1887

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Volume 7, Issue 8

Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen Open Access

Abstract

The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi have evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point mutation (RIP) is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIPs is expected to deactivate TEs over the course of a few generations. The evolutionary dynamics of TEs at the population level in a species with highly repressive genome defences is poorly understood. Here, we analyse 366 whole-genome sequences of , a fungal pathogen of wheat with efficient RIP. A global population genomics analysis revealed high levels of genetic diversity and signs of frequent sexual recombination. Contrary to expectations for a species with RIP, we identified recent TE activity in multiple populations. The TE composition and copy numbers showed little divergence among global populations regardless of the demographic history. Miniature inverted-repeat transposable elements (MITEs) and terminal repeat retrotransposons in miniature (TRIMs) were largely underlying recent intra-species TE expansions. We inferred RIP footprints in individual TE families and found that recently active, high-copy TEs have possibly evaded genomic defences. We find no evidence that recent positive selection acted on TE-mediated mutations rather that purifying selection maintained new TE insertions at low insertion frequencies in populations. Our findings highlight the complex evolutionary equilibria established by the joint action of TE activity, selection and genomic repression.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): adaptation , genetic diversity , pathogen , repeat-induced point mutations , selfish elements and transposable elements
Funding
This study was supported by the:
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BR)
    • Principle Award Recipient: DaniloPereira
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-08-23
2024-04-18
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References

  1. Baranova MA, Logacheva MD, Penin AA, Seplyarskiy VB, Safonova YY et al. Extraordinary genetic diversity in a wood decay mushroom. Mol Biol Evol 2015; 32:2775–2783 [View Article] [PubMed]
     [Google Scholar]
  2. Goddard MR, Godfray HCJ, Burt A. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 2005; 434:636–640
     [Google Scholar]
  3. Wolfe KH, Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997; 387:708–713
     [Google Scholar]
  4. Horns F, Petit E, Hood ME. Massive expansion of Gypsy-like retrotransposons in Microbotryum fungi. Genome Biol Evol 2017; 9:363–371
     [Google Scholar]
  5. Kidwell MG. Transposable elements and the evolution of genome size in eukaryotes. Genetica 2002; 115:49–63
     [Google Scholar]
  6. De Cecco M, Criscione SW, Peckham EJ, Hillenmeyer S, Hamm EA et al. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 2013; 12:247–256 [View Article] [PubMed]
     [Google Scholar]
  7. Chen F, Everhart SE, Bryson PK, Luo C, Song X et al. Fungicide-induced transposon movement in Monilinia fructicola. Fungal Genet Biol 2015; 85:38–44 [View Article] [PubMed]
     [Google Scholar]
  8. Hedges DJ, Deininger PL. Inviting instability: transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat Res 2007; 616:46–59 [View Article] [PubMed]
     [Google Scholar]
  9. Burns KH, Boeke JD. Human transposon tectonics. Cell 2012; 149:740–752 [View Article] [PubMed]
     [Google Scholar]
  10. Chou H-H, Hayakawa T, Diaz S, Krings M, Indriati E et al. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci USA 2002; 99:11736–11741 [View Article] [PubMed]
     [Google Scholar]
  11. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH et al. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 2008; 17:3952–3971 [View Article] [PubMed]
     [Google Scholar]
  12. Raffaele S, Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 2012; 10:417–430 [View Article] [PubMed]
     [Google Scholar]
  13. Möller M, Stukenbrock EH. Evolution and genome architecture in fungal plant pathogens. Nat Rev Microbiol 2017; 15:756–771
     [Google Scholar]
  14. Seidl MF, Thomma BPHJ. Transposable elements direct the coevolution between plants and microbes. Trends Genet 2017; 33:842–851 [View Article] [PubMed]
     [Google Scholar]
  15. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 2010; 330:1543–1546 [View Article] [PubMed]
     [Google Scholar]
  16. Hartmann FE, Sánchez-Vallet A, McDonald BA, Croll D. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. ISME J 2017; 11:1189–1204 [View Article] [PubMed]
     [Google Scholar]
  17. Omrane S, Sghyer H, Audéon C, Lanen C, Duplaix C et al. Fungicide efflux and the MgMFS1 transporter contribute to the multidrug resistance phenotype in Zymoseptoria tritici field isolates. Environ Microbiol 2015; 17:2805–2823 [View Article] [PubMed]
     [Google Scholar]
  18. Steinhauer D, Salat M, Frey R, Mosbach A, Luksch T et al. A dispensable paralog of succinate dehydrogenase subunit C mediates standing resistance towards a subclass of SDHI fungicides in Zymoseptoria tritici. PLoS Pathog 2019; 15:e1007780 [View Article] [PubMed]
     [Google Scholar]
  19. Dutheil JY, Mannhaupt G, Schweizer G, M K Sieber C, Münsterkötter M et al. A tale of genome compartmentalization: the evolution of virulence clusters in smut fungi. Genome Biol Evol 2016; 8:681–704 [View Article] [PubMed]
     [Google Scholar]
  20. Faino L, Seidl MF, Shi-Kunne X, Pauper M, van den Berg GCM et al. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res 2016; 26:1091–1100 [View Article] [PubMed]
     [Google Scholar]
  21. Wang Q, Jiang C, Wang C, Chen C, Xu J-R et al. Characterization of the two-speed subgenomes of Fusarium graminearum reveals the fast-speed subgenome specialized for adaption and infection. Front Plant Sci 2017; 8:140 [View Article] [PubMed]
     [Google Scholar]
  22. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2011; 2:202 [View Article] [PubMed]
     [Google Scholar]
  23. Fouché S, Plissonneau C, Croll D. The birth and death of effectors in rapidly evolving filamentous pathogen genomes. Curr Opin Microbiol 2018; 46:34–42
     [Google Scholar]
  24. Richards JK, Stukenbrock EH, Carpenter J, Liu Z, Cowger C et al. Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States. PLoS Genet 2019; 15:e1008223 [View Article] [PubMed]
     [Google Scholar]
  25. Yoshida K, Saunders DGO, Mitsuoka C, Natsume S, Kosugi S et al. Host specialization of the blast fungus Magnaporthe oryzae is associated with dynamic gain and loss of genes linked to transposable elements. BMC Genomics 2016; 17:370 [View Article] [PubMed]
     [Google Scholar]
  26. Hartmann FE, Croll D. Distinct trajectories of massive recent gene gains and losses in populations of a microbial eukaryotic pathogen. Mol Biol Evol 2017; 34:2808–2822
     [Google Scholar]
  27. Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 2009; 19:1419–1428
     [Google Scholar]
  28. Nolan T. The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res 2005; 33:1564–1573
     [Google Scholar]
  29. Gladyshev E. Repeat-induced point mutation and other genome defense mechanisms in fungi. Microbiol Spectr 2017; 5:FUNK-0042-2017 [View Article] [PubMed]
     [Google Scholar]
  30. Selker EU. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 1990; 24:579–613
     [Google Scholar]
  31. Ikeda K, Nakayashiki H, Kataoka T, Tamba H, Hashimoto Y. Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context: repeat-induced point mutation in Magnaporthe grisea. Mol Microbiol 2002; 45:1355–1364
     [Google Scholar]
  32. Hane JK, Oliver RP. RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinform 2008; 9:478
     [Google Scholar]
  33. Fudal I, Ross S, Brun H, Besnard A-. L, Ermel M et al. Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward vi rulence in Leptosphaeria maculans. Mol Plant Microbe Interact 2009; 22:932–941
     [Google Scholar]
  34. Dhillon B, Gill N, Hamelin RC, Goodwin SB. The landscape of transposable elements in the finished genome of the fungal wheat pathogen Mycosphaerella graminicola. BMC Genom 2014; 15:1132
     [Google Scholar]
  35. Van de Wouw AP, Elliott CE, Popa KM, Idnurm A. Analysis of repeat induced point (RIP) mutations in Leptosphaeria maculans indicates variability in the RIP process between fungal species. Genetics 2019; 211:89–104 [View Article] [PubMed]
     [Google Scholar]
  36. Plissonneau C, Hartmann FE, Croll D. Pangenome analyses of the wheat pathogen Zymoseptoria tritici reveal the structural basis of a highly plastic eukaryotic genome. BMC Biol 2018; 16:5 [View Article]
     [Google Scholar]
  37. Syme RA, Tan K-C, Rybak K, Friesen TL, McDonald BA et al. Pan-Parastagonospora comparative genome analysis – effector prediction and genome evolution. Genome Biol Evol 2018; 10:2443–2457 [View Article] [PubMed]
     [Google Scholar]
  38. Wyatt NA, Richards JK, Brueggeman RS, Friesen TL. Reference assembly and annotation of the Pyrenophora teres f. teres isolate 0-1. G3 2018; 8:g3.117.300196 [View Article] [PubMed]
     [Google Scholar]
  39. Badet T, Oggenfuss U, Abraham L, McDonald BA, Croll D. A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici. BMC Biol 2020; 18:12 [View Article] [PubMed]
     [Google Scholar]
  40. Oggenfuss U, Badet T, Wicker T, Hartmann FE, Singh NK et al. A population-level invasion by transposable elements in a fungal pathogen. bioRxiv 2020944652
     [Google Scholar]
  41. Fouché S, Badet T, Oggenfuss U, Plissonneau C, Francisco CS et al. Stress-driven transposable element de-repression dynamics and virulence evolution in a fungal pathogen. Mol Biol Evol 2020; 37:221–239 [View Article] [PubMed]
     [Google Scholar]
  42. Smith KM, Phatale PA, Bredeweg EL, Connolly LR, Pomraning KR et al. Epigenetics of filamentous fungi. In Meyers R. eds Encyclopedia of Molecular Cell Biology and Molecular Medicine Weinheim: Wiley-VCH Verlag; 2012
     [Google Scholar]
  43. Pereira D, McDonald BA, Croll D. The genetic architecture of emerging fungicide resistance in populations of a global wheat pathogen. Genome Biol Evol 2020; 12:2231–2244 [View Article] [PubMed]
     [Google Scholar]
  44. Pereira D, Croll D, Brunner PC, McDonald BA. Natural selection drives population divergence for local adaptation in a wheat pathogen. Fungal Genet Biol 2020; 141:103398 [View Article]
     [Google Scholar]
  45. Oliver R, Friesen T, Faris J, Solomon P. Stagonospora nodorum: from pathology to genomics and host resistance. Annu Rev Phytopathol 2012; 50:23–43
     [Google Scholar]
  46. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 2006; 38:953–956 [View Article] [PubMed]
     [Google Scholar]
  47. McDonald MC, Taranto AP, Hill E, Schwessinger B, Liu Z et al. Transposon-mediated horizontal transfer of the host-specific virulence protein ToxA between three fungal wheat pathogens. mBio 2019; 10:e01515-19 [View Article] [PubMed]
     [Google Scholar]
  48. Hane JK, Lowe RGT, Solomon PS, Tan K-. C, Schoch CL et al. Dothideomycete–plant interactions illuminated by genome sequencing and EST analysis of the wheat pa thogen Stagonospora nodorum. Plant Cell 2007; 19:3347–3368
     [Google Scholar]
  49. Hane JK, Oliver RP. In silico reversal of repeat-induced point mutation (RIP) identifies the origins of repeat families and uncovers obscured duplicated genes. BMC Genom 2010; 11:655
     [Google Scholar]
  50. Sommerhalder RJ, McDonald BA, Zhan J. The frequencies and spatial distribution of mating types in Stagonospora nodorum are consistent with recurring sexual reproduction. Phytopathology 2006; 96:234–239
     [Google Scholar]
  51. Stukenbrock EH, Banke S, McDonald BA. Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Mol Ecol 2006; 15:2895–2904
     [Google Scholar]
  52. McDonald MC, Razavi M, Friesen TL, Brunner PC, McDonald BA. Phylogenetic and population genetic analyses of Phaeosphaeria nodorum and its close relatives indicate cryptic species and an origin in the Fertile Crescent. Fungal Genet Biol 2012; 49:882–895 [View Article] [PubMed]
     [Google Scholar]
  53. McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA. Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol 2013; 199:241–251 [View Article] [PubMed]
     [Google Scholar]
  54. Pereira DA, McDonald BA, Brunner PC. Mutations in the CYP51 gene reduce DMI sensitivity in Parastagonospora nodorum populations in Europe and China. Pest Manag Sci 2017; 73:1503–1510
     [Google Scholar]
  55. Bolger A, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120
     [Google Scholar]
  56. Richards JK, Wyatt NA, Liu Z, Faris JD, Friesen TL. Reference quality genome assemblies of three Parastagonospora nodorum isolates differing in virulence on wheat. G3 2018; 8:393–399 [View Article] [PubMed]
     [Google Scholar]
  57. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
     [Google Scholar]
  58. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
     [Google Scholar]
  59. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [View Article] [PubMed]
     [Google Scholar]
  60. Danecek P, Auton A, Abecasis G, Albers CA, Banks E et al. The variant call format and VCFtools. Bioinformatics 2011; 27:2156–2158 [View Article] [PubMed]
     [Google Scholar]
  61. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313
     [Google Scholar]
  62. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006; 23:254–267
     [Google Scholar]
  63. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259
     [Google Scholar]
  64. Lischer HEL, Excoffier L. PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 2012; 28:298–299
     [Google Scholar]
  65. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000; 155:945–959
     [Google Scholar]
  66. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 2007; 23:2633–2635 [View Article] [PubMed]
     [Google Scholar]
  67. R Core TeamR: a language and environment for statistical computing Vienna: R Foundation for Statistical Computing; 2019 https://www.R-project.org
  68. Wickham H. ggplot2: Elegant Graphics for Data Analysis, 2nd edn. New York: Springer; 2009
     [Google Scholar]
  69. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005; 14:2611–2620
     [Google Scholar]
  70. Francis RM. pophelper: an R package and web app to analyse and visualize population structure. Mol Ecol Resour 2017; 17:27–32 [View Article] [PubMed]
     [Google Scholar]
  71. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989; 123:585–595
     [Google Scholar]
  72. Pavlidis P, Živkovic D, Stamatakis A, Alachiotis N. SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol Biol Evol 2013; 30:2224–2234
     [Google Scholar]
  73. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842
     [Google Scholar]
  74. Jones P, Binns D, Chang H-Y, Fraser M, Li W et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014; 30:1236–1240 [View Article] [PubMed]
     [Google Scholar]
  75. Nielsen H. Predicting secretory proteins with signalP. In Kihara D. ed Protein Function Prediction New York: Springer; 2017 pp 59–73
     [Google Scholar]
  76. Käll L, Krogh A, Sonnhammer ELL. A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004; 338:1027–1036
     [Google Scholar]
  77. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580
     [Google Scholar]
  78. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007; 23:257–258
     [Google Scholar]
  79. Bao W, Kojima KK, Kohany O. Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA 2015; 6:11 [View Article] [PubMed]
     [Google Scholar]
  80. Smit AFA, Hubley R, Green P. RepeatMasker Open-4.0 ( http://www.repeatmasker.org) 2013
  81. Breen JM, Wicker T, Kong X, Zhang J, Ma W et al. A highly conserved gene island of three genes on chromosome 3B of hexaploid wheat: diverse gene function and genomic structure maintained in a tightly linked block. BMC Plant Biol 2010; 10:98 [View Article] [PubMed]
     [Google Scholar]
  82. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
     [Google Scholar]
  83. Higgins DG, Sharp PM. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 1988; 73:237–244
     [Google Scholar]
  84. Sonnhammer ELL, Durbin R. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 1995; 167:GC1–GC10 [View Article] [PubMed]
     [Google Scholar]
  85. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet 2007; 8:973–982 [View Article] [PubMed]
     [Google Scholar]
  86. Guy L, Kultima JR, Andersson SGE. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 2010; 26:2334–2335
     [Google Scholar]
  87. Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R et al. Database indexing for production MegaBLAST searches. Bioinformatics 2008; 24:1757–1764 [View Article] [PubMed]
     [Google Scholar]
  88. Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol 2000; 7:203–214
     [Google Scholar]
  89. Madeira F, Park YM, Lee J, Buso N, Gur T et al. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 2019; 47:W636–W641 [View Article] [PubMed]
     [Google Scholar]
  90. Linheiro RS, Bergman CM. Whole genome resequencing reveals natural target site preferences of transposable elements in Drosophila melanogaster. PloS One 2012; 7:e30008
     [Google Scholar]
  91. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760
     [Google Scholar]
  92. Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M et al. Software for computing and annotating genomic ranges. PLoS Comput Biol 2013; 9:e1003118 [View Article] [PubMed]
     [Google Scholar]
  93. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 2012; 8:e1003037 [View Article] [PubMed]
     [Google Scholar]
  94. Watters MK, Randall TA, Margolin BS, Selker EU, Stadler DR. Action of repeat-induced point mutation on both strands of a duplex and on tandem duplications of various sizes in Neurospora. Genetics 1999; 153:705–714 [PubMed]
     [Google Scholar]
  95. Croll D, McDonald BA. The genetic basis of local adaptation for pathogenic fungi in agricultural ecosystems. Mol Ecol 2017; 26:2027–2040
     [Google Scholar]
  96. McDonald BA, Linde C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 2002; 40:349–379
     [Google Scholar]
  97. Stritt C, Gordon SP, Wicker T, Vogel JP, Roulin AC. Recent activity in expanding populations and purifying selection have shaped transposable element landscapes across natural accessions of the Mediterranean grass Brachypodium distachyon. Genome Biol Evol 2018; 10:304–318
     [Google Scholar]
  98. Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA. Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 2007; 24:398–411 [View Article] [PubMed]
     [Google Scholar]
  99. Möller M, Habig M, Lorrain C, Feurtey A, Haueisen J et al. Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen. bioRxiv 2020012203
     [Google Scholar]
  100. Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA et al. The Arabidopsis thaliana mobilome and its impact at the species level. eLife 2016; 5:e15716 [View Article] [PubMed]
     [Google Scholar]
  101. Badouin H, Gladieux P, Gouzy J, Siguenza S, Aguileta G et al. Widespread selective sweeps throughout the genome of model plant pathogenic fungi and identification of effector candidates. Mol Ecol 2017; 26:2041–2062 [View Article] [PubMed]
     [Google Scholar]
  102. Mohd-Assaad N, McDonald BA, Croll D. Genome-Wide detection of genes under positive selection in worldwide populations of the barley scald pathogen. Genome Biol Evol 2018; 10:1315–1332 [View Article] [PubMed]
     [Google Scholar]
  103. Muszewska A, Steczkiewicz K, Stepniewska-Dziubinska M, Ginalski K. Cut-and-paste transposons in fungi with diverse lifestyles. Genome Biol Evol 2017; 9:3463–3477 [View Article]
     [Google Scholar]
  104. Santana MF, Silva JCF, Mizubuti ESG, Araújo EF, Queiroz MV. Analysis of Tc1-Mariner elements in Sclerotinia sclerotiorum suggests recent activity and flexible transposases. BMC Microbiol 2014; 14:256 [View Article] [PubMed]
     [Google Scholar]
  105. Amselem J, Lebrun M-H, Quesneville H. Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes. BMC Genom 2015; 16:141 [View Article]
     [Google Scholar]
  106. Wang L, Sun Y, Sun X, Yu L, Xue L et al. Repeat-induced point mutation in Neurospora crassa causes the highest known mutation rate and mutational burden of any cellular life. Genome Biol 2020; 21:142 [View Article]
     [Google Scholar]
  107. Yeadon PJ, Catcheside DEA. Guest: a 98 bp inverted repeat transposable element in Neurospora crassa. Mol Gen Genet 1995; 247:105–109 [View Article] [PubMed]
     [Google Scholar]
  108. Cambareri EB, Singer MJ, Selker EU. Recurrence of repeat-induced point mutation (RIP) in Neurospora crassa. Genetics 1991; 127:699–710 [View Article] [PubMed]
     [Google Scholar]
  109. Witte C-P, Le QH, Bureau T, Kumar A. Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 2001; 98:13778–13783 [View Article] [PubMed]
     [Google Scholar]
  110. Santiago N, Herráiz C, Goñi JR, Messeguer X, Casacuberta JM. Genome-wide analysis of the emigrant family of MITEs of Arabidopsis thaliana. Mol Biol Evol 2002; 19:2285–2293 [View Article] [PubMed]
     [Google Scholar]
  111. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 2009; 461:1130–1134 [View Article] [PubMed]
     [Google Scholar]
  112. Feschotte C, Swamy L, Wessler SR. Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). Genetics 2003; 163:747–758 [PubMed]
     [Google Scholar]
  113. Feschotte C, Pritham EJ. DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 2007; 41:331–368 [View Article] [PubMed]
     [Google Scholar]
  114. Kang S, Lebrun MH, Farrall L, Valent B. Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol Plant Microbe Interact 2001; 14:671–674 [View Article] [PubMed]
     [Google Scholar]
  115. Wachter S, Raghavan R, Wachter J, Minnick MF. Identification of novel MITEs (miniature inverted-repeat transposable elements) in Coxiella burnetii: implications for protein and small RNA evolution. BMC Genomics 2018; 19:247 [View Article] [PubMed]
     [Google Scholar]
  116. Lu C, Chen J, Zhang Y, Hu Q, Su W et al. Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol 2012; 29:1005–1017 [View Article] [PubMed]
     [Google Scholar]
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Population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen
M Gen 7, 000540 (2021); https://doi.org/10.1099/mgen.0.000540
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