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Epigenomics pp 321-341 | Cite as

Genome Defense: The Neurospora Paradigm

  • M.R. Rountree
  • E.U. Selker

Abstract

Eukaryotes deploy an array of defensive mechanisms to limit the destructive effects of “selfish” DNA. These protective mechanisms include both transcriptional gene silencing (TGS) and RNA-based post-transcriptional gene silencing (PTGS) mechanisms. The filamentous fungus Neurospora crassa defends its genome with incredible tenacity utilizing two TGS mechanisms, repeat-induced point mutation (RIP) and DNA methylation and two PTGS mechanisms, quelling and meiotic silencing of unpaired DNA (MSUD).

Keywords

DNA methylation Genome defense MSUD Quelling RIP 

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References

  1. Alexander WG, Raju NB, Xiao H, Hammond TM, Perdue TD, Metzenberg RL, Pukkila PJ, Shiu PK: DCL-1 colocalizes with other components of the MSUD machinery and is required for silencing. Fungal Genet Biol2008 45(5):719–727 (Epub 2007).Google Scholar
  2. Aramayo R, Metzenberg RL: Meiotic transvection in fungi. Cell1996, 86(1):103–113.PubMedGoogle Scholar
  3. Aravin A, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T: The small RNA profile during Drosophila melanogaster development. Dev Cell2003, 5(2):337–350.PubMedGoogle Scholar
  4. Bachman KE, Rountree MR, Baylin SB: Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem2001, 276(34):32282–32287.PubMedGoogle Scholar
  5. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T: Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature2001, 410(6824):120–124.PubMedGoogle Scholar
  6. Bardiya N, Alexander WG, Perdue TD, Barry EG, Metzenberg RL, Pukkila PJ, Shiu PK: Characterization of interactions between and among components of the meiotic silencing by unpaired DNA machinery in Neurospora crassa using bimolecular fluorescence complementation. Genetics2008, 178(1):593–596.PubMedGoogle Scholar
  7. Bhat A, Kasbekar DP: Escape from repeat-induced point mutation of a gene-sized duplication in neurospora crassa crosses that are heterozygous for a larger chromosome segment duplication. Genetics2001, 157(4):1581–1590.PubMedGoogle Scholar
  8. Bouhouche K ZD, Debuchy R, Arnaise S.: Altering a gene involved in nuclear distribution increases the repeat-induced point mutation process in the fungus Podospora anserina. Genetics2004, 167(1):151–159.PubMedGoogle Scholar
  9. Butler DK, Metzenberg RL: Premeiotic change of nucleolus organizer size in Neurospora. Genetics1989, 122:783–791.PubMedGoogle Scholar
  10. Butler DK, Metzenberg RL: Expansion and contraction of the nucleolus organizer region of Neurospora: changes originate in both proximal and distal segments. Genetics1990, 126(2):325–333.PubMedGoogle Scholar
  11. Butler DK, Metzenberg RL: Amplification of the nucleolus organizer region during the sexual phase of Neurospora crassa. Chromosoma1993, 102(8):519–525.PubMedGoogle Scholar
  12. Cambareri EB, Aisner R, Carbon J: Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats. Mol Cell Biol1998, 18(9):5465–5477.PubMedGoogle Scholar
  13. Cambareri EB, Jensen BC, Schabtach E, Selker EU: Repeat-induced G-C to A-T mutations in Neurospora. Science1989,244(4912):1571–1575.PubMedGoogle Scholar
  14. Cambareri EB, Singer MJ, Selker EU: Recurrence of repeat-induced point mutation (RIP) in Neurospora crassa. Genetics1991, 127(4):699–710.PubMedGoogle Scholar
  15. Catalanotto C, Azzalin G, Macino G, Cogoni C: Involvement of small RNAs and role of the qde genes in the gene silencing pathway in Neurospora. Genes Dev2002, 16(7):790–795.PubMedGoogle Scholar
  16. Catalanotto C, Pallotta M, ReFalo P, Sachs MS, Vayssie L, Macino G, Cogoni C: Redundancy of the two dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa. Mol Cell Biol2004, 24(6):2536–2545.PubMedGoogle Scholar
  17. Chalvet F GC, Kaper F, Langin T, Daboussi MJ.: Hop, an active Mutator-like element in the genome of the fungus Fusarium oxysporum. Mol Biol Evol2003, 20(8):1362–1375.PubMedGoogle Scholar
  18. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE: RNA silencing genes control de novo DNA methylation. Science2004, 303(5662):1336.PubMedGoogle Scholar
  19. Chicas A, Cogoni C, Macino G: RNAi-dependent and RNAi-independent mechanisms contribute to the silencing of RIPed sequences in Neurospora crassa. Nucleic Acids Res2004, 32(14):4237–4243.PubMedGoogle Scholar
  20. Chicas A, Forrest EC, Sepich S, Cogoni C, Macino G: Small interfering RNAs that trigger posttranscriptional gene silencing are not required for the histone H3 Lys9 methylation necessary for transgenic tandem repeat stabilization in Neurospora crassa. Mol Cell Biol2005, 25(9):3793–3801.PubMedGoogle Scholar
  21. Chiu YL, Ali A, Chu CY, Cao H, Rana TM: Visualizing a correlation between siRNA localization, cellular uptake, and RNAi in living cells. Chem Biol2004, 11(8):1165–1175.PubMedGoogle Scholar
  22. Cogoni C, Irelan JT, Schumacher M, Schmidhauser TJ, Selker EU, Macino G: Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J1996, 15(12):3153–3163.PubMedGoogle Scholar
  23. Cogoni C, Macino G: Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature1999a, 399(6732):166–169.Google Scholar
  24. Cogoni C, Macino G: Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science1999b, 286(5448):2342–2344.Google Scholar
  25. Davière JM LT, Daboussi MJ.: Potential role of transposable elements in the rapid reorganization of the Fusarium oxysporum genome. Fungal Genet Biol2001, 34(3):177–192.PubMedGoogle Scholar
  26. Davis RH: Neurospora: Contributions of a Model Organism: Oxford University Press, Oxford; 2000.Google Scholar
  27. Eissenberg JC, Elgin SC: The HP1 protein family: getting a grip on chromatin. Current Opin Genet Dev2000, 10(2):204–210.Google Scholar
  28. Fincham JRS, Connerton IF, Notarianni E, Harrington K: Premeiotic disruption of duplicated and triplicated copies of the Neurospora crassa am (glutamate dehydrogenase) gene. Curr Genet1989, 15(5):327–334.PubMedGoogle Scholar
  29. Foss HM, Roberts CJ, Claeys KM, Selker EU: Abnormal chromosome behavior in Neurospora mutants defective in DNA methylation. Science1993, 262:1737–1741.PubMedGoogle Scholar
  30. Freedman T, Pukkila PJ: De novo methylation of repeated sequences in Coprinus cinereus. Genetics1993, 135:357–366.PubMedGoogle Scholar
  31. Freitag M, Hickey PC, Khlafallah TK, Read ND, Selker EU: HP1 is essential for DNA methylation in Neurospora. Mol Cell2004a, 13(3):427–434.Google Scholar
  32. Freitag M, Lee DW, Kothe GO, Pratt RJ, Aramayo R, Selker EU: DNA methylation is independent of RNA interference in Neurospora. Science2004b, 304(5679):1939.Google Scholar
  33. 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 A2002, 99(13):8802–8807.PubMedGoogle Scholar
  34. Fujita N, Watanabe S, Ichimura T, Tsuruzoe S, Shinkai Y, Tachibana M, Chiba T, Nakao M: Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J Biol Chem2003, 278(26):24132–24138.PubMedGoogle Scholar
  35. Fuks F, Hurd PJ, Deplus R, Kouzarides T: The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res2003, 31(9):2305–2312.PubMedGoogle Scholar
  36. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell Set al: The genome sequence of the filamentous fungus Neurospora crassa. Nature2003, 422(6934):859–868.PubMedGoogle Scholar
  37. Galagan JE, Selker EU: RIP: the evolutionary cost of genome defense. Trends Genet2004, 20(9):417–423.PubMedGoogle Scholar
  38. Goll MG BT: Eukaryotic cytosine methyltransferases. Annu Rev Biochem2005, 74:481–514.PubMedGoogle Scholar
  39. Graia F, Lespinet O, Rimbault B, Dequard-Chablat M, Coppin E, Picard M: Genome Quality Control: RIP (repeat-induced point mutation) comes to Podospora. Mol Microbiol2001, 39:1–11.Google Scholar
  40. Grayburn WS, Selker EU: A natural case of RIP: Degeneration of DNA sequence in an ancestral tandem duplication. Mol Cell Biol1989, 9(10):4416–4421.PubMedGoogle Scholar
  41. Grünweller A, Gillen C, Erdmann VA, Kurreck J: Cellular uptake and localization of a Cy3-labeled siRNA specific for the serine/threonine kinase Pim-1. Oligonucleotides2003, 13(5):345–352.PubMedGoogle Scholar
  42. Hall IM, Shankaranarayana GD, Noma KI, Ayoub N, Cohen A, Grewal SI: Establishment and Maintenance of a Heterochromatin Domain. Science2002, 297:2232–2237.PubMedGoogle Scholar
  43. Ikeda K, Nakayashiki H, Kataoka T, Tamba H, Hashimoto Y, Tosa Y, Mayama S: Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context. Mol Microbiol2002, 45(5):1355–1364.PubMedGoogle Scholar
  44. Jackson JP, Lindroth AM, Cao X, Jacobsen SE: Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature2002, 416(6880):556–560.PubMedGoogle Scholar
  45. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, Eissenberg JC, Allis CD, Khorasanizadeh S: Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J2001, 20(18):5232–5241.Google Scholar
  46. Kachroo P, Leong SA, Chattoo BB: Pot2, an inverted repeat transposon from the rice blast fungus Magnaporthe grisea. Mol Gen Genet1994, 245(3):339–348.PubMedGoogle Scholar
  47. Kelly WG, Aramayo R: Meiotic silencing and the epigenetics of sex. Chromosome Res2007, 15(5):633–651.PubMedGoogle Scholar
  48. Ketting RF, Haverkamp TH, van Luenen HG, Plasterk RH: Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell1999, 99(2):133–141.PubMedGoogle Scholar
  49. Kinsey JA: Restricted distribution of the Tad transposon in strains of Neurospora. Curr Genet1989, 15:271–275.PubMedGoogle Scholar
  50. Kinsey JA, Garrett-Engele PW, Cambareri EB, Selker EU: The Neurospora transposon Tad is sensitive to repeat-induced point Mutation (RIP). Genetics1994, 138:657–664.PubMedGoogle Scholar
  51. Kito H TY, Sato J, Fukiya S, Sone T, Tomita F.: Occan, a novel transposon in the Fot1 family, is ubiquitously found in several Magnaporthe grisea isolates. Curr Genet2003, 42(6):322–331.PubMedGoogle Scholar
  52. Kouzminova EA, Selker EU: Dim-2encodes a DNA-methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO J2001, 20(15):4309–4323.PubMedGoogle Scholar
  53. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T: Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature2001, 410(6824):116–120.PubMedGoogle Scholar
  54. Lee DW, Pratt RJ, McLaughlin M, Aramayo R: An argonaute-like protein is required for meiotic silencing. Genetics2003, 164(2):821–828.PubMedGoogle Scholar
  55. Lee DW, Seong KY, Pratt RJ, Baker K, Aramayo R: Properties of unpaired DNA required for efficient silencing in Neurospora crassa. Genetics2004, 167(1):131–150.PubMedGoogle Scholar
  56. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH: Suv39h-mediated histone h3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol2003, 13(14):1192–1200.PubMedGoogle Scholar
  57. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ: Argonaute2 is the catalytic engine of mammalian RNAi. Science2004, 305(5689):1437–1441.PubMedGoogle Scholar
  58. Llave C, Kasschau KD, Rector MA, Carrington JC: Endogenous and Silencing-Associated Small RNAs in Plants. Plant Cell2002, 14(7):1605–1619.PubMedGoogle Scholar
  59. Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. Science2000, 290(5494):1151–1155.PubMedGoogle Scholar
  60. Maiti M, Lee HC, Liu Y: QIP, a putative exonuclease, interacts with the Neurospora Argonaute protein and facilitates conversion of duplex siRNA into single strands. Genes Dev2007, 21(5):590–600.PubMedGoogle Scholar
  61. Malagnac F, Bartee L, Bender J: An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J2002, 21(24):6842–6852.PubMedGoogle Scholar
  62. Malagnac F, Wendel B, Goyon C, Faugeron G, Zickler D, Rossignol JL, Noyer-Weidner M, Vollmayr P, Trautner TA, Walter J: A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell1997, 91(2):281–290.PubMedGoogle Scholar
  63. Margolin BS, Garrett-Engele PW, Stevens JN, Yen-Fritz D, Garrett-Engele C, Metzenberg RL, Selker EU: A methylated Neurospora 5S rRNA pseudogene contains a transposable element inactivated by RIP. Genetics1998, 149:1787–1797.PubMedGoogle Scholar
  64. Mautino MR, Rosa AL: Analysis of models involving enzymatic activities for the occurrence of C–$>$T transition mutations during repeat-induced point mutation (RIP) in Neurospora crassa. J Theor Biol1998, 192(1):61–71.PubMedGoogle Scholar
  65. Miao VP, Freitag M, Selker EU: Short TpA-rich segments of the zeta-eta region induce DNA methylation in Neurospora crassa. J Mol Biol2000, 300(2):249–273.PubMedGoogle Scholar
  66. Nakayashiki H: RNA silencing in fungi: mechanisms and applications. FEBS Lett2005, 579(26):5950–5970.PubMedGoogle Scholar
  67. Nakayashiki H, Nishimoto N, Ikeda K, Tosa Y, Mayama S: Degenerate MAGGY elements in a subgroup of Pyricularia grisea: a possible example of successful capture of a genetic invader by a fungal genome. Mol Gen Genet1999, 261(6):958–966.PubMedGoogle Scholar
  68. Nolan T, Braccini L, Azzalin G, De Toni A, Macino G, Cogoni C: The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res2005, 33(5):1564–1573.PubMedGoogle Scholar
  69. Nolan T, Cecere G, Mancone C, Alonzi T, Tripodi M, Catalanotto C, Cogoni C: The RNA-dependent RNA polymerase essential for post-transcriptional gene silencing in Neurospora crassa interacts with replication protein A. Nucleic Acids Res2008, 36(2):532–538.PubMedGoogle Scholar
  70. Pal-Bhadra M, Leibovitch BA, Gandhi SG, Rao M, Bhadra U, Birchler JA, Elgin SC: Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science2004, 303(5658):669–672.PubMedGoogle Scholar
  71. Perkins DD, Margolin BS, Selker EU, Haedo SD: Occurrence of repeat induced point mutation in long segmental duplications of Neurospora. Genetics1997, 147(1):125–136.PubMedGoogle Scholar
  72. Perkins DD, Metzenberg RL, Raju NB, Selker EU, Barry EG: Reversal of a Neurospora translocation by crossing over involving displaced rDNA, and methylation of the rDNA segments that result from recombination. Genetics1986, 114:791–817.PubMedGoogle Scholar
  73. Pratt RJ, Lee DW, Aramayo R: DNA methylation affects meiotic trans-sensing, not meiotic silencing, in Neurospora. Genetics2004, 168(4):1925–1935.PubMedGoogle Scholar
  74. Raju NB, Metzenberg RL, Shiu PK: Neurospora spore killers Sk-2 and Sk-3 suppress meiotic silencing by unpaired DNA. Genetics2007, 176(1):43–52.PubMedGoogle Scholar
  75. Reese BE BK, Baylin SB, Rountree MR.: The methyl-CpG binding protein MBD1 interacts with the p150 subunit of chromatin assembly factor 1. Mol Cell Biol2003, 23(9):3226–3236.PubMedGoogle Scholar
  76. Reeves R: Molecular biology of HMGA proteins: hubs of nuclear function. Gene2001, 277(1–2):63–81.PubMedGoogle Scholar
  77. Romano N, Macino G: Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol1992, 6(22):3343–3353.PubMedGoogle Scholar
  78. Rosa AL FH, Mautino MR.: In vivo levels of S-adenosylmethionine modulate C:G to T:A mutations associated with repeat-induced point mutation in Neurospora crassa. Mutat Res2004, 548(1–2):85–95.PubMedGoogle Scholar
  79. Rossignol J-L, Faugeron G: Gene inactivation triggered by recognition between DNA repeats. Experientia1994, 50:307–317.PubMedGoogle Scholar
  80. Rountree MR, Selker EU: DNA methylation inhibits elongation but not initiation of transcription in Neurospora crassa. Genes Dev1997, 11:2383–2395.PubMedGoogle Scholar
  81. Selker EU: Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet1990, 24:579–613.PubMedGoogle Scholar
  82. Selker EU: Repeat-induced point mutation (RIP) and DNA methylation. In: More gene manipulations in fungi. Edited by Bennet JW, Lasure L. New York: Academic Press, Inc.; 1991:258–265.Google Scholar
  83. Selker EU: Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc Natl Acad Sci U S A1998, 95(16):9430–9435.PubMedGoogle Scholar
  84. Selker EU: Gene silencing: repeats that count. Cell1999, 97(2):157–160.PubMedGoogle Scholar
  85. Selker EU, Freitag M, Kothe GO, Margolin BS, Rountree MR, Allis CD, Tamaru H: Induction and maintenance of nonsymmetrical DNA methylation in Neurospora. Proc Natl Acad Sci U S A2002, 99 Suppl 4:16485–16490.PubMedGoogle Scholar
  86. Selker EU, Fritz DY, Singer MJ: Dense non-symmetrical DNA methylation resulting from repeat-induced point mutation (RIP) in Neurospora. Science1993, 262:1724–1728.PubMedGoogle Scholar
  87. Selker EU, Garrett PW: DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci USA1988, 85(18):6870–6874.PubMedGoogle Scholar
  88. Selker EU, Jensen BC, Richardson GA: A portable signal causing faithful DNA methylation de novo inNeurospora crassa. Science1987, 238:48–53.PubMedGoogle Scholar
  89. Selker EU, Stevens JN: DNA methylation at asymmetric sites is associated with numerous transition mutations. Proc Natl Acad Sci USA1985, 82:8114–8118.PubMedGoogle Scholar
  90. Selker EU, Tountas NA, Cross SH, Margolin BS, Murphy JG, Bird AP, Freitag M: The methylated component of the Neurospora crassa genome. Nature2003, 422(6934):893–897.PubMedGoogle Scholar
  91. Shiu PK, Metzenberg RL: Meiotic silencing by unpaired DNA: properties, regulation and suppression. Genetics2002, 161(4):1483–1495.PubMedGoogle Scholar
  92. Shiu PK, Raju NB, Zickler D, Metzenberg RL: Meiotic silencing by unpaired DNA. Cell2001, 107(7):905–916.PubMedGoogle Scholar
  93. Shiu PK, Zickler D, Raju NB, Ruprich-Robert G, Metzenberg RL: SAD-2 is required for meiotic silencing by unpaired DNA and perinuclear localization of SAD-1 RNA-directed RNA polymerase. Proc Natl Acad Sci U S A2006, 103(7):2243–2248.PubMedGoogle Scholar
  94. Singer MJ, Marcotte BA, Selker EU: DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol Cell Biol1995, 15(10):5586–5597.PubMedGoogle Scholar
  95. Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A, Timmons L, Fire A, Mello CC: The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell1999, 99(2):123–132.PubMedGoogle Scholar
  96. Tamaru H, Selker EU: A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature2001, 414(6861):277–283.PubMedGoogle Scholar
  97. Tamaru H, Selker EU: Synthesis of Signals for De Novo DNA Methylation in Neurospora crassa. Mol Cell Biol2003, 23(7):2379–2394.PubMedGoogle Scholar
  98. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU: Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet2003, 34(1):75–79.PubMedGoogle Scholar
  99. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA: Regulation of Heterochromatic Silencing and Histone H3 Lysine-9 Methylation by RNAi. Science2002, 297(5588):1833–1837.PubMedGoogle Scholar
  100. Walsh J: How often do duplicated genes evolve new functions? Genetics1995, 139(1):421–428.PubMedGoogle Scholar
  101. Waterhouse P, Wang M, Lough T: Gene silencing as an adaptive defence against viruses. Nature2001, 411(6839):834–842.PubMedGoogle Scholar
  102. 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. Genetics1999, 153(2):705–714.PubMedGoogle Scholar
  103. Wu-Scharf D, Jeong B, Zhang C, Cerutti H: Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science2000, 290(5494):1159–1162.PubMedGoogle Scholar
  104. Yebra MJ, Bhagwat AS: A cytosine methyltransferase converts 5-methylcytosine in DNA to thymine. Biochemistry1995, 34(45):14752–14757.PubMedGoogle Scholar
  105. Yoder JA, Walsh CP, Bestor TH: Cytosine methylation and the ecology of intragenomic parasites. Trends Genet1997, 13(8):335–340.PubMedGoogle Scholar
  106. Zhou Y, Cambareri EB, Kinsey JA: DNA methylation inhibits expression and transposition of the Neurospora Tad retrotransposon. Mol Gen Genet2001, 265:748–754.Google Scholar
  107. Zilberman D, Cao X, Jacobsen SE: ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 2003, 299(5607):716–719.PubMedGoogle Scholar
  108. Zingg JM, Shen JC, Yang AS, Rapoport H, Jones PA: Methylation inhibitors can increase the rate of cytosine deamination by (cytosine-5)-DNA methyltransferase. Nucleic Acids Res1996, 24(16):3267–3275.PubMedGoogle Scholar

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© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • M.R. Rountree
  • E.U. Selker
    • 1
  1. 1.Institute of Molecular BiologyUniversity of OregonEugene

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