Functional & Integrative Genomics

, Volume 9, Issue 1, pp 27–42 | Cite as

Non-LTR retrotransposons in fungi

  • Olga NovikovaEmail author
  • Victor Fet
  • Alexander Blinov


Non-long terminal repeat (non-LTR) retrotransposons have contributed to shaping the structure and function of genomes. Fungi have small genomes, usually with limited amounts of repetitive DNA. In silico approach has been used to survey the non-LTR elements in 57 fungal genomes. More than 100 novel non-LTR retrotransposons were found, which belonged to five diverse clades. The present survey identified two novel clades of fungal non-LTR retrotransposons. The copy number of non-LTR retroelements varied widely. Some of the studied species contained a single copy of non-LTR retrotransposon, whereas others possessed a great number of non-LTR retrotransposon copies per genome. Although evolutionary relationships of most elements are congruent with phylogeny of host species, a new case of possible horizontal transfer was found between Eurotiomycetes and Sordariomycetes.


Fungi Non-LTR retrotransposons Horizontal transmission Ribonuclease H 



The sequence data for P. chrysosporium, L. bicolor, T. reesei, A. niger, and P. stipitis were produced by the US Department of Energy Joint Genome Institute ( Preliminary sequence data for Ascosphaera apis was obtained from Baylor College of Medicine Human Genome Sequencing Center website at Preliminary sequence data for Alternaria brassicicola were obtained from Genome Sequencing Center at Washington University Medical School (

This work was supported in part by state contract 10002-251/П-25/155-270/200404-082 and Siberian Branch of the Russian Academy of Sciences (project No. 10.4).

Supplementary material

10142_2008_93_MOESM1_ESM.doc (88 kb)
Table S1 List of species, genomes of which were analyzed in silico in the present study and the sources of genomic sequences. (Word file). (DOC 88.5 KB)
10142_2008_93_MOESM2_ESM.doc (177 kb)
Table S2 Novel non-LTR retrotransposons from fungi detected in this study and their accession numbers. (Word file). (DOC 177 KB)
10142_2008_93_MOESM3_ESM.doc (215 kb)
Table S3 Novel non-LTR retrotransposons from fungi detected in this study, their copy number, and putative structure. (Word file). (DOC 215 KB)
10142_2008_93_MOESM4_ESM.doc (106 kb)
Table S4 Amino acid divergences of 11 cellular proteins from A. niger, A. fumigatus, A. oryzae, F. oxysporum, and C. globosum. (Word file). (DOC 106 KB)
10142_2008_93_MOESM5_ESM.pdf (20 kb)
Fig. S1 The percentage of non-LTR retrotransposons sequences in investigated fungal genomes plotted against the genome size. (Adobe Reader file). (PDF 20.3 KB)
10142_2008_93_MOESM6_ESM.pdf (53 kb)
Fig. S2 The 50% consensus tree of the Bayesian inference based on RT amino acid sequences of non-LTR retrotransposons including newly described elements from fungi. Posterior probabilities are indicated. (Adobe Reader file). (PDF 52.9 KB)


  1. Aksoy S, Williams S, Chang S, Richards FF (1990) SLACS retrotransposon from Trypanosoma brucei gambiense is similar to mammalian LINEs. Nucleic Acids Res 18:785–792PubMedCrossRefGoogle Scholar
  2. Arkhipova IR (2005) Mobile genetic elements and sexual reproduction. Cytogenet Genome Res 110:372–382PubMedCrossRefGoogle Scholar
  3. Arkhipova IR, Morrison HG (2001) Three retrotransposon families in the genome of Giardia lamblia: two telomeric, one dead. Proc Natl Acad Sci USA 98:14497–14502PubMedCrossRefGoogle Scholar
  4. Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127Google Scholar
  5. Berbee ML, Taylor JW (2001) Fungal molecular evolution: Gene trees and geologic time. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota: a comprehensive treatise on fungi as experimental systems for basic and applied research. Volume VII: Systematics and Evolution, Part B, (2001). Springer-Verlag, New YorkGoogle Scholar
  6. Biedler J, Tu Z (2003) Non-LTR retrotransposons in the African malaria mosquito, Anopheles gambiae: unprecedented diversity and evidence of recent activity. Mol Biol Evol 20:1811–1825PubMedCrossRefGoogle Scholar
  7. Bowman BH, White TJ, Taylor JW (1996) Human pathogeneic fungi and their close nonpathogenic relatives. Mol Phylogenet Evol 6:89–96PubMedCrossRefGoogle Scholar
  8. Brookfield JF, Badge RM (1997) Population genetics models of transposable elements. Genetica 100:281–294PubMedCrossRefGoogle Scholar
  9. Burke WD, Malik HS, Rich SM, Eickbush TH (2002) Ancient lineages of non-LTR retrotransposons in the primitive eukaryote, Giardia lamblia. Mol Biol Evol 19:619–630PubMedGoogle Scholar
  10. Casaregola S, Neuveglise C, Bon E, Gaillardin C (2002) Ylli, a non-LTR retrotransposon L1 family in the dimorphic yeast Yarrowia lipolytica. Mol Biol Evol 19:664–677PubMedGoogle Scholar
  11. Cavalier-Smith T (1991) Archamoebae: the ancestral eukaryotes? Biosystems 25:25–38PubMedCrossRefGoogle Scholar
  12. Cogoni C, Macino G (1999) Homology-dependent gene silencing in plants and fungi: a number of variations on the same theme. Curr Opin Microbiol 2:657–662PubMedCrossRefGoogle Scholar
  13. Drew AC, Brindley PJ (1997) A retrotransposon of the non-long terminal repeat class from the human blood fluke Schistosoma mansoni. Similarities to the chicken-repeat-1-like elements of vertebrates. Mol Biol Evol 14:602–610PubMedGoogle Scholar
  14. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763PubMedCrossRefGoogle Scholar
  15. Eichler EE, Clark RA, She X (2004) An assessment of the sequence gaps: unfinished business in a finished human genome. Nat Rev Genet 5:345–354PubMedCrossRefGoogle Scholar
  16. Eickbush TH, Malik HS (2002) Origins and evolution of retrotransposons. In: Craig N, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. ASM, WashingtonGoogle Scholar
  17. Faugeron G (2000) Diversity of homology-dependent gene silencing strategies in fungi. Curr Opin Microbiol 3:144–148PubMedCrossRefGoogle Scholar
  18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  19. Finnegan DJ (1992) Transposable elements. Curr Opin Genet Dev 2:861–867PubMedCrossRefGoogle Scholar
  20. Fitzpatrick DA, Logue ME, Stajich JE, Butler G (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99PubMedCrossRefGoogle Scholar
  21. Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20:417–423PubMedCrossRefGoogle Scholar
  22. Galagan JE, Henn MR, Ma LJ, Cuomo CA, Birren B (2005) Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res 15:1620–1631PubMedCrossRefGoogle Scholar
  23. Gollotte A, L’Haridon F, Chatagnier O, Wettstein G, Arnould C, van Tuinen D, Gianinazzi-Pearson V (2006) Repetitive DNA sequences include retrotransposons in genomes of the Glomeromycota. Genetica 128:455–469PubMedGoogle Scholar
  24. Goodwin TJ, Poulter RT (2001) The diversity of retrotransposons in the yeast Cryptococcus neoformans. Yeast 18:865–880PubMedCrossRefGoogle Scholar
  25. Goodwin TJ, Ormandy JE, Poulter RT (2001) L1-like non-LTR retrotransposons in the yeast Candida albicans. Curr Genet 39:83–91PubMedCrossRefGoogle Scholar
  26. Goyon C, Rossignol JL, Faugeron G (1996) Native DNA repeats and methylation in Ascobolus. Nucleic Acids Res 24:3348–3356PubMedCrossRefGoogle Scholar
  27. Hamer JE, Farall L, Orbach MJ, Valent B, Chumley FG (1989) Host species-specific conservation of a family of repeated DNA sequences in the genome of a fungal plant pathogen. Proc Natl Acad Sci USA 86:9981–9985PubMedCrossRefGoogle Scholar
  28. Hartl DL, Lohe AR, Lozovskaya ER (1997) Modern thoughts on an ancyent marinere: function, evolution, regulation. Annu Rev Genet 31:337–358PubMedCrossRefGoogle Scholar
  29. He C, Nourse JP, Kelemu S, Irwin JAG, Manners JM (1996) CgT1: a non-LTR retrotransposon with restricted distribution in the fungal phytopathogen Colletotrichum gloeosporioides. Mol Gen Genet 252:320–331PubMedGoogle Scholar
  30. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133PubMedCrossRefGoogle Scholar
  31. Hedges SB (2002) The origin and evolution of model organisms. Nat Rev Genet 3:838–849PubMedCrossRefGoogle Scholar
  32. Hibbett DS, Grimaldi D, Donoghue MJ (1997) Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of Homobasidiomycetes. Am J Bot 84:981–991CrossRefGoogle Scholar
  33. Hickey DA (1982) Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101:519–531PubMedGoogle Scholar
  34. Hood ME (2005) Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124:1–10PubMedCrossRefGoogle Scholar
  35. Hua-Van A, Le Rouzic A, Maisonhaute C, Capy P (2005) Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenet Genome Res 110:426–440PubMedCrossRefGoogle Scholar
  36. Johnson LJ (2007) The genome strikes back: the evolutionary importance of defense against mobile elements. Evol Biol 34:121–129CrossRefGoogle Scholar
  37. Jordan IK, McDonald JF (1999) Comparative genomics and evolutionary dynamics of Saccharomyces cerevisiae Ty elements. Genetica 107:3–13PubMedCrossRefGoogle Scholar
  38. Jordan IK, Matyunina LV, McDonald JF (1999) Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc Natl Acad Sci USA 96:12621–12625PubMedCrossRefGoogle Scholar
  39. Kanaya S, Oobatake M, Liu Y (1996) Thermal stability of Escherichia coli ribonuclease HI and its active site mutants in the presence and absence of the Mg2+ ion. Proposal of a novel catalytic role for Glu48. J Biol Chem 271:32729–32736PubMedCrossRefGoogle Scholar
  40. Kasuga T, White TJ, Taylor JW (2002) Estimation of nucleotide substitution rates in Eurotiomycete fungi. Mol Biol Evol 19:2318–2324PubMedGoogle Scholar
  41. Kempken F, Kück U (1998) Transposons in filamentous fungi—facts and perspectives. Bioessays 20:652–659PubMedCrossRefGoogle Scholar
  42. Khaldi N, Collemare J, Lebrun MH, Wolfe KH (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9:R18PubMedCrossRefGoogle Scholar
  43. Kidwell MG (1992) Horizontal transfer. Curr Opin Genet Dev 2:868–873PubMedCrossRefGoogle Scholar
  44. Kinsey JA, Helber J (1989) Isolation of a transposable element from Neurospora crassa. Proc Natl Acad Sci USA 86:1929–1933PubMedCrossRefGoogle Scholar
  45. Kojima KK, Fujiwara H (2005) An extraordinary retrotransposon family encoding dual endonucleases. Genome Res 15:1106–1117PubMedCrossRefGoogle Scholar
  46. Kordiš D, Gubenšek F (1998) Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. Proc Natl Acad Sci USA 95:10704–10709PubMedCrossRefGoogle Scholar
  47. Le Rouzic A, Capy P (2005) The first steps of transposable elements invasion: parasitic strategy vs. genetic drift. Genetics 169:1033–1043PubMedCrossRefGoogle Scholar
  48. Lovšin N, Gubenšek F, Kordiš D (2001) Evolutionary dynamics in a novel L2 clade of non-LTR retrotransposons in Deuterostomia. Mol Biol Evol 18:2213–2224PubMedGoogle Scholar
  49. Malik HS (2005) Ribonuclease H evolution in retrotransposable elements. Cytogenet Genome Res 110:392–401PubMedCrossRefGoogle Scholar
  50. Malik HS, Eickbush TH (2000) NeSL-1, an ancient lineage of site-specific non-LTR retrotransposons from Caenorhabditis elegans. Genetics 154:193–203PubMedGoogle Scholar
  51. Malik HS, Eickbush TH (2001) Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res 11:1187–1197PubMedCrossRefGoogle Scholar
  52. Malik HS, Burke WD, Eickbush TH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16:793–805PubMedGoogle Scholar
  53. Martin SL, Bushman FD (2001) Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol Cell Biol 21:467–475PubMedCrossRefGoogle Scholar
  54. McClure MA, Smith C, Elton P (1996) Parameterization studies for the SAM and HMMER methods of hidden Markov model generation. Proc Int Conf Intell Syst Mol Biol 4:155–164PubMedGoogle Scholar
  55. Medstrand P, Landry JR, Mager DL (2001) Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J Biol Chem 276:1896–1903PubMedCrossRefGoogle Scholar
  56. Mizrokhi LJ, Mazo AM (1990) Evidence for horizontal transmission of the mobile element jockey between distant Drosophila species. Proc Natl Acad Sci USA 87:9216–9220PubMedCrossRefGoogle Scholar
  57. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. New York, Oxford University PressGoogle Scholar
  58. Novikova O, Sliwińska E, Fet V, Settele J, Blinov A, Woyciechowski M (2007) CR1 clade of non-LTR retrotransposons from Maculinea butterflies (Lepidoptera: Lycaenidae): evidence for recent horizontal transmission. BMC Evol Biol 7:93PubMedCrossRefGoogle Scholar
  59. Ono R, Kobayashi S, Wagatsuma H, Aisaka K, Kohda T, Kaneko-Ishino T, Ishino F (2001) A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73:232–237PubMedCrossRefGoogle Scholar
  60. Peyretaillade E, Biderre C, Peyret P, Duffieux F, Méténier G, Gouy M, Michot B, Vivarès CP (1998) Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res 26:3513–3520PubMedCrossRefGoogle Scholar
  61. Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241–245PubMedCrossRefGoogle Scholar
  62. Roulin A, Piegu B, Wing RA, Panaud O (2008) Evidence of multiple horizontal transfers of the long terminal repeat retrotransposon RIRE1 within the genus Oryza. Plant J 53:950–959PubMedCrossRefGoogle Scholar
  63. Sánchez-Gracia A, Maside X, Charlesworth B (2005) High rate of horizontal transfer of transposable elements in Drosophila. Trends Genet 21:200–203PubMedCrossRefGoogle Scholar
  64. Silva JC, Kidwell MG (2004) Evolution of P elements in natural populations of Drosophila willistoni and D. sturtevanti. Genetics 168:1323–1335PubMedCrossRefGoogle Scholar
  65. Slot JC, Hibbett DS (2007) Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS ONE 2:e1097PubMedCrossRefGoogle Scholar
  66. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  67. Taylor TN, Hass H, Kerp H (1999) The oldest fossil ascomycetes. Nature 399:648PubMedCrossRefGoogle Scholar
  68. Teng SC, Wang SX, Gabriel A (1995) A new non-LTR retrotransposon provides evidence for multiple distinct site-specific elements in Crithidia fasciculata miniexon arrays. Nucleic Acids Res 23:2929–2936PubMedCrossRefGoogle Scholar
  69. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  70. Vivarès CP, Méténier G (2000) Towards the minimal eukaryotic parasitic genome. Curr Opin Microbiol 3:463–467PubMedCrossRefGoogle Scholar
  71. Volff JN, Körting C, Schartl M (2000) Multiple lineages of the non-LTR retrotransposon Rex1 with varying success in invading fish genomes. Mol Biol Evol 17:1673–1684PubMedGoogle Scholar
  72. Wenzl P, Wong L, Kwang-won K, Jefferson RA (2005) A functional screen identifies lateral transfer of beta-glucuronidase (gus) from bacteria to fungi. Mol Biol Evol 22:308–316PubMedCrossRefGoogle Scholar
  73. 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 8:973–982PubMedCrossRefGoogle Scholar
  74. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S et al (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880PubMedCrossRefGoogle Scholar
  75. Wöstemeyer J, Kreibich A (2002) Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 41:189–198PubMedCrossRefGoogle Scholar
  76. Zingler N, Weichenrieder O, Schumann GG (2005) APE-type non-LTR retrotransposons: determinants involved in target site recognition. Cytogenet Genome Res 110:250–268PubMedCrossRefGoogle Scholar
  77. Župunski V, Gubenšek F, Kordiš D (2001) Evolutionary dynamics and evolutionary history in the RTE clade of non-LTR retrotransposons. Mol Biol Evol 18:1849–1863PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Institute of Cytology and GeneticsNovosibirskRussia
  2. 2.Marshall UniversityHuntingtonUSA

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