Whole genome comparative analysis of transposable elements provides new insight into mechanisms of their inactivation in fungal genomes

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Amselem, Joëlle ^a,b   Lebrun, Marc Henri ^b   Quesneville, Hadi ^a  

^a Centre de recherche de Versailles   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

C5 methyltransferase; Fungi; Repeat induced point mutation; Transposable elements

Indexed keywords

CYTOSINE; DNA METHYLTRANSFERASE 1; THYMINE; TRANSPOSON;

ARTICLE; ASCOMYCETES; BASIDIOMYCETES; BLUMERIA; BLUMERIA GRAMINIS F. SP. HORDEI; BOTRYTIS CINEREA; CONTROLLED STUDY; DINUCLEOTIDE REPEAT; FUNGAL GENOME; GENE INACTIVATION; GENE MUTATION; GENE SEQUENCE; GENOME ANALYSIS; LEPTOSPHAERIA MACULANS; MAGNAPORTHE ORYZAE; MELAMPSORA; MICROBOTRYUM VIOLACEUM; MUTATION RATE; NONHUMAN; PHYLOGENOMICS; PUCCINIA; SCLEROTINIA SCLEROTIORUM; TRANSPOSON; TUBER MELANOSPORUM; GENETICS; MOLECULAR GENETICS; MUTATION; SPECIES DIFFERENCE;

ASCOMYCOTA; BASIDIOMYCOTA; BLUMERIA; FUNGI; MELAMPSORA; PUCCINIA;

ASCOMYCOTA; BASIDIOMYCOTA; DNA TRANSPOSABLE ELEMENTS; GENOME, FUNGAL; MOLECULAR SEQUENCE ANNOTATION; MUTATION; SPECIES SPECIFICITY;

EID: 84928747135     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1347-1     Document Type: Article

References (59)

1. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8:973-82.
2. Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L. Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet. 2005;21:673-82.
3. Biemont C. A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics. 2010;186:1085-93.
4. Manning VA, Pandelova I, Dhillon B, Wilhelm LJ, Goodwin SB, Berlin AM, et al. Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. G3 (Bethesda). 2013;3:41-63.
5. Fudal I, Ross S, Brun H, Besnard AL, Ermel M, Kuhn ML, et al. Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant Microbe Interact. 2009;22:932-41.
6. Kim MY, Zilberman D. DNA methylation as a system of plant genomic immunity. Trends Plant Sci. 2014;19:320-6.
7. Jeffrey T, Selker EU. Gene silencing in filamentous fungi: RIP, MIP and quelling. J Genet. 1996;75:313-24.
8. Selker EU, Cambareri EB, Jensen BC, Haack KR. Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell. 1987;51:741-52.
9. Cambareri EB, Jensen BC, Schabtach E, Selker EU. Repeat-induced G-C to A-T mutations in Neurospora. Science. 1989;244:1571-5.
10. Galagan JE, Selker EU. RIP: the evolutionary cost of genome defense. Trends Genet. 2004;20:417-23.
11. Neuveglise C, Sarfati J, Latge JP, Paris S. Afut1, a retrotransposon-like element from Aspergillus fumigatus. Nucleic Acids Res. 1996;24:1428-34.
12. Braumann I, van den Berg M, Kempken F. Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr Genet. 2008;53:287-97.
13. Clutterbuck AJ. Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol. 2011;48:306-26.
14. Jurkowski TP, Jeltsch A. On the evolutionary origin of eukaryotic DNA methyltransferases and Dnmt2. PLoS One. 2011;6:e28104.
15. Ponger L, Li WH. Evolutionary diversification of DNA Methyltransferases in eukaryotic Genomes. Mol Biol Evol. 2005;22:1119-28.
16. Freitag M, Williams RL, Kothe GO, Selker EU. A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci U S A. 2002;99:8802-7.
17. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature. 2005;438:1105-15.
18. Cuomo CA, Gueldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science. 2007;317:1400-2.
19. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun. 2011;2:202.
20. Goyon C, Faugeron G. Targeted transformation of Ascobolus immersus and de novo methylation of the resulting duplicated DNA sequences. Mol Cell Biol. 1989;9:2818-27.
21. Malagnac F, Wendel B, Goyon C, Faugeron G, Zickler D, Rossignol JL, et al. A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell. 1997;91:281-90.
22. Malagnac F, Gregoire A, Goyon C, Rossignol JL, Faugeron G. Masc2, a gene from Ascobolus encoding a protein with a DNA-methyltransferase activity in vitro, is dispensable for in vivo methylation. Mol Microbiol. 1999;31:331-8.
23. Romano N, Macino G. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol. 1992;6:3343-53.
24. Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci U S A. 2000;97:11650-4.
25. Fulci V, Macino G. Quelling: post-transcriptional gene silencing guided by small RNAs in Neurospora crassa. Curr Opin Microbiol. 2007;10:199-203.
26. Shiu PK, Raju NB, Zickler D, Metzenberg RL. Meiotic silencing by unpaired DNA. Cell. 2001;107:905-16.
27. Kouzminova E. Selker EU: dim-2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora. Embo J. 2001;20:4309-23.
28. Chernov AV, Vollmayr P, Walter J, Trautner TA. Masc2, a C5-DNA-methyltransferase from Ascobolus immersus with similarity to methyltransferases of higher organisms. Biol Chem. 1997;378:1467-73.
29. Johnson LJ, Giraud T, Anderson R, Hood ME. The impact of genome defense on mobile elements in Microbotryum. Genetica. 2010;138:313-9.
30. Cooper DN, Youssoufian H. The CpG dinucleotide and human genetic disease. Hum Genet. 1988;78:151-5.
31. Horns F, Petit E, Yockteng R, Hood ME. Patterns of repeat-induced point mutation in transposable elements of basidiomycete fungi. Genome Biol Evol. 2012;4:240-7.
32. Flutre T, Duprat E, Feuillet C, Quesneville H. Considering transposable element diversification in de novo annotation approaches. PLoS One. 2011;6:e16526.
33. Hoede C, Arnoux S, Moisset M, Chaumier T, Inizan O, Jamilloux V, et al. PASTEC: an automatic transposable element classification tool. PLoS One. 2014;9:e91929.
34. Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, Ashburner M, et al. Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol. 2005;1:166-75.
35. Hane JK, Oliver RP. RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics. 2008;9:478.
36. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, Couloux A, et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 2011;7:e1002230.
37. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stuber K, et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science. 2010;330:1543-6.
38. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature. 2005;434:980-6.
39. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, et al. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature. 2010;464:1033-8.
40. Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A. 2011;108:9166-71.
41. Raffaele S, Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol. 2012;10:417-30.
42. Wicker T, Oberhaensli S, Parlange F, Buchmann JP, Shatalina M, Roffler S, et al. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat Genet. 2013;45(9):1092-6. advance online publication.
43. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 2011;39:6919-31.
44. Maumus F, Quesneville H. Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLoS One. 2014;9:e94101.
45. Buisine N, Quesneville H, Colot V. Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets. Genomics. 2008;91:467-75.
46. Callebaut I, Courvalin JC, Mornon JP. The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation. FEBS Lett. 1999;446:189-93.
47. Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet. 2000;25:269-77.
48. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet. 2012;44:1060-5.
49. Montanini B, Chen PY, Morselli M, Jaroszewicz A, Lopez D, Martin F, et al. Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content. Genome Biol. 2014;15:411.
50. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462-7.
51. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
52. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, et al. InterProScan: protein domains identifier. Nucleic Acids Res. 2005;33:W116-20.
53. Notredame C, Higgins DG, Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol. 2000;302:205-17.
54. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol. 2006;55:539-52.
55. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36:W465-9.
56. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540-52.
57. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696-704.
58. Chevenet F, Brun C, Banuls AL, Jacq B, Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics. 2006;7:439.
59. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36.