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Biology, dynamics, and applications of transposable elements in basidiomycete fungi

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Abstract

The phylum Basidiomycota includes filamentous fungi and yeast species with different ecological and genomic characteristics. Transposable elements (TEs) are abundant components of most eukaryotic genomes, and their transition from being genomic parasites to key drivers of genomic architecture, functionality, and evolution is a subject receiving much attention. In light of the abundant genomic information released during the last decade, the aims of this mini-review are to discuss the dynamics and impact of TEs in basidiomycete fungi. To do this, we surveyed and explored data from 75 genomes, which encompass the phylogenetic diversity of the phylum Basidiomycota. We describe annotation approaches and analyze TE distribution in the context of species phylogeny and genome size. Further, we review the most relevant literature about the role of TEs in species lifestyle, their impact on genome architecture and functionality, and the defense mechanisms evolved to control their proliferation. Finally, we discuss potential applications of TEs that can drive future innovations in fungal research

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References

  • Alfaro M, Oguiza JA, Ramírez L, Pisabarro AG (2014) Comparative analysis of secretomes in basidiomycete fungi. J Proteome 102:28–43

    Article  CAS  Google Scholar 

  • Ali S, Laurie JD, Linning R, Cervantes-Chávez JA, Gaudet D, Bakkeren G (2014) An immunity-triggering effector from the barley smut fungus Ustilago hordei resides in an Ustilaginaceae-specific cluster bearing signs of transposable element-assisted evolution. PLoS Pathog. doi:10.1371/journal.ppat.1004223

    Google Scholar 

  • Amselem J, Lebrun M-H, Quesneville H (2015) Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes. BMC Genomics 16:141. doi:10.1186/s12864-015-1347-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Bao D, Gong M, Zheng H, Chen M, Zhang L, Wang H, Jiang J, Wu L, Zhu Y, Zhu G, Zhou Y, Li C, Wang S, Zhao Y, Zhao G, Tan Q (2013) Sequencing and comparative analysis of the straw mushroom (Volvariella volvacea) genome. PLoS One. doi:10.1371/journal.pone.0058294

    Google Scholar 

  • Binder M, Justo a, Riley R, Salamov a, Lopez-Giraldez F, Sjokvist E, Copeland a, Foster B, Sun H, Larsson E, Larsson K-H, Townsend J, Grigoriev IV, Hibbett DS (2013) Phylogenetic and phylogenomic overview of the Polyporales. Mycologia 105:1350–1373. doi:10.3852/13-003

    Article  CAS  PubMed  Google Scholar 

  • Binz T, D’Mello N, Horgen PA (1998) A comparison of DNA methylation levels in selected isolates of higher fungi. Mycologia 90:785. doi:10.2307/3761319

    Article  CAS  Google Scholar 

  • Branco S, Gladieux P, Ellison CE, Kuo A, Labutti K, Lipzen A, Grigoriev IV, Liao HL, Vilgalys R, Peay KG, Taylor JW, Bruns TD (2015) Genetic isolation between two recently diverged populations of a symbiotic fungus. Mol Ecol 24:2747–2758. doi:10.1111/mec.13132

    Article  CAS  PubMed  Google Scholar 

  • Canapa A, Barucca M, Biscotti MA, Forconi M, Olmo E (2016) Transposons, genome size, and evolutionary insights in animals. Cytogenet Genome Res 147:217–239

    Article  Google Scholar 

  • Cantu D, Govindarajulu M, Kozik A, Wang M, Chen X, Kojima KK, Jurka J, Michelmore RW, Dubcovsky J (2011) Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One. doi:10.1371/journal.pone.0024230

    PubMed  PubMed Central  Google Scholar 

  • Castanera R, López-Varas L, Borgognone A, LaButti K, Lapidus A, Schmutz J, Grimwood J, Pérez G, Pisabarro AG, Grigoriev IV, Stajich JE, Ramírez L (2016) Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLoS Genet 12:e1006108. doi:10.1371/journal.pgen.1006108

    Article  PubMed  PubMed Central  Google Scholar 

  • Castanera R, Pérez G, López L, Sancho R, Santoyo F, Alfaro M, Gabaldón T, Pisabarro AG, Oguiza JA, Ramírez L (2014) Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi. BMC Genomics 15:1071. doi:10.1186/1471-2164-15-1071

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S, Xu J, Liu C, Zhu Y, Nelson DR, Zhou S, Li C, Wang L, Guo X, Sun Y, Luo H, Li Y, Song J, Henrissat B, Levasseur A, Qian J, Li J, Luo X, Shi L, He L, Xiang L, Xu X, Niu Y, Li Q, Han MV, Yan H, Zhang J, Chen H, Lv A, Wang Z, Liu M, Schwartz DC, Sun C (2012) Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 3:913. doi:10.1038/ncomms1923

    Article  PubMed  PubMed Central  Google Scholar 

  • Chénais B, Caruso A, Hiard S, Casse N (2012) The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene. doi:10.1016/j.gene.2012.07.042

    PubMed  Google Scholar 

  • Daboussi M-J, Capy P (2003) Transposable elements in filamentous fungi. Annu Rev Microbiol 57:275–299. doi:10.1146/annurev.micro.57.030502.091029

    Article  CAS  PubMed  Google Scholar 

  • Díez J, Béguiristain T, Le Tacon F, Casacuberta JM, Tagu D, Jesu TB, Tacon L (2003) Identification of Ty1-copia retrotransposons in three ectomycorrhizal basidiomycetes: evolutionary relationships and use as molecular markers. Curr Genet 43:34–44. doi:10.1007/s00294-002-0363-2

    PubMed  Google Scholar 

  • Dioh W, Tharreau D, Notteghem JL, Orbach M, Lebrun MH (2000) Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol Plant-Microbe Interact 13:217–227. doi:10.1094/MPMI.2000.13.2.217

    Article  CAS  PubMed  Google Scholar 

  • Duplessis S, Cuomo CA, Lin Y-C, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, Chiu R, Coutinho PM, Feaue N, Field M, Frey P, Gelhaye E, Goldberg J, Grabherr MG, Kodira CD, Kohler A, Kües U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Murat C, Pangilinan JL, Park R, Pearson M, Quesneville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan GA, Henrissat B, Van De Peer Y, Rouzé P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A 108:9166–9171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutheil JY, Mannhaupt G, Schweizer G, Sieber CM, Münsterkötter M, Güldener U, Schirawski J, Kahmann R (2016) A tale of genome compartmentalization: the evolution of virulence clusters in smut fungi. Genome Biol Evol 8:681–704. doi:10.1093/gbe/evw026

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellinghaus D, Kurtz S, Willhoeft U (2008) LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9:18. doi:10.1186/1471-2105-9-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, Asiegbu FO, Baker SE, Barry K, Bendiksby M, Blumentritt M, Coutinho PM, Cullen D, De Vries RP, Gathman A, Goodell B, Henrissat B, Ihrmark K, Kauserud H, Kohler A, LaButti K, Lapidus A, Lavin JL, Lee Y-H, Lindquist E, Lilly W, Lucas S, Morin E, Murat C, Oguiza JA, Park J, Pisabarro AG, Riley R, Rosling A, Salamov A, Schmidt O, Schmutz J, Skrede I, Stenlid J, Wiebenga A, Xie X, Kües U, Hibbett DS, Hoffmeister D, Högberg N, Martin F, Grigoriev IV, Watkinson SC (2011) The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333(80):762–765

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Fueyo E, Ruiz-Dueñas FJ, Ferreira P, Floudas D, Hibbett DS, Canessa P, Larrondo LF, James TY, Seelenfreund D, Lobos S, Polanco R, Tello M, Honda Y, Watanabe T, Ryu JS, Kubicek CP, Schmoll M, Gaskell J, Hammel KE, St John FJ, Vanden Wymelenberg A, Sabat G, SS BD, Syed K, Yadav JS, Doddapaneni H, Subramanian V, Lavín JL, Oguiza JA, Perez G, Pisabarro AG, Ramirez L, Santoyo F, Master E, Coutinho PM, Henrissat B, Lombard V, Magnuson JK, Kües U, Hori C, Igarashi K, Samejima M, Held BW, Barry KW, KM LB, Lapidus A, Lindquist EA, Lucas SM, Riley R, Salamov AA, Hoffmeister D, Schwenk D, Hadar Y, Yarden O, De Vries RP, Wiebenga A, Stenlid J, Eastwood D, Grigoriev IV, Berka RM, Blanchette RA, Kersten P, Martinez AT, Vicuna R, Cullen D (2012) Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis (Proceedings of the National Academy of Sciences (2012) 109 (5458-5463) DOI: 10.1073/pnas. 1119912109). Proc Natl Acad Sci U S A 109:8352

    Article  CAS  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42

  • Firrincieli A, Otillar R, Salamov A, Schmutz J, Khan Z, Redman RS, Fleck ND, Lindquist E, Grigoriev IV, Doty SL (2015) Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1. Front Microbiol 6:978. doi:10.3389/fmicb.2015.00978

    Article  PubMed  PubMed Central  Google Scholar 

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Gorecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kues U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Duenas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St. John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(80):1715–1719. doi:10.1126/science.1221748

    Article  CAS  PubMed  Google Scholar 

  • Flutre T, Duprat E, Feuillet C, Quesneville H (2011) Considering transposable element diversification in de novo annotation approaches. PLoS One. doi:10.1371/journal.pone.0016526

    PubMed  PubMed Central  Google Scholar 

  • Foulongne-Oriol M, Murat C, Castanera R, Ramírez L, Sonnenberg ASM (2013) Genome-wide survey of repetitive DNA elements in the button mushroom Agaricus bisporus. Fungal Genet Biol 55:6–21

    Article  CAS  PubMed  Google Scholar 

  • Fowler TJ, Mitton MF (2000) Scooter, a new active transposon in Schizophyllum commune, has disrupted two genes regulating signal transduction. Genetics 156:1585–1594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaskell J, Van den Wymelenberg A, Cullen D (1995) Structure, inheritance, and transcriptional effects of Pce1, an insertional element within Phanerochaete chrysosporium lignin peroxidase gene lipI. Proc Natl Acad Sci U S A 92:7465–7469. doi:10.1073/pnas.92.16.7465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, Smirnova T, Nordberg H, Dubchak I, Shabalov I (2014) MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. doi:10.1093/nar/gkt1183

    Google Scholar 

  • Hane JK, Anderson JP, Williams AH, Sperschneider J, Singh KB (2014) Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet. doi:10.1371/journal.pgen.1004281

    PubMed  PubMed Central  Google Scholar 

  • Hess J, Skrede I, Wolfe BE, Butti KL, Ohm RA, Grigoriev IV, Pringle A (2014) Transposable element dynamics among asymbiotic and ectomycorrhizal Amanita fungi. Genome Biol Evol 6:1564–1578. doi:10.1093/gbe/evu121

    Article  PubMed  PubMed Central  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547. doi:10.1016/j.mycres.2007.03.004

    Article  PubMed  Google Scholar 

  • Hoede C, Arnoux S, Moisset M, Chaumier T, Inizan O, Jamilloux V, Quesneville H (2014) PASTEC: an automatic transposable element classification tool. PLoS One. doi:10.1371/journal.pone.0091929

    Google Scholar 

  • Hood ME (2005) Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124:1–10. doi:10.1007/s10709-004-6615-y

    Article  CAS  PubMed  Google Scholar 

  • Horns F, Petit E, Yockteng R, Hood ME (2012) Patterns of repeat-induced point mutation in transposable elements of basidiomycete fungi. Genome Biol Evol 4:240–247. doi:10.1093/gbe/evs005

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu G, Kronstad JW (2006) Gene disruption in Cryptococcus neoformans and Cryptococcus gattii by in vitro transposition. Curr Genet 49:341–350. doi:10.1007/s00294-005-0054-x

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Stenlid J, Elfstrand M, Olson A (2013) Evolution of RNA interference proteins dicer and argonaute in Basidiomycota. Mycologia 105:1489–1498. doi:10.3852/13-171

    Article  CAS  PubMed  Google Scholar 

  • Hua-Van A, Pamphile JA, Langin T, Daboussi MJ (2001) Transposition of autonomous and engineered impala transposons in Fusarium oxysporum and a related species. Mol Gen Genet 264:724–731. doi:10.1007/s004380000395

    Article  CAS  PubMed  Google Scholar 

  • Janbon G, Ormerod KL, Paulet D, Byrnes EJ, Yadav V, Chatterjee G, Mullapudi N, Hon CC, Billmyre RB, Brunel F, Bahn YS, Chen W, Chen Y, Chow EWL, Coppée JY, Floyd-Averette A, Gaillardin C, Gerik KJ, Goldberg J, Gonzalez-Hilarion S, Gujja S, Hamlin JL, Hsueh YP, Ianiri G, Jones S, Kodira CD, Kozubowski L, Lam W, Marra M, Mesner LD, Mieczkowski PA, Moyrand F, Nielsen K, Proux C, Rossignol T, Schein JE, Sun S, Wollschlaeger C, Wood IA, Zeng Q, Neuvéglis C, Newlon CS, Perfect JR, Lodge JK, Idnurm A, Stajich JE, Kronstad JW, Sanyal K, Heitman J, Fraser JA, Cuomo CA, Dietrich FS (2014) Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet. doi:10.1371/journal.pgen.1004261

    PubMed  PubMed Central  Google Scholar 

  • Jeon J, Choi J, Lee G-W, Park S-Y, Huh A, Dean R a, Lee Y-H (2015) Genome-wide profiling of DNA methylation provides insights into epigenetic regulation of fungal development in a plant pathogenic fungus, Magnaporthe oryzae. Sci Rep 5:8567. doi:10.1038/srep08567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467. doi:10.1159/000084979

    Article  CAS  PubMed  Google Scholar 

  • Kalendar R (2011) The use of retrotransposon-based molecular markers to analyze genetic diversity. Ratar i Povrt 48:261–274. doi:10.5937/ratpov1102261K

    Article  Google Scholar 

  • Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Mülle O, Perlin MH, Wösten HAB, de Vries R, Ruiz-Herrera J, Reynaga-Peña CG, Snetselaar K, McCann M, Pérez-Martín J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, González-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Münch K, Rössel N, Scherer M, Vraneš M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho ECH, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Häuser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schlüter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Güldener U, Münsterkötter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444 (7115):97–101

  • Kempken F, Kück U (1996) Restless, an active Ac-like transposon from the fungus Tolypocladium inflatum: structure, expression, and alternative RNA splicing. Mol Cell Biol 16:6563–6572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A, Colpaert J, Copeland A, Costa MD, Doré J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Högberg N, Johansson T, Khouja H-R, LaButti K, Lahrmann U, Levasseur A, Lindquist EA, Lipzen A, Marmeisse R, Martino E, Murat C, Ngan CY, Nehls U, Plett JM, Pringle A, Ohm RA, Perotto S, Peter M, Riley R, Rineau F, Ruytinx J, Salamov A, Shah F, Sun H, Tarkka M, Tritt A, Veneault-Fourrey C, Zuccaro A, Tunlid A, Grigoriev IV, Hibbett DS, Martin F (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415. doi:10.1038/ng.3223

    Article  CAS  PubMed  Google Scholar 

  • Konishi M, Hatada Y, Horiuchi J.-i (2013) Draft genome sequence of the Basidiomycetous yeast-Like Fungus Pseudozyma hubeiensis SY62, which produces an abundant amount of the biosurfactant mannosylerythritol lipids. Genome Announcements 1(4):e00409-13-e00409-13

  • Kourist R, Bracharz F, Lorenzen J, Kracht ON, Chovatia M, Daum C, Deshpande S, Lipzen A, Nolan M, Ohm RA, Grigoriev IV, Sun S, Heitman J, Brück T, Nowrousian M (2015) Genomics and transcriptomics analyses of the oil-accumulating basidiomycete yeast Trichosporon oleaginosus: insights into substrate utilization and alternative evolutionary trajectories of fungal mating systems. MBio. doi:10.1128/mBio.00918-15

    PubMed  PubMed Central  Google Scholar 

  • Labbe J, Murat C, Morin E, Tuskan GA, Le Tacon F, Martin F (2012) Characterization of transposable elements in the ectomycorrhizal fungus Laccaria bicolor. PLoS One 7:e40197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladendorf O, Brachmann A, Kämper J (2003) Heterologous transposition in Ustilago maydis. Mol Gen Genomics 269:395–405. doi:10.1007/s00438-003-0848-9

    Article  CAS  Google Scholar 

  • Laurie JD, Ali S, Linning R, Mannhaupt G, Wong P, Güldener U, Münsterkötter M, Moore R, Kahmann R, Bakkeren G, Schirawski J (2012) Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24:1733–1745. doi:10.1105/tpc.112.097261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le QV, Won HK, Lee TS, Lee CY, Lee HS, Ro HS (2008) Retrotransposon microsatellite amplified polymorphism strain fingerprinting markers applicable to various mushroom species. Mycobiology 36:161–166. doi:10.4489/MYCO.2008.36.3.161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S-I, Kim N-S (2014) Transposable elements and genome size variations in plants. Genomics Inform 12:87–97. doi:10.5808/GI.2014.12.3.87

    Article  PubMed  PubMed Central  Google Scholar 

  • Lerat E (2010) Identifying repeats and transposable elements in sequenced genomes: how to find your way through the dense forest of programs. Heredity (Edinb) 104:520–533. doi:10.1038/hdy.2009.165

    Article  CAS  Google Scholar 

  • Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA, Allen JE, Bosdet IE, Brent MR, Chiu R, Doering TL, Dontin MJ, D’Souza CA, Fox DS, Grinberg V, Fu JM, Fukushima M, Haas BJ, Huang JC, Janbon G, Jones SJM, Koo HL, Krzywinski MI, Kwon-Chung JK, Lengeler KB, Maiti R (2005) The genome of the Basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307(80):1321–1324. doi:10.1126/science.1103773

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch M (2007) The origins of genome architecture 2007. Sinauer, Sunderland

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(80):1401–1404. doi:10.1126/science.1089370

    Article  CAS  PubMed  Google Scholar 

  • Martin F, Aerts A, Ahrén D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452(7183):88–92

  • Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury J-M, Ballario P, Bolchi A, Brenna A, Brun A, Buee M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, Hilselberger B, Iotti M, Marcais B, Mello A, Miranda M, Pacioni G, Quesneville H, Riccioni C, Ruotolo R, Splivallo R, Stocchi V, Tisserant E, Viscomi AR, Zambonelli A, Zampieri E, Henrissat B, Lebrun M-H, Paolocci F, Bonfante P, Ottonello S, Wincker P (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038. doi:10.1038/nature08867

    Article  CAS  PubMed  Google Scholar 

  • Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700. doi:10.1038/nbt967

    Article  CAS  PubMed  Google Scholar 

  • McCarthy EM, McDonald JF (2003) LTR STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics 19:362–367. doi:10.1093/bioinformatics/btf878

    Article  CAS  PubMed  Google Scholar 

  • Migheli Q, Laugé R, Davière JM, Gerlinger C, Kaper F, Langin T, Daboussi MJ (1999) Transposition of the autonomous Fot1 element in the filamentous fungus Fusarium oxysporum. Genetics 151:1005–1013

    CAS  PubMed  PubMed Central  Google Scholar 

  • Min B, Park H, Jang Y, Kim JJ, Kim KH, Pangilinan J, Lipzen A, Riley R, Grigoriev IV, Spatafora JW, Choi IG (2015) Genome sequence of a white rot fungus Schizopora paradoxa KUC8140 for wood decay and mycoremediation. J Biotechnol 211:42–43. doi:10.1016/j.jbiotec.2015.06.426

    Article  CAS  PubMed  Google Scholar 

  • Montanini B, Chen P-Y, Morselli M, Jaroszewicz A, Lopez D, Martin F, Ottonello S, Pellegrini M (2014) Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content. Genome Biol 15:411. doi:10.1186/s13059-014-0411-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V, Nagy LG, Ohm RA, Patyshakuliyeva A, Brun A, Aerts AL, Bailey AM, Billette C, Coutinho PM, Deakin G, Doddapaneni H, Floudas D, Grimwood J, Hildén K, Kües U, Labutti KM, Lapidus A, Lindquist EA, Lucas SM, Murat C, Riley RW, Salamov AA, Schmutz J, Subramanian V, Wösten HAB, Xu J, Eastwood DC, Foster GD, Sonnenberg ASM, Cullen D, de Vries RP, Lundell T, Hibbett DS, Henrissat B, Burton KS, Kerrigan RW, Challen MP, Grigoriev IV, Martin F (2012) Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci U S A 109:17501–17506. doi:10.1073/pnas.1206847109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morita T, Koike H, Koyama Y, Hagiwara H, Ito E, Fukuoka T, Imura T, Machida M, Kitamoto D (2013) Genome sequence of the Basidiomycetous yeast Pseudozyma antarctica T-34, a producer of the glycolipid biosurfactants mannosylerythritol lipids. Genome Announcements 1(2):e00064-13-e00064-13

  • Murata H, Babasaki K, Yamada A (2005) Highly polymorphic DNA markers to specify strains of the ectomycorrhizal basidiomycete Tricholoma matsutake based on sigmamarY1, the long terminal repeat of gypsy-type retroelement marY1. Mycorrhiza 15:179–186. doi:10.1007/s00572-004-0319-0

    Article  CAS  PubMed  Google Scholar 

  • Murata H, Miyazaki Y, Babasaki K (2001) The Long Terminal Repeat (LTR) sequence of marY1, a retroelement from the ectomycorrhizal homobasidiomycete Tricholoma matsutake, is highly conserved in various higher fungi. Bioscience, Biotechnology, and Biochemistry 65(10):2297-2300

  • Muszewska A, Hoffman-Sommer M, Grynberg M (2011) LTR retrotransposons in fungi. PLoS One 6:e29425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muszewska A, Steczkiewicz K, Ginalski K (2013) DIRS and Ngaro retrotransposons in fungi. PLoS One. doi:10.1371/journal.pone.0076319

    PubMed  PubMed Central  Google Scholar 

  • Nemri A, Saunders DGO, Anderson C, Upadhyaya NM, Win J, Lawrence GJ, Jones DA, Kamoun S, Ellis JG, Dodds PN (2014) The genome sequence and effector complement of the flax rust pathogen Melampsora lini. Front Plant Sci 5:98. doi:10.3389/fpls.2014.00098

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohm RA, De Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, De Vries RP, Record E, Levasseur A, Baker SE, Bartholomew KA, Coutinho PM, Erdmann S, Fowler TJ, Gathman AC, Lombard V, Henrissat B, Knabe N, Kües U, Lilly WW, Lindquist E, Lucas S, Magnuson JK, Piumi F, Raudaskoski M, Salamov A, Schmutz J, Schwarze FWMR, Vankuyk PA, Horton JS, Grigoriev IV, Wösten HAB (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28:957–963

    Article  CAS  PubMed  Google Scholar 

  • Olson Å, Aerts A, Asiegbu F, Belbahri L, Bouzid O, Broberg A, Canbäck B, Coutinho PM, Cullen D, Dalman K, Deflorio G, van Diepen LTA, Dunand C, Duplessis S, Durling M, Gonthier P, Grimwood J, Fossdal CG, Hansson D, Henrissat B, Hietala A, Himmelstrand K, Hoffmeister D, Högberg N, James TY, Karlsson M, Kohler A, Kües U, Lee Y-H, Lin Y-C, Lind M, Lindquist E, Lombard V, Lucas S, Lundén K, Morin E, Murat C, Park J, Raffaello T, Rouzé P, Salamov A, Schmutz J, Solheim H, Ståhlberg J, Vélëz H, de Vries RP, Wiebenga A, Woodward S, Yakovlev I, Garbelotto M, Martin F, Grigoriev IV, Stenlid J (2012) Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol 194:1001–1013

    Article  PubMed  Google Scholar 

  • Padamsee M, Kumar TKA, Riley R, Binder M, Boyd A, Calvo AM, Furukawa K, Hesse C, Hohmann S, James TY, LaButti K, Lapidus A, Lindquist E, Lucas S, Miller K, Shantappa S, Grigoriev IV, Hibbett DS, McLaughlin DJ, Spatafora JW, Aime MC (2012) The genome of the xerotolerant mold Wallemia sebi reveals adaptations to osmotic stress and suggests cryptic sexual reproduction. Fungal Genet Biol 49:217–226

    Article  CAS  PubMed  Google Scholar 

  • Perlin MH, Amselem J, Fontanillas E, Toh SS, Chen Z, Goldberg J, Duplessis S, Henrissat B, Young S, Zeng Q, Aguileta G, Petit E, Badouin H, Andrews J, Razeeq D, Gabaldón T, Quesneville H, Giraud T, Hood ME, Schultz DJ, Cuomo C a (2015) Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus. BMC Genomics 16:461. doi:10.1186/s12864-015-1660-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21:I351–I358

    Article  CAS  PubMed  Google Scholar 

  • Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10:417–430. doi:10.1038/nrmicro2790

    CAS  PubMed  Google Scholar 

  • Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW, Levasseur A, Lombard V, Morin E, Otillar R, Lindquist EA, Sun H, LaButti KM, Schmutz J, Jabbour D, Luo H, Baker SE, Pisabarro AG, Walton JD, Blanchette RA, Henrissat B, Martin F, Cullen D, Hibbett DS, Grigoriev IV (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A 111:9923–9928. doi:10.1073/pnas.1400592111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romao J, Hamer JE (1992) Genetic organization of a repeated DNA sequence family in the rice blast fungus. Proc Natl Acad Sci U S A 89:5316–5320. doi:10.1073/pnas.89.12.5316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schirawski J, Mannhaupt G, Munch K, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rossel N, Mendoza-Mendoza A, Pester D, Muller O, Winterberg B, Meyer E, Ghareeb H, Wollenberg T, Munsterkotter M, Wong P, Walter M, Stukenbrock E, Guldener U, Kahmann R (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330(6010):1546–1548

  • Selker EU, Tountas N a, Cross SH, Margolin BS, Murphy JG, Bird AP, Freitag M (2003) The methylated component of the Neurospora crassa genome. Nature 422:893–897. doi:10.1038/nature01564

    Article  CAS  PubMed  Google Scholar 

  • Sonnenberg ASM, Baars JJP, Mikosch TSP, Schaap PJ, Van Griensven LJLD (1999) Abr1, a transposon-like element in the genome of the cultivated mushroom Agaricus bisporus (Lange) imbach. Appl Environ Microbiol 65:3347–3353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sonnenberg ASM, Gao W, Lavrijssen B, Hendrickx P, Sedaghat-Tellgerd N, Foulongne-Oriol M, Kong W-S, Schijlen EGWM, Baars JJP, Visser RGF (2016) A detailed analysis of the recombination landscape of the button mushroom Agaricus bisporus var. bisporus. Fungal Genet Biol 93:35–45. doi:10.1016/j.fgb.2016.06.001

    Article  CAS  PubMed  Google Scholar 

  • Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stuber K, Ver Loren van Themaat E, Brown JKM, Butcher SA, Gurr SJ, Lebrun M-H, Ridout CJ, Schulze-Lefert P, Talbot NJ, Ahmadinejad N, Ametz C, Barton GR, Benjdia M, Bidzinski P, Bindschedler LV, Both M, Brewer MT, Cadle-Davidson L, Cadle-Davidson MM, Collemare J, Cramer R, Frenkel O, Godfrey D, Harriman J, Hoede C, King BC, Klages S, Kleemann J, Knoll D, Koti PS, Kreplak J, Lopez-Ruiz FJ, Lu X, Maekawa T, Mahanil S, Micali C, Milgroom MG, Montana G, Noir S, RJ O’C, Oberhaensli S, Parlange F, Pedersen C, Quesneville H, Reinhardt R, Rott M, Sacristan S, Schmidt SM, Schon M, Skamnioti P, Sommer H, Stephens A, Takahara H, Thordal-Christensen H, Vigouroux M, Wessling R, Wicker T, Panstruga R (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546. doi:10.1126/science.1194573

    Article  CAS  PubMed  Google Scholar 

  • Stajich JE, Wilke SK, Ahrén D, Hang C, Birren BW, Borodovsky M, Burns C, James TY, Kamada T, Kilaru S, Kodira C, Kües U, Kupfer D, Kwan HS (2010) Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus ). PNAS 107:11889–11894. doi:10.1073/pnas.1003391107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki H, MacDonald J, Syed K, Salamov A, Hori C, Aerts A, Henrissat B, Wiebenga A, van Kuyk PA, Barry K, Lindquist E, La Butti K, Lapidus A, Lucas S, Coutinho P, Gong Y, Samejima M, Mahadevan R, Abou-Zaid M, de Vries RP, Igarashi K, Yadav JS, Grigoriev I V, Master ER (2012) Comparative genomics of the white-rot fungi, Phanerochaete carnosa and P. chrysosporium, to elucidate the genetic basis of the distinct wood types they colonize

  • Toome M, Ohm RA, Riley RW, James TY, Lazarus KL, Henrissat B, Albu S, Boyd A, Chow J, Clum A, Heller G, Lipzen A, Nolan M, Sandor L, Zvenigorodsky N, Grigoriev IV, Spatafora JW, Aime MC (2014) Genome sequencing provides insight into the reproductive biology, nutritional mode and ploidy of the fern pathogen Mixia osmundae. New Phytol 202:554–564. doi:10.1111/nph.12653

    Article  CAS  PubMed  Google Scholar 

  • Zajc J, Liu Y, Dai W, Yang Z, Hu J, Gostinčar C, Gunde-Cimerman N (2013) Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent. BMC Genomics 14:617. doi:10.1186/1471-2164-14-617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Hsueh YP, Li W, Floyd A, Skalsky R, Heitman J (2010) Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev 24:2566–2582. doi:10.1101/gad.1970910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Wang P, Sun S, Darwiche S, Idnurm A, Heitman J (2012) Transgene induced co-suppression during vegetative growth in Cryptococcus neoformans. PLoS Genet. doi:10.1371/journal.pgen.1002885

    Google Scholar 

  • Weld RJ, Plummer KM, Carpenter M a, Ridgway HJ (2006) Approaches to functional genomics in filamentous fungi. Cell Res 16:31–44. doi:10.1038/sj.cr.7310006

    Article  CAS  PubMed  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982. doi:10.1038/nrg2165

    Article  CAS  PubMed  Google Scholar 

  • Wong LH, Choo KHA (2004) Evolutionary dynamics of transposable elements at the centromere. Trends Genet 20:611–616

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, Kronstad JW, DeAngelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears R, Yuan B, Dawson TL (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proceedings of the National Academy of Sciences 104(47):18730–18735

  • Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919. doi:10.1126/science.1186366

    Article  CAS  PubMed  Google Scholar 

  • Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel KH (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. doi:10.1371/journal.ppat.1002290

    PubMed  PubMed Central  Google Scholar 

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Correspondence to Lucía Ramírez.

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This work was supported by Spanish National Research Plan (Projects AGL2011 30495 and AGL2014-55971-R) and FEDER funds, Public University of Navarre ( http://www.unavarra.es ). A.B holds a Ph.D. Studentship from the Public University of Navarre. R.C. holds an FPI Ph.D. studentship from the Spanish Ministry of Economy, Industry and Competitiveness.

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Castanera, R., Borgognone, A., Pisabarro, A.G. et al. Biology, dynamics, and applications of transposable elements in basidiomycete fungi. Appl Microbiol Biotechnol 101, 1337–1350 (2017). https://doi.org/10.1007/s00253-017-8097-8

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