Chromosomal rearrangements with stable repertoires of genes and transposable elements in an invasive forest-pathogenic fungus

10.24072/pcjournal.127 - Peer Community Journal, Volume 2 (2022), article no. e28.

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Chromosomal rearrangements have been largely described among eukaryotes, and may have important consequences on evolution of species. High genome plasticity has been often reported in Fungi, which may explain their apparent ability to quickly adapt to new environments. Cryphonectria parasitica, causing the Chestnut blight disease, is an invasive fungal pathogen species associated with several recent host shifts during its successive introductions from Asia to North America and Europe. Previous cytological karyotyping and genomic studies suggested several chromosomal rearrangements which remains to be described in detail for this species. A serious limitation for valid genome comparisons is the access to robust genome assemblies that usually contain genomic regions of low complexity. We present a new de novo whole-genome assembly obtained from a new method of DNA extraction and long-reads sequencing Nanopore technology obtained from a Japanese isolate sampled in the native area of the species. The comparison with a recently published reference genome revealed stable gene and transposable elements (TEs) repertoires. We also showed that the C. parasitica genome is lowly compartmentalized, with a poor association between TEs and genes, such as those potentially involved in host interactions (i.e., genes coding for small secreted proteins or for secondary metabolites). This genome comparison, however, detected several large chromosomal rearrangements that may have important consequences in gene regulations and sexual mating in this invasive species. This study opens the way for more comparisons of high-quality assembled genomes, and questions the role of structural variations in the invasive success of this fungal pathogen species.

Published online:
DOI: 10.24072/pcjournal.127
Demené, Arthur 1; Laurent, Benoît 1; Cros-Arteil, Sandrine 2; Boury, Christophe 1; Dutech, Cyril 1

1 INRAE, Univ. Bordeaux, BIOGECO, F-33610 Cestas, France
2 PHIM, INRAE, CIRAD, Campus International de Baillarguet, 34980 Montferrier-sur-Lez, France
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Demené, Arthur; Laurent, Benoît; Cros-Arteil, Sandrine; Boury, Christophe; Dutech, Cyril. Chromosomal rearrangements with stable repertoires of genes and transposable elements in an invasive forest-pathogenic fungus. Peer Community Journal, Volume 2 (2022), article  no. e28. doi : 10.24072/pcjournal.127.

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100013

[1] Alonge, M.; Wang, X.; Benoit, M.; Soyk, S.; Pereira, L.; Zhang, L.; Suresh, H.; Ramakrishnan, S.; Maumus, F.; Ciren, D.; Levy, Y.; Harel, T. H.; Shalev-Schlosser, G.; Amsellem, Z.; Razifard, H.; Caicedo, A. L.; Tieman, D. M.; Klee, H.; Kirsche, M.; Aganezov, S.; Ranallo-Benavidez, T. R.; Lemmon, Z. H.; Kim, J.; Robitaille, G.; Kramer, M.; Goodwin, S.; McCombie, W. R.; Hutton, S.; Van Eck, J.; Gillis, J.; Eshed, Y.; Sedlazeck, F. J.; van der Knaap, E.; Schatz, M. C.; Lippman, Z. B. Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato, Cell, Volume 182 (2020) no. 1 | Article

[2] Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | Article

[3] Anagnostakis, S. L. Chestnut Blight: The Classical Problem of an Introduced Pathogen, Mycologia, Volume 79 (1987) no. 1, pp. 23-27 | Article

[4] Antipov, D.; Korobeynikov, A.; McLean, J. S.; Pevzner, P. A. hybridSPAdes: an algorithm for hybrid assembly of short and long reads, Bioinformatics, Volume 32 (2015) no. 7, pp. 1009-1015 | Article

[5] Almagro Armenteros, J. J.; Tsirigos, K. D.; Sønderby, C. K.; Petersen, T. N.; Winther, O.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 5.0 improves signal peptide predictions using deep neural networks, Nature Biotechnology, Volume 37 (2019) no. 4, pp. 420-423 | Article

[6] Badet, T.; Oggenfuss, U.; Abraham, L.; McDonald, B. A.; Croll, D. A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici, BMC Biology, Volume 18 (2020) no. 1 | Article

[7] Badouin, H.; Hood, M. E.; Gouzy, J.; Aguileta, G.; Siguenza, S.; Perlin, M. H.; Cuomo, C. A.; Fairhead, C.; Branca, A.; Giraud, T. Chaos of Rearrangements in the Mating-Type Chromosomes of the Anther-Smut Fungus Microbotryum lychnidis-dioicae, Genetics, Volume 200 (2015) no. 4, pp. 1275-1284 | Article

[8] Badouin, H.; Gladieux, P.; Gouzy, J.; Siguenza, S.; Aguileta, G.; Snirc, A.; Le Prieur, S.; Jeziorski, C.; Branca, A.; Giraud, T. Widespread selective sweeps throughout the genome of model plant pathogenic fungi and identification of effector candidates, Molecular Ecology, Volume 26 (2017) no. 7, pp. 2041-2062 | Article

[9] Bayat, A.; Deshpande, N. P.; Wilkins, M. R.; Parameswaran, S. Fast Short Read De-Novo Assembly Using Overlap-Layout-Consensus Approach, IEEE/ACM Transactions on Computational Biology and Bioinformatics, Volume 17 (2020) no. 1, pp. 334-338 | Article

[10] Bills, G. F.; Gloer, J. B. Biologically Active Secondary Metabolites from the Fungi, Microbiology Spectrum, Volume 4 (2016) no. 6 | Article

[11] Blin, K.; Shaw, S.; Steinke, K.; Villebro, R.; Ziemert, N.; Lee, S. Y.; Medema, M. H.; Weber, T. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline, Nucleic Acids Research, Volume 47 (2019) no. W1 | Article

[12] Brown, J. K. M.; Tellier, A. Plant-Parasite Coevolution: Bridging the Gap between Genetics and Ecology, Annual Review of Phytopathology, Volume 49 (2011) no. 1, pp. 345-367 | Article

[13] Cao, M. D.; Nguyen, S. H.; Ganesamoorthy, D.; Elliott, A. G.; Cooper, M. A.; Coin, L. J. M. Scaffolding and completing genome assemblies in real-time with nanopore sequencing, Nature Communications, Volume 8 (2017) no. 1 | Article

[14] Casas-Vila, N.; Scheibe, M.; Freiwald, A.; Kappei, D.; Butter, F. Identification of TTAGGG-binding proteins in Neurospora crassa, a fungus with vertebrate-like telomere repeats, BMC Genomics, Volume 16 (2015) no. 1 | Article

[15] Castanera, R.; López-Varas, L.; Borgognone, A.; LaButti, K.; Lapidus, A.; Schmutz, J.; Grimwood, J.; Pérez, G.; Pisabarro, A. G.; Grigoriev, I. V.; Stajich, J. E.; Ramírez, L. Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles, PLOS Genetics, Volume 12 (2016) no. 6 | Article

[16] Chang, S.-L.; Lai, H.-Y.; Tung, S.-Y.; Leu, J.-Y. Dynamic Large-Scale Chromosomal Rearrangements Fuel Rapid Adaptation in Yeast Populations, PLoS Genetics, Volume 9 (2013) no. 1 | Article

[17] Cheeseman, K.; Ropars, J.; Renault, P.; Dupont, J.; Gouzy, J.; Branca, A.; Abraham, A.-L.; Ceppi, M.; Conseiller, E.; Debuchy, R.; Malagnac, F.; Goarin, A.; Silar, P.; Lacoste, S.; Sallet, E.; Bensimon, A.; Giraud, T.; Brygoo, Y. Multiple recent horizontal transfers of a large genomic region in cheese making fungi, Nature Communications, Volume 5 (2014) no. 1 | Article

[18] Chuma, I.; Isobe, C.; Hotta, Y.; Ibaragi, K.; Futamata, N.; Kusaba, M.; Yoshida, K.; Terauchi, R.; Fujita, Y.; Nakayashiki, H.; Valent, B.; Tosa, Y. Multiple Translocation of the AVR-Pita Effector Gene among Chromosomes of the Rice Blast Fungus Magnaporthe oryzae and Related Species, PLoS Pathogens, Volume 7 (2011) no. 7 | Article

[19] John Clutterbuck, A. Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes, Fungal Genetics and Biology, Volume 48 (2011) no. 3, pp. 306-326 | Article

[20] Courtine, D.; Provaznik, J.; Reboul, J.; Blanc, G.; Benes, V.; Ewbank, J. J. Long-read only assembly of Drechmeria coniospora genomes reveals widespread chromosome plasticity and illustrates the limitations of current nanopore methods, GigaScience, Volume 9 (2020) no. 9 | Article

[21] Croll, D.; Lendenmann, M. H.; Stewart, E.; McDonald, B. A. The Impact of Recombination Hotspots on Genome Evolution of a Fungal Plant Pathogen, Genetics, Volume 201 (2015) no. 3, pp. 1213-1228 | Article

[22] Crouch, J. A.; Dawe, A.; Aerts, A.; Barry, K.; Churchill, A. C. L.; Grimwood, J.; Hillman, B. I.; Milgroom, M. G.; Pangilinan, J.; Smith, M.; Salamov, A.; Schmutz, J.; Yadav, J. S.; Grigoriev, I. V.; Nuss, D. L. Genome Sequence of the Chestnut Blight Fungus Cryphonectria parasitica EP155: A Fundamental Resource for an Archetypical Invasive Plant Pathogen, Phytopathology, Volume 110 (2020) no. 6, pp. 1180-1188 | Article

[23] Daboussi, M.-J.; Capy, P. Transposable Elements in Filamentous Fungi, Annual Review of Microbiology, Volume 57 (2003) no. 1, pp. 275-299 | Article

[24] Demené, A.; Legrand, L.; Gouzy, J.; Debuchy, R.; Saint-Jean, G.; Fabreguettes, O.; Dutech, C. Whole-genome sequencing reveals recent and frequent genetic recombination between clonal lineages of Cryphonectria parasitica in western Europe, Fungal Genetics and Biology, Volume 130 (2019), pp. 122-133 | Article

[25] Dennert, F.; Meyer, J. B.; Rigling, D.; Prospero, S. Assessing the Phytosanitary Risk Posed by an Intraspecific Invasion of Cryphonectria parasitica in Europe, Phytopathology, Volume 109 (2019) no. 12, pp. 2055-2063 | Article

[26] Dhillon, B.; Feau, N.; Aerts, A. L.; Beauseigle, S.; Bernier, L.; Copeland, A.; Foster, A.; Gill, N.; Henrissat, B.; Herath, P.; LaButti, K. M.; Levasseur, A.; Lindquist, E. A.; Majoor, E.; Ohm, R. A.; Pangilinan, J. L.; Pribowo, A.; Saddler, J. N.; Sakalidis, M. L.; de Vries, R. P.; Grigoriev, I. V.; Goodwin, S. B.; Tanguay, P.; Hamelin, R. C. Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 11, pp. 3451-3456 | Article

[27] Donath, A.; Jühling, F.; Al-Arab, M.; Bernhart, S. H.; Reinhardt, F.; Stadler, P. F.; Middendorf, M.; Bernt, M. Improved annotation of protein-coding genes boundaries in metazoan mitochondrial genomes, Nucleic Acids Research, Volume 47 (2019) no. 20, pp. 10543-10552 | Article

[28] Dong, S.; Raffaele, S.; Kamoun, S. The two-speed genomes of filamentous pathogens: waltz with plants, Current Opinion in Genetics & Development, Volume 35 (2015), pp. 57-65 | Article

[29] Dunham, M. J.; Badrane, H.; Ferea, T.; Adams, J.; Brown, P. O.; Rosenzweig, F.; Botstein, D. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 25, pp. 16144-16149 | Article

[30] Duplessis, S.; Cuomo, C. A.; Lin, Y.-C.; Aerts, A.; Tisserant, E.; Veneault-Fourrey, C.; Joly, D. L.; Hacquard, S.; Amselem, J.; Cantarel, B. L.; Chiu, R.; Coutinho, P. M.; Feau, N.; Field, M.; Frey, P.; Gelhaye, E.; Goldberg, J.; Grabherr, M. G.; Kodira, C. D.; Kohler, A.; Kües, U.; Lindquist, E. A.; Lucas, S. M.; Mago, R.; Mauceli, E.; Morin, E.; Murat, C.; Pangilinan, J. L.; Park, R.; Pearson, M.; Quesneville, H.; Rouhier, N.; Sakthikumar, S.; Salamov, A. A.; Schmutz, J.; Selles, B.; Shapiro, H.; Tanguay, P.; Tuskan, G. A.; Henrissat, B.; Van de Peer, Y.; Rouzé, P.; Ellis, J. G.; Dodds, P. N.; Schein, J. E.; Zhong, S.; Hamelin, R. C.; Grigoriev, I. V.; Szabo, L. J.; Martin, F. Obligate biotrophy features unraveled by the genomic analysis of rust fungi, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 22, pp. 9166-9171 | Article

[31] Dutech, C.; Fabreguettes, O.; Capdevielle, X.; Robin, C. Multiple introductions of divergent genetic lineages in an invasive fungal pathogen, Cryphonectria parasitica, in France, Heredity, Volume 105 (2009) no. 2, pp. 220-228 | Article

[32] Dutech, C.; Barrès, B.; Bridier, J.; Robin, C.; Milgroom, M. G.; Ravigné, V. The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen, Molecular Ecology, Volume 21 (2012) no. 16, pp. 3931-3946 | Article

[33] Dutheil, J. Y.; Mannhaupt, G.; Schweizer, G.; M.K. Sieber, C.; Münsterkötter, M.; Güldener, U.; Schirawski, J.; Kahmann, R. A Tale of Genome Compartmentalization: The Evolution of Virulence Clusters in Smut Fungi, Genome Biology and Evolution, Volume 8 (2016) no. 3, pp. 681-704 | Article

[34] Emms, D. M.; Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics, Genome Biology, Volume 20 (2019) no. 1 | Article

[35] Eschenbrenner, C. J.; Feurtey, A.; Stukenbrock, E. H. Population Genomics of Fungal Plant Pathogens and the Analyses of Rapidly Evolving Genome Compartments, Methods in Molecular Biology, Springer US, New York, NY, 2020, pp. 337-355 | Article

[36] Eusebio-Cope, A.; Suzuki, N.; Sadeghi-Garmaroodi, H.; Taga, M. Cytological and electrophoretic karyotyping of the chestnut blight fungus Cryphonectria parasitica, Fungal Genetics and Biology, Volume 46 (2009) no. 4, pp. 342-351 | Article

[37] Faino, L.; Seidl, M. F.; Shi-Kunne, X.; Pauper, M.; van den Berg, G. C.; Wittenberg, A. H.; Thomma, B. P. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen, Genome Research, Volume 26 (2016) no. 8, pp. 1091-1100 | Article

[38] Fedorova, N. D.; Khaldi, N.; Joardar, V. S.; Maiti, R.; Amedeo, P.; Anderson, M. J.; Crabtree, J.; Silva, J. C.; Badger, J. H.; Albarraq, A.; Angiuoli, S.; Bussey, H.; Bowyer, P.; Cotty, P. J.; Dyer, P. S.; Egan, A.; Galens, K.; Fraser-Liggett, C. M.; Haas, B. J.; Inman, J. M.; Kent, R.; Lemieux, S.; Malavazi, I.; Orvis, J.; Roemer, T.; Ronning, C. M.; Sundaram, J. P.; Sutton, G.; Turner, G.; Venter, J. C.; White, O. R.; Whitty, B. R.; Youngman, P.; Wolfe, K. H.; Goldman, G. H.; Wortman, J. R.; Jiang, B.; Denning, D. W.; Nierman, W. C. Genomic Islands in the Pathogenic Filamentous Fungus Aspergillus fumigatus, PLoS Genetics, Volume 4 (2008) no. 4 | Article

[39] Fisher, S.; Barry, A.; Abreu, J.; Minie, B.; Nolan, J.; Delorey, T. M.; Young, G.; Fennell, T. J.; Allen, A.; Ambrogio, L.; Berlin, A. M.; Blumenstiel, B.; Cibulskis, K.; Friedrich, D.; Johnson, R.; Juhn, F.; Reilly, B.; Shammas, R.; Stalker, J.; Sykes, S. M.; Thompson, J.; Walsh, J.; Zimmer, A.; Zwirko, Z.; Gabriel, S.; Nicol, R.; Nusbaum, C. A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries, Genome Biology, Volume 12 (2011) no. 1 | Article

[40] Flutre, T.; Duprat, E.; Feuillet, C.; Quesneville, H. Considering Transposable Element Diversification in De Novo Annotation Approaches, PLoS ONE, Volume 6 (2011) no. 1 | Article

[41] Frantzeskakis, L.; Kracher, B.; Kusch, S.; Yoshikawa-Maekawa, M.; Bauer, S.; Pedersen, C.; Spanu, P. D.; Maekawa, T.; Schulze-Lefert, P.; Panstruga, R. Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen, BMC Genomics, Volume 19 (2018) no. 1 | Article

[42] Frantzeskakis, L.; Kusch, S.; Panstruga, R. The need for speed: compartmentalized genome evolution in filamentous phytopathogens, Molecular Plant Pathology, Volume 20 (2019) no. 1, pp. 3-7 | Article

[43] Freitag, M.; Williams, R. L.; Kothe, G. O.; Selker, E. U. A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 13, pp. 8802-8807 | Article

[44] Gladieux, P.; Feurtey, A.; Hood, M. E.; Snirc, A.; Clavel, J.; Dutech, C.; Roy, M.; Giraud, T. The population biology of fungal invasions, Molecular Ecology, Volume 24 (2015) no. 9, pp. 1969-1986 | Article

[45] Gotz, S.; Garcia-Gomez, J. M.; Terol, J.; Williams, T. D.; Nagaraj, S. H.; Nueda, M. J.; Robles, M.; Talon, M.; Dopazo, J.; Conesa, A. High-throughput functional annotation and data mining with the Blast2GO suite, Nucleic Acids Research, Volume 36 (2008) no. 10, pp. 3420-3435 | Article

[46] Gout, L.; Fudal, I.; Kuhn, M.; Blaise, F.; Eckert, M.; Cattolico, L.; Balesdent, M.; Rouxel, T. Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans, Molecular Microbiology, Volume 60 (2006) no. 1, pp. 67-80 | Article

[47] Grandaubert, J.; Lowe, R. G.; Soyer, J. L.; Schoch, C. L.; Van de Wouw, A. P.; Fudal, I.; Robbertse, B.; Lapalu, N.; Links, M. G.; Ollivier, B.; Linglin, J.; Barbe, V.; Mangenot, S.; Cruaud, C.; Borhan, H.; Howlett, B. J.; Balesdent, M.-H.; Rouxel, T. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens, BMC Genomics, Volume 15 (2014) no. 1 | Article

[48] Gremme, G.; Steinbiss, S.; Kurtz, S. GenomeTools: A Comprehensive Software Library for Efficient Processing of Structured Genome Annotations, IEEE/ACM Transactions on Computational Biology and Bioinformatics, Volume 10 (2013) no. 3, pp. 645-656 | Article

[49] Haghshenas, E.; Hach, F.; Sahinalp, S. C.; Chauve, C. CoLoRMap: Correcting Long Reads by Mapping short reads, Bioinformatics, Volume 32 (2016) no. 17 | Article

[50] Hane, J. K.; Rouxel, T.; Howlett, B. J.; Kema, G. H.; Goodwin, S. B.; Oliver, R. P. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi, Genome Biology, Volume 12 (2011) no. 5 | Article

[51] Hartmann, F. E.; Sánchez-Vallet, A.; McDonald, B. A.; Croll, D. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements, The ISME Journal, Volume 11 (2017) no. 5, pp. 1189-1204 | Article

[52] Hartmann, F. E.; Rodríguez de la Vega, R. C.; Brandenburg, J.-T.; Carpentier, F.; Giraud, T. Gene Presence–Absence Polymorphism in Castrating Anther-Smut Fungi: Recent Gene Gains and Phylogeographic Structure, Genome Biology and Evolution, Volume 10 (2018) no. 5, pp. 1298-1314 | Article

[53] Hoede, C.; Arnoux, S.; Moisset, M.; Chaumier, T.; Inizan, O.; Jamilloux, V.; Quesneville, H. PASTEC: An Automatic Transposable Element Classification Tool, PLoS ONE, Volume 9 (2014) no. 5 | Article

[54] Hoegger, P. J.; Rigling, D.; Holdenrieder, O.; Heiniger, U. Genetic structure of newly established populations of Cryphonectria parasitica, Mycological Research, Volume 104 (2000) no. 9, pp. 1108-1116 | Article

[55] Hoff, K. J.; Lomsadze, A.; Borodovsky, M.; Stanke, M. Whole-Genome Annotation with BRAKER, Methods in Molecular Biology, Springer New York, New York, NY, 2019, pp. 65-95 | Article

[56] Hou, J.; Friedrich, A.; de Montigny, J.; Schacherer, J. Chromosomal Rearrangements as a Major Mechanism in the Onset of Reproductive Isolation in Saccharomyces cerevisiae, Current Biology, Volume 24 (2014) no. 10, pp. 1153-1159 | Article

[57] Ikeda, K.-i.; Nakayashiki, H.; Kataoka, T.; Tamba, H.; Hashimoto, Y.; Tosa, Y.; Mayama, S. Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context, Molecular Microbiology, Volume 45 (2002) no. 5, pp. 1355-1364 | Article

[58] Jones, P.; Binns, D.; Chang, H.-Y.; Fraser, M.; Li, W.; McAnulla, C.; McWilliam, H.; Maslen, J.; Mitchell, A.; Nuka, G.; Pesseat, S.; Quinn, A. F.; Sangrador-Vegas, A.; Scheremetjew, M.; Yong, S.-Y.; Lopez, R.; Hunter, S. InterProScan 5: genome-scale protein function classification, Bioinformatics, Volume 30 (2014) no. 9, pp. 1236-1240 | Article

[59] de Jonge, R.; Bolton, M. D.; Kombrink, A.; van den Berg, G. C.; Yadeta, K. A.; Thomma, B. P. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen, Genome Research, Volume 23 (2013) no. 8, pp. 1271-1282 | Article

[60] Kamoun, S. A Catalogue of the Effector Secretome of Plant Pathogenic Oomycetes, Annual Review of Phytopathology, Volume 44 (2006) no. 1, pp. 41-60 | Article

[61] Kistler, H. C.; Miao, V. P. W. New Modes of Genetic Change in Filamentous Fungi, Annual Review of Phytopathology, Volume 30 (1992) no. 1, pp. 131-152 | Article

[62] Langmead, B.; Salzberg, S. L. Fast gapped-read alignment with Bowtie 2, Nature Methods, Volume 9 (2012) no. 4, pp. 357-359 | Article

[63] Laurent, B.; Palaiokostas, C.; Spataro, C.; Moinard, M.; Zehraoui, E.; Houston, R. D.; Foulongne‐Oriol, M. High‐resolution mapping of the recombination landscape of the phytopathogen Fusarium graminearum suggests two‐speed genome evolution, Molecular Plant Pathology, Volume 19 (2018) no. 2, pp. 341-354 | Article

[64] Li, H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences, Bioinformatics, Volume 32 (2016) no. 14, pp. 2103-2110 | Article

[65] Li, H. Minimap2: pairwise alignment for nucleotide sequences, Bioinformatics, Volume 34 (2018) no. 18, pp. 3094-3100 | Article

[66] Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools, Bioinformatics, Volume 25 (2009) no. 16, pp. 2078-2079 | Article

[67] Linder-Basso, D.; Foglia, R.; Zhu, P.; Hillman, B. Crypt1, an active Ac-like transposon from the chestnut blight fungus, Cryphonectria parasitica, Molecular Genetics and Genomics, Volume 265 (2001) no. 4, pp. 730-738 | Article

[68] Liu, Y.; Linder‐Basso, D.; Hillman, B. I.; Kaneko, S.; Milgroom, M. G. Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria, Molecular Ecology, Volume 12 (2003) no. 6, pp. 1619-1628 | Article

[69] Lovat, C.-A.; Donnelly, D. J. Mechanisms and metabolomics of the host-pathogen interactions between Chestnut (Castanea species) and Chestnut blight (Cryphonectria parasitica), Forest Pathology, Volume 49 (2019) no. 6 | Article

[70] Lu, H.; Giordano, F.; Ning, Z. Oxford Nanopore MinION Sequencing and Genome Assembly, Genomics, Proteomics & Bioinformatics, Volume 14 (2016) no. 5, pp. 265-279 | Article

[71] Ma, L.-J.; van der Does, H. C.; Borkovich, K. A.; Coleman, J. J.; Daboussi, M.-J.; Di Pietro, A.; Dufresne, M.; Freitag, M.; Grabherr, M.; Henrissat, B.; Houterman, P. M.; Kang, S.; Shim, W.-B.; Woloshuk, C.; Xie, X.; Xu, J.-R.; Antoniw, J.; Baker, S. E.; Bluhm, B. H.; Breakspear, A.; Brown, D. W.; Butchko, R. A. E.; Chapman, S.; Coulson, R.; Coutinho, P. M.; Danchin, E. G. J.; Diener, A.; Gale, L. R.; Gardiner, D. M.; Goff, S.; Hammond-Kosack, K. E.; Hilburn, K.; Hua-Van, A.; Jonkers, W.; Kazan, K.; Kodira, C. D.; Koehrsen, M.; Kumar, L.; Lee, Y.-H.; Li, L.; Manners, J. M.; Miranda-Saavedra, D.; Mukherjee, M.; Park, G.; Park, J.; Park, S.-Y.; Proctor, R. H.; Regev, A.; Ruiz-Roldan, M. C.; Sain, D.; Sakthikumar, S.; Sykes, S.; Schwartz, D. C.; Turgeon, B. G.; Wapinski, I.; Yoder, O.; Young, S.; Zeng, Q.; Zhou, S.; Galagan, J.; Cuomo, C. A.; Kistler, H. C.; Rep, M. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium, Nature, Volume 464 (2010) no. 7287, pp. 367-373 | Article

[72] Mapleson, D.; Garcia Accinelli, G.; Kettleborough, G.; Wright, J.; Clavijo, B. J. KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies, Bioinformatics, Volume 33 (2016), pp. 574-576 | Article

[73] Marçais, G.; Delcher, A. L.; Phillippy, A. M.; Coston, R.; Salzberg, S. L.; Zimin, A. MUMmer4: A fast and versatile genome alignment system, PLOS Computational Biology, Volume 14 (2018) no. 1 | Article

[74] Margolin, B. S.; Garrett-Engele, P. W.; Stevens, J. N.; Fritz, D. Y.; Garrett-Engele, C.; Metzenberg, R. L.; Selker, E. U. A Methylated Neurospora 5S rRNA Pseudogene Contains a Transposable Element Inactivated by Repeat-Induced Point Mutation, Genetics, Volume 149 (1998) no. 4, pp. 1787-1797 | Article

[75] Marijon, P.; Chikhi, R.; Varré, J.-S. Graph analysis of fragmented long-read bacterial genome assemblies, Bioinformatics, Volume 35 (2019) no. 21, pp. 4239-4246 | Article

[76] McGuire, I.; Marra, R. E.; Turgeon, B.; Milgroom, M. G. Analysis of Mating-Type Genes in the Chestnut Blight Fungus, Cryphonectria parasitica, Fungal Genetics and Biology, Volume 34 (2001) no. 2, pp. 131-144 | Article

[77] Milgroom, M. G.; Lipari, S. E.; Powell, W. A. DNA fingerprinting and analysis of population structure in the chestnut blight fungus, Cryphonectria parasitica., Genetics, Volume 131 (1992) no. 2, pp. 297-306 | Article

[78] Milgroom, M. G.; Wang, K.; Zhou, Y.; Lipari, S. E.; Kaneko, S. Intercontinental Population Structure of the Chestnut Blight Fungus, Cryphonectria parasitica, Mycologia, Volume 88 (1996) no. 2, pp. 179-180 | Article

[79] Milgroom, M. G.; Jiménez-Gasco, M. d. M.; Olivares García, C.; Drott, M. T.; Jiménez-Díaz, R. M. Recombination between Clonal Lineages of the Asexual Fungus Verticillium dahliae Detected by Genotyping by Sequencing, PLoS ONE, Volume 9 (2014) no. 9 | Article

[80] Milgroom, M. G.; Sotirovski, K.; Spica, D.; Davis, J. E.; Brewer, M. T.; Milev, M.; Cortesi, P. Clonal population structure of the chestnut blight fungus in expanding ranges in southeastern Europe, Molecular Ecology, Volume 17 (2008) no. 20, pp. 4446-4458 | Article

[81] Möller, E.; Bahnweg, G.; Sandermann, H.; Geiger, H. A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues, Nucleic Acids Research, Volume 20 (1992) no. 22, pp. 6115-6116 | Article

[82] Muszewska, A.; Hoffman-Sommer, M.; Grynberg, M. LTR Retrotransposons in Fungi, PLoS ONE, Volume 6 (2011) no. 12 | Article

[83] Muszewska, A.; Steczkiewicz, K.; Stepniewska-Dziubinska, M.; Ginalski, K. Transposable elements contribute to fungal genes and impact fungal lifestyle, Scientific Reports, Volume 9 (2019) no. 1 | Article

[84] Nikolenko, S. I.; Korobeynikov, A. I.; Alekseyev, M. A. BayesHammer: Bayesian clustering for error correction in single-cell sequencing, BMC Genomics, Volume 14 (2013) no. Suppl 1 | Article

[85] Olarte, R. A.; Menke, J.; Zhang, Y.; Sullivan, S.; Slot, J. C.; Huang, Y.; Badalamenti, J. P.; Quandt, A. C.; Spatafora, J. W.; Bushley, K. E. Chromosome rearrangements shape the diversification of secondary metabolism in the cyclosporin producing fungus Tolypocladium inflatum, BMC Genomics, Volume 20 (2019) no. 1 | Article

[86] Plissonneau, C.; Stürchler, A.; Croll, D. The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat, mBio, Volume 7 (2016) no. 5 | Article

[87] Plissonneau, C.; Hartmann, F. E.; Croll, D. Pangenome analyses of the wheat pathogen Zymoseptoria tritici reveal the structural basis of a highly plastic eukaryotic genome, BMC Biology, Volume 16 (2018) no. 1 | Article

[88] Qi, X.; Li, Y.; Honda, S.; Hoffmann, S.; Marz, M.; Mosig, A.; Podlevsky, J. D.; Stadler, P. F.; Selker, E. U.; Chen, J. J.-L. The common ancestral core of vertebrate and fungal telomerase RNAs, Nucleic Acids Research, Volume 41 (2012) no. 1, pp. 450-462 | Article

[89] Quesneville, H.; Bergman, C. M.; Andrieu, O.; Autard, D.; Nouaud, D.; Ashburner, M.; Anxolabehere, D. Combined Evidence Annotation of Transposable Elements in Genome Sequences, PLoS Computational Biology, Volume 1 (2005) no. 2, pp. 166-175 | Article

[90] Raffaele, S.; Kamoun, S. Genome evolution in filamentous plant pathogens: why bigger can be better, Nature Reviews Microbiology, Volume 10 (2012) no. 6, pp. 417-430 | Article

[91] Rajarammohan, S.; Pental, D.; Kaur, J. Near-Complete Genome Assembly of Alternaria brassicae—A Necrotrophic Pathogen of Brassica Crops, Molecular Plant-Microbe Interactions®, Volume 32 (2019) no. 8, pp. 928-930 | Article

[92] Ramírez, F.; Ryan, D. P.; Grüning, B.; Bhardwaj, V.; Kilpert, F.; Richter, A. S.; Heyne, S.; Dündar, F.; Manke, T. deepTools2: a next generation web server for deep-sequencing data analysis, Nucleic Acids Research, Volume 44 (2016) no. W1 | Article

[93] Riley, R.; Salamov, A. A.; Brown, D. W.; Nagy, L. G.; Floudas, D.; Held, B. W.; Levasseur, A.; Lombard, V.; Morin, E.; Otillar, R.; Lindquist, E. A.; Sun, H.; LaButti, K. M.; Schmutz, J.; Jabbour, D.; Luo, H.; Baker, S. E.; Pisabarro, A. G.; Walton, J. D.; Blanchette, R. A.; Henrissat, B.; Martin, F.; Cullen, D.; Hibbett, D. S.; Grigoriev, I. V. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 27, pp. 9923-9928 | Article

[94] Sánchez-Vallet, A.; Fouché, S.; Fudal, I.; Hartmann, F. E.; Soyer, J. L.; Tellier, A.; Croll, D. The Genome Biology of Effector Gene Evolution in Filamentous Plant Pathogens, Annual Review of Phytopathology, Volume 56 (2018) no. 1, pp. 21-40 | Article

[95] Schalamun, M.; Nagar, R.; Kainer, D.; Beavan, E.; Eccles, D.; Rathjen, J. P.; Lanfear, R.; Schwessinger, B. Harnessing the MinION: An example of how to establish long‐read sequencing in a laboratory using challenging plant tissue from Eucalyptus pauciflora, Molecular Ecology Resources, Volume 19 (2019) no. 1, pp. 77-89 | Article

[96] Schmieder, R.; Edwards, R. Quality control and preprocessing of metagenomic datasets, Bioinformatics, Volume 27 (2011) no. 6, pp. 863-864 | Article

[97] Schwessinger, B.; Sperschneider, J.; Cuddy, W. S.; Garnica, D. P.; Miller, M. E.; Taylor, J. M.; Dodds, P. N.; Figueroa, M.; Park, R. F.; Rathjen, J. P. A Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity, mBio, Volume 9 (2018) no. 1 | Article

[98] Seidl, M. F.; Thomma, B. P. Transposable Elements Direct The Coevolution between Plants and Microbes, Trends in Genetics, Volume 33 (2017) no. 11, pp. 842-851 | Article

[99] Selker, E. U. Premeiotic instability of repeated sequences in Neurospora crassa, Annual Review of Genetics, Volume 24 (1990) no. 1, pp. 579-613 | Article

[100] Selker, E. U.; Cambareri, E. B.; Jensen, B. C.; Haack, K. R. Rearrangement of duplicated DNA in specialized cells of Neurospora, Cell, Volume 51 (1987) no. 5, pp. 741-752 | Article

[101] Simão, F. A.; Waterhouse, R. M.; Ioannidis, P.; Kriventseva, E. V.; Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs, Bioinformatics, Volume 31 (2015) no. 19, pp. 3210-3212 | Article

[102] Spanu, P. D.; Abbott, J. C.; Amselem, J.; Burgis, T. A.; Soanes, D. M.; Stüber, K.; Loren van Themaat, E. V.; Brown, J. K. M.; Butcher, S. A.; Gurr, S. J.; Lebrun, M.-H.; Ridout, C. J.; Schulze-Lefert, P.; Talbot, N. J.; Ahmadinejad, N.; Ametz, C.; Barton, G. R.; Benjdia, M.; Bidzinski, P.; Bindschedler, L. V.; Both, M.; Brewer, M. T.; Cadle-Davidson, L.; Cadle-Davidson, M. M.; Collemare, J.; Cramer, R.; Frenkel, O.; Godfrey, D.; Harriman, J.; Hoede, C.; King, B. C.; Klages, S.; Kleemann, J.; Knoll, D.; Koti, P. S.; Kreplak, J.; López-Ruiz, F. J.; Lu, X.; Maekawa, T.; Mahanil, S.; Micali, C.; Milgroom, M. G.; Montana, G.; Noir, S.; O’Connell, R. J.; Oberhaensli, S.; Parlange, F.; Pedersen, C.; Quesneville, H.; Reinhardt, R.; Rott, M.; Sacristán, S.; Schmidt, S. M.; Schön, M.; Skamnioti, P.; Sommer, H.; Stephens, A.; Takahara, H.; Thordal-Christensen, H.; Vigouroux, M.; Weßling, R.; Wicker, T.; Panstruga, R. Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism, Science, Volume 330 (2010) no. 6010, pp. 1543-1546 | Article

[103] Sperschneider, J.; Dodds, P. N.; Gardiner, D. M.; Singh, K. B.; Taylor, J. M. Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0, Molecular Plant Pathology, Volume 19 (2018) no. 9, pp. 2094-2110 | Article

[104] Stam, R.; Münsterkötter, M.; Pophaly, S. D.; Fokkens, L.; Sghyer, H.; Güldener, U.; Hückelhoven, R.; Hess, M. A New Reference Genome Shows the One-Speed Genome Structure of the Barley Pathogen Ramularia collo-cygni, Genome Biology and Evolution, Volume 10 (2018) no. 12, pp. 3243-3249 | Article

[105] Stanke, M.; Diekhans, M.; Baertsch, R.; Haussler, D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding, Bioinformatics, Volume 24 (2008) no. 5, pp. 637-644 | Article

[106] Stauber, L.; Prospero, S.; Croll, D. Comparative Genomics Analyses of Lifestyle Transitions at the Origin of an Invasive Fungal Pathogen in the Genus Cryphonectria, mSphere, Volume 5 (2020) no. 5 | Article

[107] Stauber, L.; Badet, T.; Feurtey, A.; Prospero, S.; Croll, D. Emergence and diversification of a highly invasive chestnut pathogen lineage across southeastern Europe, eLife, Volume 10 (2021) | Article

[108] Stukenbrock, E. H.; Bataillon, T. A Population Genomics Perspective on the Emergence and Adaptation of New Plant Pathogens in Agro-Ecosystems, PLoS Pathogens, Volume 8 (2012) no. 9 | Article

[109] Thorvaldsdottir, H.; Robinson, J. T.; Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration, Briefings in Bioinformatics, Volume 14 (2012) no. 2, pp. 178-192 | Article

[110] Torres, D. E.; Oggenfuss, U.; Croll, D.; Seidl, M. F. Genome evolution in fungal plant pathogens: looking beyond the two-speed genome model, Fungal Biology Reviews, Volume 34 (2020) no. 3, pp. 136-143 | Article

[111] Tsushima, A.; Gan, P.; Kumakura, N.; Narusaka, M.; Takano, Y.; Narusaka, Y.; Shirasu, K. Genomic Plasticity Mediated by Transposable Elements in the Plant Pathogenic Fungus Colletotrichum higginsianum, Genome Biology and Evolution, Volume 11 (2019) no. 5, pp. 1487-1500 | Article

[112] Vuković, R.; Liber, Z.; Ježić, M.; Sotirovski, K.; Ćurković‐Perica, M. Link between epigenetic diversity and invasive status of south‐eastern European populations of phytopathogenic fungus Cryphonectria parasitica, Environmental Microbiology, Volume 21 (2019) no. 12, pp. 4521-4536 | Article

[113] Wang, Q.; Jiang, C.; Wang, C.; Chen, C.; Xu, J.-R.; Liu, H. Characterization of the Two-Speed Subgenomes of Fusarium graminearum Reveals the Fast-Speed Subgenome Specialized for Adaption and Infection, Frontiers in Plant Science, Volume 8 (2017) | Article

[114] Wang, Q.; Sun, M.; Zhang, Y.; Song, Z.; Zhang, S.; Zhang, Q.; Xu, J.; Liu, H. Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi, Molecular Plant Pathology, Volume 21 (2020) no. 3, pp. 330-348 | Article

[115] Wellenreuther, M.; Mérot, C.; Berdan, E.; Bernatchez, L. Going beyond SNPs: The role of structural genomic variants in adaptive evolution and species diversification, Molecular Ecology, Volume 28 (2019) no. 6, pp. 1203-1209 | Article

[116] Wicker, T.; Sabot, F.; Hua-Van, A.; Bennetzen, J. L.; Capy, P.; Chalhoub, B.; Flavell, A.; Leroy, P.; Morgante, M.; Panaud, O.; Paux, E.; SanMiguel, P.; Schulman, A. H. A unified classification system for eukaryotic transposable elements, Nature Reviews Genetics, Volume 8 (2007) no. 12, pp. 973-982 | Article

[117] Yadav, V.; Sun, S.; Coelho, M. A.; Heitman, J. Centromere scission drives chromosome shuffling and reproductive isolation, Proceedings of the National Academy of Sciences, Volume 117 (2020) no. 14, pp. 7917-7928 | Article

[118] Yoshida, K.; Saunders, D. G. O.; Mitsuoka, C.; Natsume, S.; Kosugi, S.; Saitoh, H.; Inoue, Y.; Chuma, I.; Tosa, Y.; Cano, L. M.; Kamoun, S.; Terauchi, R. Host specialization of the blast fungus Magnaporthe oryzae is associated with dynamic gain and loss of genes linked to transposable elements, BMC Genomics, Volume 17 (2016) no. 1 | Article

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