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Repeat-Induced Point Mutation: A Fungal-Specific, Endogenous Mutagenesis Process

  • James K. HaneEmail author
  • Angela H. Williams
  • Adam P. Taranto
  • Peter S. Solomon
  • Richard P. Oliver
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Repeat-induced point mutation (RIP) is a form of genome mutation that is targeted towards repeated DNA sequences and which is observed only in certain fungal taxa; the Pezizomycotina (filamentous Ascomycota) and some species of the Basidiomycota. RIP is widely believed to have evolved to protect fungal genomes against transposon replication.

RIP was first observed during the sexual reproductive cycle of the ascomycete Neurospora crassa. During the haploid dikaryotic stage that occurs following fertilization and prior to meiosis, the RIP process selectively mutated duplicated sequences in both DNA strands by inducing single-nucleotide point (SNP) mutations that converted C:G base pairs to T:A. This often led to the introduction of nonsense or missense mutations which affected the expression of these sequences. The precise mechanism by which detection and subsequent mutation of duplicated regions occurs is still unknown, but is dependent on a cytosine methyltransferase.

RIP has also been observed to influence the evolution of fungal genes. With the exception of ribosomal DNA repeats, RIP acts upon repeated genomic regions including tandem repeats, unlinked repeats, and large segmental duplications including endogenous genes. RIP has the potential to either enhance or impede the generation of genetic diversity. Species exhibiting high levels of RIP are observed to be deficient in gene family diversity, whereas diversity among gene families in species with low levels of RIP is increased. Furthermore, RIP has also been reported to affect non-duplicated genes adjacent to RIP-affected repetitive DNA sequences, which may drive the evolution of these genes and can promote rapid adaptation to selection pressures in some species.

Keywords

Repeat-induced point mutation Repetitive DNA Fungal genomes Neurospora crassa RIP in Neurospora crassa 

References

  1. Amyotte SG, Tan X, Pennerman K, Jimenez-Gasco Mdel M, Klosterman SJ, Ma LJ, Dobinson KF, Veronese P (2012) Transposable elements in phytopathogenic Verticillium spp.: insights into genome evolution and inter- and intra-specific diversification. BMC Genomics 13:314CrossRefPubMedCentralPubMedGoogle Scholar
  2. Aramayo R, Selker EU (2013) Neurospora crassa, a model system for epigenetics research. Cold Spring Harb Perspect Biol 5(10):a017921CrossRefPubMedGoogle Scholar
  3. Arnaise S, Zickler D, Bourdais A, Dequard-Chablat M, Debuchy R (2008) Mutations in mating-type genes greatly decrease repeat-induced point mutation process in the fungus Podospora anserina. Fungal Genet Biol 45(3):207–220CrossRefPubMedGoogle Scholar
  4. Attard A, Gout L, Ross S, Parlange F, Cattolico L, Balesdent MH, Rouxel T (2005) Truncated and RIP-degenerated copies of the LTR retrotransposon Pholy are clustered in a pericentromeric region of the Leptosphaeria maculans genome. Fungal Genet Biol 42(1):30–41CrossRefPubMedGoogle Scholar
  5. Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J, Eber F, Chevre AM, Leflon M, Rouxel T (2013) The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol 198(3):887–898CrossRefPubMedGoogle Scholar
  6. Bhat A, Tamuli R, Kasbekar DP (2004) Genetic transformation of Neurospora tetrasperma, demonstration of repeat-induced point mutation (RIP) in self-crosses and a screen for recessive RIP-defective mutants. Genetics 167(3):1155–1164CrossRefPubMedCentralPubMedGoogle Scholar
  7. Bouhouche K, Zickler D, Debuchy R, Arnaise S (2004) Altering a gene involved in nuclear distribution increases the repeat-induced point mutation process in the fungus Podospora anserina. Genetics 167(1):151–159CrossRefPubMedCentralPubMedGoogle Scholar
  8. Braumann I, van den Berg M, Kempken F (2008) Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr Genet 53:287CrossRefPubMedGoogle Scholar
  9. Brown NA, Antoniw J, Hammond-Kosack KE (2012) The predicted secretome of the plant pathogenic fungus Fusarium graminearum: a refined comparative analysis. PLoS One 7(4):e33731CrossRefPubMedCentralPubMedGoogle Scholar
  10. Cambareri EB, Jensen BC, Schabtach E, Selker EU (1989) Repeat-induced G-C to A-T mutations in Neurospora. Science 244(4912):1571–1575CrossRefPubMedGoogle Scholar
  11. Cambareri EB, Singer MJ, Selker EU (1991) Recurrence of repeat-induced point mutation (RIP) in Neurospora crassa. Genetics 127(4):699–710PubMedCentralPubMedGoogle Scholar
  12. Chicas A, Cogoni C, Macino G (2004) RNAi-dependent and RNAi-independent mechanisms contribute to the silencing of RIPed sequences in Neurospora crassa. Nucleic Acids Res 32(14):4237–4243CrossRefPubMedCentralPubMedGoogle Scholar
  13. Clutterbuck AJ (2011) Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 48(3):306–326CrossRefPubMedGoogle Scholar
  14. Crouch JA, Glasheen BM, Giunta MA, Clarke BB, Hillman BI (2008) The evolution of transposon repeat-induced point mutation in the genome of Colletotrichum cereale: Reconciling sex, recombination and homoplasy in an “asexual” pathogen. Fungal Genet Biol 45(3):190–206CrossRefPubMedGoogle Scholar
  15. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M, Adam G, Antoniw J, Baldwin T, Calvo S, Chang YL, Decaprio D, Gale LR, Gnerre S, Goswami RS, Hammond-Kosack K, Harris LJ, Hilburn K, Kennell JC, Kroken S, Magnuson JK, Mannhaupt G, Mauceli E, Mewes HW, Mitterbauer R, Muehlbauer G, Munsterkotter M, Nelson D, O'Donnell K, Ouellet T, Qi W, Quesneville H, Roncero MI, Seong KY, Tetko IV, Urban M, Waalwijk C, Ward TJ, Yao J, Birren BW, Kistler HC (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317(5843):1400–1402CrossRefPubMedGoogle Scholar
  16. Daboussi MJ, Daviere JM, Graziani S, Langin T (2002) Evolution of the Fot1 transposons in the genus Fusarium: discontinuous distribution and epigenetic inactivation. Mol Biol Evol 19(4):510–520CrossRefPubMedGoogle Scholar
  17. de Jonge R, Bolton MD, Thomma BP (2011) How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr Opin Plant Biol 14(4):400–406CrossRefPubMedGoogle Scholar
  18. de Wit PJGM, van der Burgt A, Okmen B, Stergiopoulos I, Abd-Elsalam KA, Aerts AL, Bahkali AH, Beenen HG, Chettri P, Cox MP, Datema E, de Vries RP, Dhillon B, Ganley AR, Griffiths SA, Guo Y, Hamelin RC, Henrissat B, Kabir MS, Jashni MK, Kema G, Klaubauf S, Lapidus A, Levasseur A, Lindquist E, Mehrabi R, Ohm RA, Owen TJ, Salamov A, Schwelm A, Schijlen E, Sun H, van den Burg HA, van Ham RCHJ, Zhang S, Goodwin SB, Grigoriev IV, Collemare J, Bradshaw RE (2012) The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet 8(11):e1003088CrossRefPubMedCentralPubMedGoogle Scholar
  19. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434(7036):980–986CrossRefPubMedGoogle Scholar
  20. Farman ML (2007) Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett 273(2):125–132CrossRefPubMedGoogle Scholar
  21. Ferea TL, Bowman BJ (1996) The vacuolar ATPase of Neurospora crassa is indispensable: inactivation of the vma-1 gene by repeat-induced point mutation. Genetics 143(1):147–154PubMedCentralPubMedGoogle Scholar
  22. Fincham JR, Connerton IF, Notarianni E, Harrington K (1989) Premeiotic disruption of duplicated and triplicated copies of the Neurospora crassa am (glutamate dehydrogenase) gene. Curr Genet 15(5):327–334CrossRefPubMedGoogle Scholar
  23. Freitag M, Williams RL, Kothe GO, Selker EU (2002) A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci 99(13):8802–8807CrossRefPubMedCentralPubMedGoogle Scholar
  24. Freitag M, Lee DW, Kothe GO, Pratt RJ, Aramayo R, Selker EU (2004) DNA methylation is independent of RNA interference in Neurospora. Science 304(5679):1939CrossRefPubMedGoogle Scholar
  25. Fudal I, Ross S, Brun H, Besnard AL, Ermel M, Kuhn ML, Balesdent MH, Rouxel T (2009) Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant Microbe Interact 22(8):932–941CrossRefPubMedGoogle Scholar
  26. Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20(9):417–423CrossRefPubMedGoogle Scholar
  27. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422(6934):859–868CrossRefPubMedGoogle Scholar
  28. Gan P, Ikeda K, Irieda H, Narusaka M, O'Connell RJ, Narusaka Y, Takano Y, Kubo Y, Shirasu K (2013) Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol 197(4):1236–1249CrossRefPubMedGoogle Scholar
  29. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y, Duan Z, Hu X, Xie XQ, Zhou G, Peng G, Luo Z, Huang W, Wang B, Fang W, Wang S, Zhong Y, Ma LJ, St Leger RJ, Zhao GP, Pei Y, Feng MG, Xia Y, Wang C (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7(1):e1001264CrossRefPubMedCentralPubMedGoogle Scholar
  30. Goodwin SB, M’Barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, Van der Lee TA, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canche B, Churchill AC, Conde-Ferraez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, van Ham RC, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JP, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SF, Tu H, de Vries RP, Waalwijk C, Ware SB, Wiebenga A, Zwiers LH, Oliver RP, Grigoriev IV, Kema GH (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7(6):e1002070CrossRefPubMedCentralPubMedGoogle Scholar
  31. Graia F, Lespinet O, Rimbault B, Dequard-Chablat M, Coppin E, Picard M (2001) Genome quality control: RIP (repeat-induced point mutation) comes to Podospora. Mol Microbiol 40(3):586–595CrossRefPubMedGoogle Scholar
  32. Hane JK, Oliver RP (2008) RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinform 9:478CrossRefGoogle Scholar
  33. Hane JK, Oliver RP (2010) In silico reversal of repeat-induced point mutation (RIP) identifies the origins of repeat families and uncovers obscured duplicated genes. BMC Genomics 11:655CrossRefPubMedCentralPubMedGoogle Scholar
  34. 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 10(5):e1004281CrossRefPubMedCentralPubMedGoogle Scholar
  35. Honda S, Selker EU (2008) Direct interaction between DNA methyltransferase DIM-2 and HP1 is required for DNA methylation in Neurospora crassa. Mol Cell Biol 28(19):6044–6055CrossRefPubMedCentralPubMedGoogle Scholar
  36. Honda S, Lewis ZA, Huarte M, Cho LY, David LL, Shi Y, Selker EU (2010) The DMM complex prevents spreading of DNA methylation from transposons to nearby genes in Neurospora crassa. Genes Dev 24(5):443–454CrossRefPubMedCentralPubMedGoogle Scholar
  37. Hood ME, Katawczik M, Giraud T (2005) Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170(3):1081–1089CrossRefPubMedCentralPubMedGoogle Scholar
  38. 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(3):240–247CrossRefPubMedCentralPubMedGoogle Scholar
  39. Hua-Van A, Hericourt F, Capy P, Daboussi MJ, Langin T (1998) Three highly divergent subfamilies of the impala transposable element coexist in the genome of the fungus Fusarium oxysporum. Mol Gen Genet 259(4):354–362CrossRefPubMedGoogle Scholar
  40. Hua-Van A, Langin T, Daboussi MJ (2001) Evolutionary history of the impala transposon in Fusarium oxysporum. Mol Biol Evol 18(10):1959–1969CrossRefPubMedGoogle Scholar
  41. Idnurm A, Howlett BJ (2003) Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet Biol 39(1):31–37CrossRefPubMedGoogle Scholar
  42. Ikeda K, Nakayashiki H, Kataoka T, Tamba H, Hashimoto Y, Tosa Y, Mayama S (2002) Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context. Mol Microbiol 45(5):1355–1364CrossRefPubMedGoogle Scholar
  43. Irelan JT, Hagemann AT, Selker EU (1994) High frequency repeat-induced point mutation (RIP) is not associated with efficient recombination in Neurospora. Genetics 138(4):1093–1103PubMedCentralPubMedGoogle Scholar
  44. James TC, Elgin SC (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6(11):3862–3872PubMedCentralPubMedGoogle Scholar
  45. Julien J, Poirier-Hamon S, Brygoo Y (1992) Foret1, a reverse transcriptase-like sequence in the filamentous fungus Fusarium oxysporum. Nucleic Acids Res 20(15):3933–3937CrossRefPubMedCentralPubMedGoogle Scholar
  46. Kelkar HS, Griffith J, Case ME, Covert SF, Hall RD, Keith CH, Oliver JS, Orbach MJ, Sachs MS, Wagner JR, Weise MJ, Wunderlich JK, Arnold J (2001) The Neurospora crassa genome: cosmid libraries sorted by chromosome. Genetics 157(3):979–990PubMedCentralPubMedGoogle Scholar
  47. Kempken F, Kuck U (1998) Transposons in filamentous fungi - facts and perspectives. Bioessays 20(8):652–659CrossRefPubMedGoogle Scholar
  48. Kinsey J, Helbe J (1989) Isolation of a transposable element from Neurospora crassa. Proc Natl Acad Sci U S A 86:1929–1933CrossRefPubMedCentralPubMedGoogle Scholar
  49. Kinsey JA, Garrett-Engele PW, Cambareri EB, Selker EU (1994) The Neurospora transposon Tad is sensitive to repeat-induced point mutation (RIP). Genetics 138(3):657–664PubMedCentralPubMedGoogle Scholar
  50. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BPHJ, Chen Z, Henrissat B, Lee Y-H, Park J, Garcia-Pedrajas MD, Barbara DJ, Anchieta A, de Jonge R, Santhanam P, Maruthachalam K, Atallah Z, Amyotte SG, Paz Z, Inderbitzin P, Hayes RJ, Heiman DI, Young S, Zeng Q, Engels R, Galagan J, Cuomo CA, Dobinson KF, Ma L-J (2011) Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7(7):e1002137CrossRefPubMedCentralPubMedGoogle Scholar
  51. Laurie JD, Linning R, Wong P, Bakkeren G (2013) Do TE activity and counteracting genome defenses, RNAi and methylation, shape the sex lives of smut fungi? Plant Signal Behav 8(4):e23853CrossRefPubMedGoogle Scholar
  52. Lefebvre F, Joly DL, Labbe C, Teichmann B, Linning R, Belzile F, Bakkeren G, Belanger RR (2013) The transition from a phytopathogenic smut ancestor to an anamorphic biocontrol agent deciphered by comparative whole-genome analysis. Plant Cell 25(6):1946–1959CrossRefPubMedCentralPubMedGoogle Scholar
  53. Lewis ZA, Honda S, Khlafallah TK, Jeffress JK, Freitag M, Mohn F, Schubeler D, Selker EU (2009) Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res 19(3):427–437CrossRefPubMedCentralPubMedGoogle Scholar
  54. 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 JM, 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 MH, Paolocci F, Bonfante P, Ottonello S, Wincker P (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464(7291):1033–1038CrossRefPubMedGoogle Scholar
  55. McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A 36(6):344–355CrossRefPubMedCentralPubMedGoogle Scholar
  56. McHale MT, Roberts IN, Talbot NJ, Oliver RP (1989) Expression of reverse transcriptase genes in Fulvia fulva. Mol Plant Microbe Interact 2(4):165–168CrossRefPubMedGoogle Scholar
  57. Meerupati T, Andersson KM, Friman E, Kumar D, Tunlid A, Ahren D (2013) Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genet 9(11):e1003909CrossRefPubMedCentralPubMedGoogle Scholar
  58. Miao VP, Freitag M, Selker EU (2000) Short TpA-rich segments of the zeta-eta region induce DNA methylation in Neurospora crassa. J Mol Biol 300(2):249–273CrossRefPubMedGoogle Scholar
  59. Mishra PK, Baum M, Carbon J (2011) DNA methylation regulates phenotype-dependent transcriptional activity in Candida albicans. Proc Natl Acad Sci U S A 108(29):11965–11970CrossRefPubMedCentralPubMedGoogle Scholar
  60. Montiel MD, Lee HA, Archer DB (2006) Evidence of RIP (repeat-induced point mutation) in transposase sequences of Aspergillus oryzae. Fungal Genet Biol 43(6):439–445CrossRefPubMedGoogle Scholar
  61. Nabel CS, Manning SA, Kohli RM (2012) The curious chemical biology of cytosine: deamination, methylation, and oxidation as modulators of genomic potential. ACS Chem Biol 7(1):20–30CrossRefPubMedCentralPubMedGoogle Scholar
  62. Nakayashiki H, Nishimoto N, Ikeda K, Tosa Y, Mayama S (1999) 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 Genet 261(6):958–966CrossRefPubMedGoogle Scholar
  63. Neuveglise C, Sarfati J, Latge JP, Paris S (1996) Afut1, a retrotransposon-like element from Aspergillus fumigatus. Nucleic Acids Res 24(8):1428–1434CrossRefPubMedCentralPubMedGoogle Scholar
  64. Nielsen ML, Hermansen TD, Aleksenko A (2001) A family of DNA repeats in Aspergillus nidulans has assimilated degenerated retrotransposons. Mol Genet Genomics 265(5):883–887CrossRefPubMedGoogle Scholar
  65. Ninomiya Y, Suzuki K, Ishii C, Inoue H (2004) Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc Natl Acad Sci U S A 101(33):12248–12253CrossRefPubMedCentralPubMedGoogle Scholar
  66. Noubissi FK, McCluskey K, Kasbekar DP (2000) Repeat-induced point mutation (RIP) in crosses with wild-isolated strains of Neurospora crassa: evidence for dominant reduction of RIP. Fungal Genet Biol 31(2):91–97CrossRefPubMedGoogle Scholar
  67. Nowrousian M, Stajich JE, Chu M, Engh I, Espagne E, Halliday K, Kamerewerd J, Kempken F, Knab B, Kuo HC, Osiewacz HD, Poggeler S, Read ND, Seiler S, Smith KM, Zickler D, Kuck U, Freitag M (2010) De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet 6(4):e1000891CrossRefPubMedCentralPubMedGoogle Scholar
  68. Oliver R (2012) Genomic tillage and the harvest of fungal phytopathogens. New Phytol 196(4):1015–1023CrossRefPubMedGoogle Scholar
  69. Paietta JV, Marzluf GA (1985) Gene disruption by transformation in Neurospora crassa. Mol Cell Biol 5(7):1554–1559PubMedCentralPubMedGoogle Scholar
  70. Pattemore JAH, Hane JK, Williams AH, Wilson BAL, Stodart BJ, Ash GJ (2014) The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species. BMC Genomics 15:660CrossRefPubMedCentralPubMedGoogle Scholar
  71. Ropars J, Dupont J, Fontanillas E, Rodriguez de la Vega RC, Malagnac F, Coton M, Giraud T, Lopez-Villavicencio M (2012) Sex in cheese: evidence for sexuality in the fungus Penicillium roqueforti. PLoS One 7(11):e49665CrossRefPubMedCentralPubMedGoogle Scholar
  72. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Ciuffetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GHJ, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW, Stachowiak A, Turgeon BG, Tyler BM, Vincent D, Weissenbach J, Amselem J, Quesneville H, Oliver RP, Wincker P, Balesdent M-H, Howlett BJ (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun 2:202CrossRefPubMedCentralPubMedGoogle Scholar
  73. Selker EU (1990) Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 24(1):579–613CrossRefPubMedGoogle Scholar
  74. Selker EU (2002) Repeat-induced gene silencing in fungi. Adv Genet 46:439–450CrossRefPubMedGoogle Scholar
  75. Selker E, Garrett P (1988) DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci U S A 85:6870–6874CrossRefPubMedCentralPubMedGoogle Scholar
  76. Selker EU, Cambareri EB, Jensen BC, Haack KR (1987a) Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51(5):741–752CrossRefPubMedGoogle Scholar
  77. Selker EU, Jensen BC, Richardson GA (1987b) A portable signal causing faithful DNA methylation de novo in Neurospora crassa. Science 238(4823):48–53CrossRefPubMedGoogle Scholar
  78. Singer MJ, Selker EU (1995) Genetic and epigenetic inactivation of repetitive sequences in Neurospora crassa: RIP, DNA methylation, and quelling. Curr Top Microbiol Immunol 197:165–177PubMedGoogle Scholar
  79. Smith KM, Phatale PA, Sullivan CM, Pomraning KR, Freitag M (2011) Heterochromatin is required for normal distribution of Neurospora crassa CenH3. Mol Cell Biol 31(12):2528–2542CrossRefPubMedCentralPubMedGoogle Scholar
  80. Sneh B, Burpee L, Ogoshi A (1991) Identification of Rhizoctonia species. APS Press, St. Paul, MNGoogle Scholar
  81. Stuckenbrock EH, Croll D (2014) The evolving fungal genome. Fung Biol Rev 28(1):1–12CrossRefGoogle Scholar
  82. Tamaru H, Selker EU (2003) Synthesis of signals for de novo DNA methylation in Neurospora crassa. Mol Cell Biol 23(7):2379–2394CrossRefPubMedCentralPubMedGoogle Scholar
  83. Van de Wouw AP, Cozijnsen AJ, Hane JK, Brunner PC, McDonald BA, Oliver RP, Howlett BJ (2010) Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6(11):e1001180CrossRefPubMedCentralPubMedGoogle Scholar
  84. Vleeshouwers VG, Oliver RP (2014) Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol Plant Microbe Interact 27(3):196–206CrossRefPubMedGoogle Scholar
  85. Volpe T, Martienssen RA (2011) RNA interference and heterochromatin assembly. Cold Spring Harb Perspect Biol 3(9):a003731CrossRefPubMedCentralPubMedGoogle Scholar
  86. Watters MK, Randall TA, Margolin BS, Selker EU, Stadler DR (1999) Action of repeat-induced point mutation on both strands of a duplex and on tandem duplications of various sizes in Neurospora. Genetics 153(2):705–714PubMedCentralPubMedGoogle Scholar
  87. Yeadon PJ, Catcheside DE (1995) Guest: a 98 bp inverted repeat transposable element in Neurospora crassa. Mol Gen Genet 247(1):105–109CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • James K. Hane
    • 1
    Email author
  • Angela H. Williams
    • 2
  • Adam P. Taranto
    • 3
  • Peter S. Solomon
    • 3
  • Richard P. Oliver
    • 1
  1. 1.Centre for Crop and Disease ManagementCurtin UniversityPerthAustralia
  2. 2.The Institute of AgricultureThe University of Western AustraliaCrawleyAustralia
  3. 3.Plant Sciences Division, Research School of BiologyThe Australian National UniversityCanberraAustralia

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