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

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

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References

  • 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 13:314

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Aramayo R, Selker EU (2013) Neurospora crassa, a model system for epigenetics research. Cold Spring Harb Perspect Biol 5(10):a017921

    CrossRef  PubMed  Google Scholar 

  • 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):207–220

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):30–41

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):887–898

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):1155–1164

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):151–159

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Braumann I, van den Berg M, Kempken F (2008) Repeat induced point mutation in two asexual fungi, Aspergillus niger and Penicillium chrysogenum. Curr Genet 53:287

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):e33731

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Cambareri EB, Jensen BC, Schabtach E, Selker EU (1989) Repeat-induced G-C to A-T mutations in Neurospora. Science 244(4912):1571–1575

    CrossRef  CAS  PubMed  Google Scholar 

  • Cambareri EB, Singer MJ, Selker EU (1991) Recurrence of repeat-induced point mutation (RIP) in Neurospora crassa. Genetics 127(4):699–710

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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):4237–4243

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Clutterbuck AJ (2011) Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 48(3):306–326

    CrossRef  PubMed  Google Scholar 

  • 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):190–206

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):1400–1402

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):510–520

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):400–406

    CrossRef  PubMed  Google Scholar 

  • 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):e1003088

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):980–986

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):125–132

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):147–154

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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):327–334

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):8802–8807

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):1939

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):932–941

    CrossRef  CAS  PubMed  Google Scholar 

  • Galagan JE, Selker EU (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20(9):417–423

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):859–868

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):1236–1249

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):e1001264

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):e1002070

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):586–595

    CrossRef  CAS  PubMed  Google Scholar 

  • Hane JK, Oliver RP (2008) RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinform 9:478

    CrossRef  Google Scholar 

  • 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 11:655

    CrossRef  PubMed Central  PubMed  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 10(5):e1004281

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):6044–6055

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):443–454

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Hood ME, Katawczik M, Giraud T (2005) Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170(3):1081–1089

    CrossRef  PubMed Central  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(3):240–247

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):354–362

    CrossRef  CAS  PubMed  Google Scholar 

  • Hua-Van A, Langin T, Daboussi MJ (2001) Evolutionary history of the impala transposon in Fusarium oxysporum. Mol Biol Evol 18(10):1959–1969

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):31–37

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):1355–1364

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):1093–1103

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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):3862–3872

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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):3933–3937

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):979–990

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kempken F, Kuck U (1998) Transposons in filamentous fungi - facts and perspectives. Bioessays 20(8):652–659

    CrossRef  CAS  PubMed  Google Scholar 

  • Kinsey J, Helbe J (1989) Isolation of a transposable element from Neurospora crassa. Proc Natl Acad Sci U S A 86:1929–1933

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):657–664

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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):e1002137

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):e23853

    CrossRef  PubMed  Google Scholar 

  • 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):1946–1959

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):427–437

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):1033–1038

    CrossRef  CAS  PubMed  Google Scholar 

  • McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A 36(6):344–355

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • McHale MT, Roberts IN, Talbot NJ, Oliver RP (1989) Expression of reverse transcriptase genes in Fulvia fulva. Mol Plant Microbe Interact 2(4):165–168

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):e1003909

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):249–273

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):11965–11970

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):439–445

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):20–30

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):958–966

    CrossRef  CAS  PubMed  Google Scholar 

  • Neuveglise C, Sarfati J, Latge JP, Paris S (1996) Afut1, a retrotransposon-like element from Aspergillus fumigatus. Nucleic Acids Res 24(8):1428–1434

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Nielsen ML, Hermansen TD, Aleksenko A (2001) A family of DNA repeats in Aspergillus nidulans has assimilated degenerated retrotransposons. Mol Genet Genomics 265(5):883–887

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):12248–12253

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):91–97

    CrossRef  CAS  PubMed  Google Scholar 

  • 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):e1000891

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • Oliver R (2012) Genomic tillage and the harvest of fungal phytopathogens. New Phytol 196(4):1015–1023

    CrossRef  CAS  PubMed  Google Scholar 

  • Paietta JV, Marzluf GA (1985) Gene disruption by transformation in Neurospora crassa. Mol Cell Biol 5(7):1554–1559

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 15:660

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):e49665

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 2:202

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • Selker EU (1990) Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 24(1):579–613

    CrossRef  CAS  PubMed  Google Scholar 

  • Selker EU (2002) Repeat-induced gene silencing in fungi. Adv Genet 46:439–450

    CrossRef  CAS  PubMed  Google Scholar 

  • Selker E, Garrett P (1988) DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci U S A 85:6870–6874

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Selker EU, Cambareri EB, Jensen BC, Haack KR (1987a) Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51(5):741–752

    CrossRef  CAS  PubMed  Google Scholar 

  • Selker EU, Jensen BC, Richardson GA (1987b) A portable signal causing faithful DNA methylation de novo in Neurospora crassa. Science 238(4823):48–53

    CrossRef  CAS  PubMed  Google Scholar 

  • Singer MJ, Selker EU (1995) Genetic and epigenetic inactivation of repetitive sequences in Neurospora crassa: RIP, DNA methylation, and quelling. Curr Top Microbiol Immunol 197:165–177

    CAS  PubMed  Google Scholar 

  • 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):2528–2542

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • Sneh B, Burpee L, Ogoshi A (1991) Identification of Rhizoctonia species. APS Press, St. Paul, MN

    Google Scholar 

  • Stuckenbrock EH, Croll D (2014) The evolving fungal genome. Fung Biol Rev 28(1):1–12

    CrossRef  Google Scholar 

  • Tamaru H, Selker EU (2003) Synthesis of signals for de novo DNA methylation in Neurospora crassa. Mol Cell Biol 23(7):2379–2394

    CrossRef  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):e1001180

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):196–206

    CrossRef  CAS  PubMed  Google Scholar 

  • Volpe T, Martienssen RA (2011) RNA interference and heterochromatin assembly. Cold Spring Harb Perspect Biol 3(9):a003731

    CrossRef  PubMed Central  PubMed  Google Scholar 

  • 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):705–714

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yeadon PJ, Catcheside DE (1995) Guest: a 98 bp inverted repeat transposable element in Neurospora crassa. Mol Gen Genet 247(1):105–109

    CrossRef  CAS  PubMed  Google Scholar 

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Correspondence to James K. Hane BMolBiol. (Hons.), Ph. D. Bioinformatics .

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Hane, J.K., Williams, A.H., Taranto, A.P., Solomon, P.S., Oliver, R.P. (2015). Repeat-Induced Point Mutation: A Fungal-Specific, Endogenous Mutagenesis Process. In: van den Berg, M., Maruthachalam, K. (eds) Genetic Transformation Systems in Fungi, Volume 2. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-10503-1_4

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