
Diversity Arrays P/L, Yarralumla, Canberra, Australian Capital Territory (Australia)
Wageningen Univ. (Netherlands). Research Centre. Plant Research International B.V.; Wageningen Univ. (Netherlands). Dept. of Plant Sciences. Lab. of Plant Breeding. Graduate School of Experimental Plant Sciences

Meiosis in the haploid plant-pathogenic fungus Mycosphaerella graminicola results in eight ascospores due to a mitotic division following the two meiotic divisions. The transient diploid phase allows for recombination among homologous chromosomes. However, some chromosomes of M. graminicola lack homologs and do not pair during meiosis. Because these chromosomes are not present universally in the genome of the organism they can be considered to be dispensable. To analyze the meiotic transmission of unequal chromosome numbers, two segregating populations were generated by crossing genetically unrelated parent isolates originating from Algeria and The Netherlands that had pathogenicity towards durum or bread wheat, respectively. Detailed genetic analyses of these progenies using high-density mapping (1793 DArT, 258 AFLP and 25 SSR markers) and graphical genotyping revealed that M. graminicola has up to eight dispensable chromosomes, the highest number reported in filamentous fungi. These chromosomes vary from 0.39 to 0.77 Mb in size, and represent up to 38% of the chromosomal complement. Chromosome numbers among progeny isolates varied widely, with some progeny missing up to three chromosomes, while other strains were disomic for one or more chromosomes. Between 15–20% of the progeny isolates lacked one or more chromosomes that were present in both parents. The two high-density maps showed no recombination of dispensable chromosomes and hence, their meiotic processing may require distributive disjunction, a phenomenon that is rarely observed in fungi. The maps also enabled the identification of individual twin isolates from a single ascus that shared the same missing or doubled chromosomes indicating that the chromosomal polymorphisms were mitotically stable and originated from nondisjunction during the second division and, less frequently, during the first division of fungal meiosis. High genome plasticity could be among the strategies enabling this versatile pathogen to quickly overcome adverse biotic and abiotic conditions in wheat fields.

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Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

OSTI ID:: 1627374

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 6 Vol. 4; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

Use of Molecular Cytology to Study the Structure and Biology of Phytopathogenic and Mycorrhizal Fungi Hardham, Adrienne R.; Mitchell, Heidi J. Fungal Genetics and Biology, Vol. 24, Issue 1-2 https://doi.org/10.1006/fgbi.1998.1055	journal	June 1998
Neurospora at the Millennium Perkins, David D.; Davis, Rowland H. Fungal Genetics and Biology, Vol. 31, Issue 3 https://doi.org/10.1006/fgbi.2000.1248	journal	December 2000
Isolation and Characterization of Sexual Sporulation Mutants of Aspergillus nidulans Swart, Klaas; van Heemst, Diana; Slakhorst, Marijke Fungal Genetics and Biology, Vol. 33, Issue 1 https://doi.org/10.1006/fgbi.2001.1266	journal	June 2001
Location of pathogenicity genes on dispensable chromosomes inNectria haematococca MPVI VanEtten, Hans; Funnell-Baerg, Deanna; Wasmann, Catherine Antonie van Leeuwenhoek, Vol. 65, Issue 3 https://doi.org/10.1007/bf00871955	journal	January 1994
Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome Akbari, Mona; Wenzl, Peter; Caig, Vanessa Theoretical and Applied Genetics, Vol. 113, Issue 8 https://doi.org/10.1007/s00122-006-0365-4	journal	October 2006
Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae Chuma, I.; Tosa, Y.; Taga, M. Current Genetics, Vol. 43, Issue 3 https://doi.org/10.1007/s00294-003-0390-7	journal	March 2003
Successful crosses and molecular tetrad and progeny analyses demonstrate heterothallism in Mycosphaerella graminicola Kema, G. H. J.; Verstappen, E. C. P.; Todorova, Maria Current Genetics, Vol. 30, Issue 3 https://doi.org/10.1007/s002940050129	journal	August 1996
Meiotic behaviour of the minichromosome in the phytopathogenic ascomycete Leptosphaeria maculans Leclair, S.; Ansan-Melayah, D.; Rouxel, T. Current Genetics, Vol. 30, Issue 6 https://doi.org/10.1007/s002940050167	journal	December 1996
Sherlock Holmes, David Perkins, and the missing Neurospora inversions Kasbekar, Durgadas P. Journal of Biosciences, Vol. 42, Issue 1 https://doi.org/10.1007/s12038-017-9674-9	journal	February 2017
Identification and genetic mapping of highly polymorphic microsatellite loci from an EST database of the septoria tritici blotch pathogen Mycosphaerella graminicola Goodwin, Stephen B.; van der Lee, Theo A. J.; Cavaletto, Jessica R. Fungal Genetics and Biology, Vol. 44, Issue 5 https://doi.org/10.1016/j.fgb.2006.09.004	journal	May 2007
Concurrence of losing a chromosome and the ability to produce destruxins in a mutant ofMetarhizium anisopliae Wang, Chengshu; Skrobek, Anke; Butt, Tariq M. FEMS Microbiology Letters, Vol. 226, Issue 2 https://doi.org/10.1016/s0378-1097(03)00640-2	journal	September 2003
The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow Zhan, J.; Pettway, R. E.; McDonald, B. A. Fungal Genetics and Biology, Vol. 38, Issue 3 https://doi.org/10.1016/s1087-1845(02)00538-8	journal	April 2003
The genome sequence of the rice blast fungus Magnaporthe grisea Dean, Ralph A.; Talbot, Nicholas J.; Ebbole, Daniel J. Nature, Vol. 434, Issue 7036 https://doi.org/10.1038/nature03449	journal	April 2005
Genome instability: a mechanistic view of its causes and consequences Aguilera, Andrés; Gómez-González, Belén Nature Reviews Genetics, Vol. 9, Issue 3 https://doi.org/10.1038/nrg2268	journal	March 2008
Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments Koszul, Romain; Caburet, Sandrine; Dujon, Bernard The EMBO Journal, Vol. 23, Issue 1 https://doi.org/10.1038/sj.emboj.7600024	journal	December 2003
Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps Hackett, C. A.; Broadfoot, L. B. Heredity, Vol. 90, Issue 1 https://doi.org/10.1038/sj.hdy.6800173	journal	January 2003
Diversity Arrays Technology (DArT) for whole-genome profiling of barley Wenzl, Peter; Carling, Jason; Kudrna, David Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0401076101	journal	June 2004
Physical association between nonhomologous chromosomes precedes distributive disjunction in yeast. Loidl, J.; Scherthan, H.; Kaback, D. B. Proceedings of the National Academy of Sciences, Vol. 91, Issue 1 https://doi.org/10.1073/pnas.91.1.331	journal	January 1994
Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Guacci, V.; Kaback, D. B. Genetics, Vol. 127, Issue 3 https://doi.org/10.1093/genetics/127.3.475	journal	March 1991
A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. Tzeng, T. H.; Lyngholm, L. K.; Ford, C. F. Genetics, Vol. 130, Issue 1 https://doi.org/10.1093/genetics/130.1.81	journal	January 1992
Genetic and physical mapping of telomeres in the rice blast fungus, Magnaporthe grisea. Farman, M. L.; Leong, S. A. Genetics, Vol. 140, Issue 2 https://doi.org/10.1093/genetics/140.2.479	journal	June 1995
Sexual Reproduction Plays a Major Role in the Genetic Structure of Populations of the Fungus Mycosphaerella graminicola Chen, Ruey-Shyang; McDonald, Bruce A. Genetics, Vol. 142, Issue 4 https://doi.org/10.1093/genetics/142.4.1119	journal	April 1996
A Conditionally Dispensable Chromosome Controls Host-Specific Pathogenicity in the Fungal Plant Pathogen Alternaria alternata Hatta, Rieko; Ito, Kaoru; Hosaki, Yoshitsugu Genetics, Vol. 161, Issue 1 https://doi.org/10.1093/genetics/161.1.59	journal	May 2002
A Combined Amplified Fragment Length Polymorphism and Randomly Amplified Polymorphism DNA Genetic Linkage Map of Mycosphaerella graminicola, the Septoria Tritici Leaf Blotch Pathogen of Wheat Kema, Gert H. J.; Goodwin, Stephen B.; Hamza, Sonia Genetics, Vol. 161, Issue 4 https://doi.org/10.1093/genetics/161.4.1497	journal	August 2002
A Mutant Affecting Meiosis in Neurospora Smith, David A. Genetics, Vol. 80, Issue 1 https://doi.org/10.1093/genetics/80.1.125	journal	May 1975
MapChart: Software for the Graphical Presentation of Linkage Maps and QTLs Voorrips, R. E. Journal of Heredity, Vol. 93, Issue 1 https://doi.org/10.1093/jhered/93.1.77	journal	January 2002
Origin and Domestication of the Fungal Wheat Pathogen Mycosphaerella graminicola via Sympatric Speciation Stukenbrock, E. H.; Banke, S.; Javan-Nikkhah, M. Molecular Biology and Evolution, Vol. 24, Issue 2 https://doi.org/10.1093/molbev/msl169	journal	November 2006
Diversity Arrays: a solid state technology for sequence information independent genotyping Jaccoud, D. Nucleic Acids Research, Vol. 29, Issue 4 https://doi.org/10.1093/nar/29.4.e25	journal	February 2001
Loss of meiosis in Aspergillus Geiser, D. M.; Timberlake, W. E.; Arnold, M. L. Molecular Biology and Evolution, Vol. 13, Issue 6 https://doi.org/10.1093/oxfordjournals.molbev.a025641	journal	July 1996
Duplication of a Conditionally Dispensable Chromosome Carrying Pea Pathogenicity (PEP) Gene Clusters in Nectria haematococca Garmaroodi, Hamid S.; Taga, Masatoki Molecular Plant-Microbe Interactions®, Vol. 20, Issue 12 https://doi.org/10.1094/mpmi-20-12-1495	journal	December 2007
Electrophoretic Karyotypes ofMagnaporthe griseaPathogens of Diverse Grasses Orbach, Marc J. Molecular Plant-Microbe Interactions, Vol. 9, Issue 4 https://doi.org/10.1094/mpmi-9-0261	journal	January 1996
DNA Fingerprint Probe from Mycosphaerella graminicola Identifies an Active Transposable Element Goodwin, Stephen B.; Cavaletto, Jessica R.; Waalwijk, Cees Phytopathology®, Vol. 91, Issue 12 https://doi.org/10.1094/phyto.2001.91.12.1181	journal	December 2001
Observations on the Effects of a Chromosome Duplication in Aspergillus Nidulans Bainbridge, B. W.; Roper, J. A. Journal of General Microbiology, Vol. 42, Issue 3 https://doi.org/10.1099/00221287-42-3-417	journal	March 1966
Dothideomycete–Plant Interactions Illuminated by Genome Sequencing and EST Analysis of the Wheat Pathogen Stagonospora nodorum Hane, James K.; Lowe, Rohan G. T.; Solomon, Peter S. The Plant Cell, Vol. 19, Issue 11 https://doi.org/10.1105/tpc.107.052829	journal	November 2007
The Fusarium graminearum Genome Reveals a Link Between Localized Polymorphism and Pathogen Specialization Cuomo, C. A.; Guldener, U.; Xu, J. -R. Science, Vol. 317, Issue 5843 https://doi.org/10.1126/science.1143708	journal	September 2007
A fungal gene for antibiotic resistance on a dispensable ("B") chromosome Miao, V.; Covert, S.; VanEtten, H. Science, Vol. 254, Issue 5039 https://doi.org/10.1126/science.1763326	journal	December 1991
Chromosomal Translocation and Segmental Duplication in Cryptococcus neoformans Fraser, James A.; Huang, Johnny C.; Pukkila-Worley, Read Eukaryotic Cell, Vol. 4, Issue 2 https://doi.org/10.1128/ec.4.2.401-406.2005	journal	February 2005
Serotype AD Strains of Cryptococcus neoformans Are Diploid or Aneuploid and Are Heterozygous at the Mating-Type Locus Lengeler, Klaus B.; Cox, Gary M.; Heitman, Joseph Infection and Immunity, Vol. 69, Issue 1 https://doi.org/10.1128/iai.69.1.115-122.2001	journal	January 2001
Chromosome-length polymorphism in fungi Zolan, M. E. Microbiological Reviews, Vol. 59, Issue 4 https://doi.org/10.1128/mr.59.4.686-698.1995	journal	December 1995
Distribution of DArT, AFLP, and SSR markers in a genetic linkage map of a doubled-haploid hexaploid wheat population Semagn, Kassa; Bjørnstad, Åsmund; Skinnes, Helge Genome, Vol. 49, Issue 5 https://doi.org/10.1139/g06-002	journal	May 2006
The Cytology of the Fungi Cutter, Victor M. Annual Review of Microbiology, Vol. 5, Issue 1 https://doi.org/10.1146/annurev.mi.05.100151.000313	journal	October 1951
Stability of Large Segmental Duplications in the Yeast Genome Koszul, Romain; Dujon, Bernard; Fischer, Gilles Genetics, Vol. 172, Issue 4 https://doi.org/10.1534/genetics.105.048058	journal	April 2006
Association of ergot alkaloids with conidiation in Aspergillus fumigatus Coyle, C. M.; Kenaley, S. C.; Rittenour, W. R. Mycologia, Vol. 99, Issue 6 https://doi.org/10.3852/mycologia.99.6.804	journal	November 2007
Electrophoretic and cytological karyotyping of the foliar wheat pathogen Mycosphaerella graminicola reveals many chromosomes with a large size range Mehrabi, R.; Taga, M.; Kema, G. H. J. Mycologia, Vol. 99, Issue 6 https://doi.org/10.3852/mycologia.99.6.868	journal	November 2007

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Mycosphaerella graminicola: from genomics to disease control: Pathogen profile for M. graminicola Orton, Elizabeth S.; Deller, Sian; Brown, James K. M. Molecular Plant Pathology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1364-3703.2010.00688.x	journal	January 2011
The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A. Molecular Plant Pathology, Vol. 13, Issue 4 https://doi.org/10.1111/j.1364-3703.2011.00783.x	journal	April 2012
The Top 10 fungal pathogens in molecular plant pathology: Corrigendum Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A. Molecular Plant Pathology, Vol. 13, Issue 7 https://doi.org/10.1111/j.1364-3703.2012.00822.x	journal	July 2012
The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens Dean, Ralph; Van Kan, Jan A. L.; Pretorius, Zacharias A. Molecular Plant Pathology https://doi.org/10.1111/j.1364-3703.2012.2011.00783.x	journal	March 2012
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Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici: QTL mapping of virulence in Zymoseptoria tritici Stewart, Ethan l.; Croll, Daniel; Lendenmann, Mark H. Molecular Plant Pathology, Vol. 19, Issue 1 https://doi.org/10.1111/mpp.12515	journal	February 2017
The dispensable chromosome of L eptosphaeria maculans shelters an effector gene conferring avirulence towards B rassica rapa Balesdent, Marie‐Hélène; Fudal, Isabelle; Ollivier, Bénédicte New Phytologist, Vol. 198, Issue 3 https://doi.org/10.1111/nph.12178	journal	February 2013
Genetic structure of a Pyrenophora teres f. teres population over time in an Australian barley field as revealed by Diversity Arrays Technology markers Poudel, B.; Vaghefi, N.; McLean, M. S. Plant Pathology, Vol. 68, Issue 7 https://doi.org/10.1111/ppa.13035	journal	May 2019
Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution Todd, Robert T.; Forche, Anja; Selmecki, Anna The Fungal Kingdom https://doi.org/10.1128/9781555819583.ch28	book	September 2017
MVE1 , Encoding the Velvet Gene Product Homolog in Mycosphaerella graminicola , Is Associated with Aerial Mycelium Formation, Melanin Biosynthesis, Hyphal Swelling, and Light Signaling Choi, Yoon-E; Goodwin, Stephen B. Applied and Environmental Microbiology, Vol. 77, Issue 3 https://doi.org/10.1128/aem.01830-10	journal	February 2011
Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution Todd, Robert T.; Forche, Anja; Selmecki, Anna Microbiology Spectrum, Vol. 5, Issue 4 https://doi.org/10.1128/microbiolspec.funk-0051-2016	journal	August 2017
The landscape of transposable elements in the finished genome of the fungal wheat pathogen Mycosphaerella graminicola Dhillon, Braham; Gill, Navdeep; Hamelin, Richard C. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-1132	journal	January 2014
A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi Hane, James K.; Rouxel, Thierry; Howlett, Barbara J. Genome Biology, Vol. 12, Issue 5 https://doi.org/10.1186/gb-2011-12-5-r45	journal	January 2011
Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen Vanheule, Adriaan; Audenaert, Kris; Warris, Sven BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2941-6	journal	August 2016
Transcriptome sequencing of Mycosphaerella fijiensis during association with Musa acuminata reveals candidate pathogenicity genes Noar, Roslyn D.; Daub, Margaret E. BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3031-5	journal	August 2016
Comparative transcriptome analysis and identification of candidate effectors in two related rust species (Gymnosporangium yamadae and Gymnosporangium asiaticum) Tao, Si-Qi; Cao, Bin; Tian, Cheng-Ming BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4059-x	journal	August 2017
Trichoderma reesei meiosis generates segmentally aneuploid progeny with higher xylanase-producing capability Chuang, Yu-Chien; Li, Wan-Chen; Chen, Chia-Ling Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0202-6	journal	January 2015
Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes Schotanus, Klaas; Soyer, Jessica L.; Connolly, Lanelle R. Epigenetics & Chromatin, Vol. 8, Issue 1 https://doi.org/10.1186/s13072-015-0033-5	journal	October 2015
Whole-Genome and Chromosome Evolution Associated with Host Adaptation and Speciation of the Wheat Pathogen Mycosphaerella graminicola Stukenbrock, Eva H.; Jørgensen, Frank G.; Zala, Marcello PLoS Genetics, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pgen.1001189	journal	December 2010
Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis Goodwin, Stephen B.; Ben M'Barek, Sarrah; Dhillon, Braham PLoS Genetics, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pgen.1002070	journal	June 2011
Breakage-fusion-bridge Cycles and Large Insertions Contribute to the Rapid Evolution of Accessory Chromosomes in a Fungal Pathogen Croll, Daniel; Zala, Marcello; McDonald, Bruce A. PLoS Genetics, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pgen.1003567	journal	June 2013
Chromosomal Copy Number Variation, Selection and Uneven Rates of Recombination Reveal Cryptic Genome Diversity Linked to Pathogenicity Farrer, Rhys A.; Henk, Daniel A.; Garner, Trenton W. J. PLoS Genetics, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pgen.1003703	journal	August 2013
Destabilization of chromosome structure by histone H3 lysine 27 methylation Möller, Mareike; Schotanus, Klaas; Soyer, Jessica L. PLOS Genetics, Vol. 15, Issue 4 https://doi.org/10.1371/journal.pgen.1008093	journal	April 2019
Defining the Predicted Protein Secretome of the Fungal Wheat Leaf Pathogen Mycosphaerella graminicola Morais do Amaral, Alexandre; Antoniw, John; Rudd, Jason J. PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0049904	journal	December 2012
The Accessory Genome as a Cradle for Adaptive Evolution in Pathogens Croll, Daniel; McDonald, Bruce A. PLoS Pathogens, Vol. 8, Issue 4 https://doi.org/10.1371/journal.ppat.1002608	journal	April 2012
Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi Ohm, Robin A.; Feau, Nicolas; Henrissat, Bernard PLoS Pathogens, Vol. 8, Issue 12 https://doi.org/10.1371/journal.ppat.1003037	journal	December 2012
The landscape of transposable elements in the finished genome of the fungal wheat pathogen Mycosphaerella graminicola Dhillon, Braham; Gill, Navdeep; Hamelin, Richard C. BioMed Central https://doi.org/10.14288/1.0221569	text	January 2014
The landscape of transposable elements in the finished genome of the fungal wheat pathogen Mycosphaerella graminicola Dhillon, Braham; Gill, Navdeep; Hamelin, Richard C. BioMed Central https://doi.org/10.14288/1.0223851	text	January 2014
RNA-seq-Based Gene Annotation and Comparative Genomics of Four Fungal Grass Pathogens in the Genus Zymoseptoria Identify Novel Orphan Genes and Species-Specific Invasions of Transposable Elements Grandaubert, Jonathan; Bhattacharyya, Amitava; Stukenbrock, Eva H. G3: Genes\|Genomes\|Genetics, Vol. 5, Issue 7 https://doi.org/10.1534/g3.115.017731	journal	April 2015
The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen Croll, Daniel; Lendenmann, Mark H.; Stewart, Ethan Genetics, Vol. 201, Issue 3 https://doi.org/10.1534/genetics.115.180968	journal	September 2015
Extraordinary Genome Instability and Widespread Chromosome Rearrangements During Vegetative Growth Möller, Mareike; Habig, Michael; Freitag, Michael Genetics, Vol. 210, Issue 2 https://doi.org/10.1534/genetics.118.301050	journal	August 2018
Using Population and Comparative Genomics to Understand the Genetic Basis of Effector-Driven Fungal Pathogen Evolution Plissonneau, Clémence; Benevenuto, Juliana; Mohd-Assaad, Norfarhan Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00119	journal	February 2017
Whole-Genome and Chromosome Evolution Associated with Host Adaptation and Speciation of the Wheat Pathogen Mycosphaerella graminicola H., Stukenbrock, Eva; G., Jørgensen, Frank; Marcello, Zala, ETH Zurich https://doi.org/10.3929/ethz-b-000026092	text	January 2010
Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis Goodwin, Stephen B.; M'Barek, Sarrah B.; Dhillon, Braham ETH Zurich https://doi.org/10.3929/ethz-b-000038874	text	January 2011
The Accessory Genome as a Cradle for Adaptive Evolution in Pathogens Croll, Daniel; McDonald, Bruce A. ETH Zurich https://doi.org/10.3929/ethz-b-000048622	text	January 2012
Breakage-fusion-bridge Cycles and Large Insertions Contribute to the Rapid Evolution of Accessory Chromosomes in a Fungal Pathogen Croll, Daniel; Zala, Marcello; McDonald, Bruce A. ETH Zurich https://doi.org/10.3929/ethz-b-000072029	text	January 2013
Using Population and Comparative Genomics to Understand the Genetic Basis of Effector-Driven Fungal Pathogen Evolution Plissonneau, Clémence; Benevenuto, Juliana; Mohd-Assaad, Norfarhan ETH Zurich https://doi.org/10.3929/ethz-b-000216386	text	January 2017
Meiosis leads to pervasive copy-number variation and distorted inheritance of accessory chromosomes of the wheat pathogen Zymoseptoria tritici Fouché, Simone; Plissonneau, Clémence; McDonald, Bruce A. ETH Zurich https://doi.org/10.3929/ethz-b-000285923	text	January 2018
Meiotic drive of female-inherited supernumerary chromosomes in a pathogenic fungus Habig, Michael; Kema, Gert HJ; Holtgrewe Stukenbrock, Eva eLife, Vol. 7 https://doi.org/10.7554/elife.40251	journal	December 2018

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