Skip to main content
SpringerLink
Log in

5 Fungal Chromatin and Its Role in Regulation of Gene Expression

  • Chapter
  • First Online:
Fungal Genomics

Part of the book series: The Mycota ((MYCOTA,volume 13))

Abstract

Changes in chromatin structure and composition are now recognized as important for gene regulation, especially the initiation of transcription, for which access to the transcriptional start sites of genes is required. While there is a rich literature centered on hemiascomycetous yeasts, less is known about the filamentous fungi, although they seem ideally suited for comparative chromatin biology. This chapter summarizes current knowledge of chromatin components, in particular the histones, and reviews recent advances in the study of histone modification enzymes of filamentous fungi. Two major topics drive the field forward in the fungi: the study of formation and maintenance of constitutive heterochromatin and studies on histone modification-mediated transcriptional regulation geared predominantly toward the expression of “cryptic” gene clusters that generate secondary metabolites. These clusters present perhaps the best example of “facultative heterochromatin” in the filamentous fungi. Study of these large regions promises to fill the existing gaps in our current knowledge about chromatin-mediated gene regulation in filamentous fungi, now undertaken by a combination of genomic, transcriptomic, and metabolomic resources.

The histones are commonly regarded as unpleasant proteins for rigorous studies.

—Cook et al. 1956, cited in Van Holde 1988, p. 69

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adam M, Robert F, Larochelle M, Gaudreau L (2001) H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol 21:6270–6279

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Adhvaryu KK, Selker EU (2008) Protein phosphatase PP1 is required for normal DNA methylation in Neurospora. Genes Dev 22:3391–3396

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Adhvaryu KK, Berge E, Tamaru H, Freitag M, Selker EU (2011) Substitutions in the amino-terminal tail of Neurospora histone H3 have varied effects on DNA methylation. PLoS Genet 7:e1002423

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191–1200

    Article  PubMed  CAS  Google Scholar 

  • Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007) New nomenclature for chromatin-modifying enzymes. Cell 131:633–636

    Article  PubMed  CAS  Google Scholar 

  • Amaike S, Keller NP (2009) Distinct roles for VeA and LaeA in development and pathogenesis of Aspergillus flavus. Eukaryot Cell 8:1051–1060

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Andersen MR, Nielsen JB, Klitgaard A, Petersen LM, Zachariasen M, Hansen TJ, Blicher LH, Gotfredsen CH, Larsen TO, Nielsen KF, Mortensen UH (2013) Accurate prediction of secondary metabolite gene clusters in filamentous fungi. Proc Natl Acad Sci U S A 110:E99–E107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Arnaud MB, Cerqueira GC, Inglis DO, Skrzypek MS, Binkley J, Chibucos MC, Crabtree J, Howarth C, Orvis J, Shah P, Wymore F, Binkley G, Miyasato SR, Simison M, Sherlock G, Wortman JR (2012) The Aspergillus Genome Database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources. Nucleic Acids Res 40:D653–D659

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Atoui A, Kastner C, Larey CM, Thokala R, Etxebeste O, Espeso EA, Fischer R, Calvo AM (2010) Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet Biol 47:962–972

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Barra JL, Rhounim L, Rossignol JL, Faugeron G (2000) Histone H1 is dispensable for methylation-associated gene silencing in Ascobolus immersus and essential for long life span. Mol Cell Biol 20:61–69

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bayram O, Braus GH (2011) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev. doi:10.1111/j.1574-6976.2011.00285.x

    PubMed  Google Scholar 

  • Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506

    Article  PubMed  CAS  Google Scholar 

  • Beisel C, Paro R (2011) Silencing chromatin: comparing modes and mechanisms. Nat Rev Genet 12:123–135

    Article  PubMed  CAS  Google Scholar 

  • Bergmann JH, Rodriguez MG, Martins NM, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LE, Earnshaw WC (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30:328–340

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Black BE, Cleveland DW (2011) Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 144:471–479

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73:417–435

    Article  PubMed  CAS  Google Scholar 

  • Bok JW, Keller NP (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3:527–535

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bok JW, Balajee SA, Marr KA, Andes D, Nielsen KF, Frisvad JC, Keller NP (2005) LaeA, a regulator of morphogenetic fungal virulence factors. Eukaryot Cell 4:1574–1582

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bok JW, Noordermeer D, Kale SP, Keller NP (2006) Secondary metabolic gene cluster silencing in Aspergillus nidulans. Mol Microbiol 61:1636–1645

    Article  PubMed  CAS  Google Scholar 

  • Bok JW, Chiang YM, Szewczyk E, Reyes-Dominguez Y, Davidson AD, Sanchez JF, Lo HC, Watanabe K, Strauss J, Oakley BR, Wang CC, Keller NP (2009) Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol 5:462–464

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32

    Article  PubMed  CAS  Google Scholar 

  • Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites – strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22

    Article  PubMed  CAS  Google Scholar 

  • Brosch G, Loidl P, Graessle S (2008) Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol Rev 32:409–439

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bushley KE, Raja R, Jaiswal P, Cumbie JS, Nonogaki M, Boyd AE, Owensby CA, Knaus BJ, Elser J, Miller D, Di Y, McPhail KL, Spatafora JW (2013) The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet 9:e1003496

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SI (2005) Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37:809–819

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chang SS, Zhang Z, Liu Y (2012) RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66:305–323

    Article  PubMed  CAS  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 32:4237–4243

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407–421

    Article  PubMed  CAS  Google Scholar 

  • Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S, Schwartz DC, Freitag M, Ma LJ, Danchin EG, Henrissat B, Coutinho PM, Nelson DR, Straney D, Napoli CA, Barker BM, Gribskov M, Rep M, Kroken S, Molnar I, Rensing C, Kennell JC, Zamora J, Farman ML, Selker EU, Salamov A, Shapiro H, Pangilinan J, Lindquist E, Lamers C, Grigoriev IV, Geiser DM, Covert SF, Temporini E, Vanetten HD (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Colot V, Maloisel L, Rossignol JL (1996) Interchromosomal transfer of epigenetic states in Ascobolus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell 86:855–864

    Article  PubMed  CAS  Google Scholar 

  • Condon BJ, Leng Y, Wu D, Bushley KE, Ohm RA, Otillar R, Martin J, Schackwitz W, Grimwood J, MohdZainudin N, Xue C, Wang R, Manning VA, Dhillon B, Tu ZJ, Steffenson BJ, Salamov A, Sun H, Lowry S, LaButti K, Han J, Copeland A, Lindquist E, Barry K, Schmutz J, Baker SE, Ciuffetti LM, Grigoriev IV, Zhong S, Turgeon BG (2013) Comparative genome structure, secondary metabolite, and effector coding capacity across Cochliobolus pathogens. PLoS Genet 9:e1003233

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Connolly LR, Smith KM, Freitag M (2013) The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLOS Genet 9:e1003916

    Article  PubMed Central  PubMed  Google Scholar 

  • Cook HA, Eldredge NT, Haley MI, Kupke DW, Luck JM, Rasmussen PS (1956) On the fractionation of thymus histone. Arch Biochem Biophys 65:449–467

    Article  PubMed  CAS  Google Scholar 

  • Croll D, Zala M, McDonald BA (2013) Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet 9:e1003567

    Article  PubMed Central  PubMed  CAS  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 317:1400–1402

    Article  PubMed  CAS  Google Scholar 

  • Dai J, Hyland EM, Yuan DS, Huang H, Bader JS, Boeke JD (2008) Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. Cell 134:1066–1078

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • de la Cruz X, Lois S, Sanchez-Molina S, Martinez-Balbas MA (2005) Do protein motifs read the histone code? Bioessays 27:164–175

    Article  PubMed  CAS  Google Scholar 

  • de Wit PJ, 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 RC, 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:e1003088

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Duncan IW (2002) Transvection effects in Drosophila. Annu Rev Genet 36:521–556

    Article  PubMed  CAS  Google Scholar 

  • Durrin LK, Mann RK, Kayne PS, Grunstein M (1991) Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell 65:1023–1031

    Article  PubMed  CAS  Google Scholar 

  • Earnshaw WC, Migeon BR (1985) Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92:290–296

    Article  PubMed  CAS  Google Scholar 

  • Ehinger A, Denison SH, May GS (1990) Sequence, organization and expression of the core histone genes of Aspergillus nidulans. Mol Gen Genet 222:416–424

    Article  PubMed  CAS  Google Scholar 

  • Eissenberg JC, Shilatifard A (2010) Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 339:240–249

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ekwall K (2005) Genome-wide analysis of HDAC function. Trends Genet 21:608–615

    Article  PubMed  CAS  Google Scholar 

  • Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, Glass NL, Taylor JW (2011) Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci U S A 108:2831–2836

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Erhard KF Jr, Hollick JB (2011) Paramutation: a process for acquiring trans-generational regulatory states. Curr Opin Plant Biol 14:210–216

    Article  PubMed  CAS  Google Scholar 

  • Farboud B, Nix P, Jow MM, Gladden JM, Meyer BJ (2013) Molecular antagonism between X-chromosome and autosome signals determines nematode sex. Genes Dev 27:1159–1178

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Faugeron G, Rhounim L, Rossignol J-L (1990) How does the cell count the number of ectopic copies of a gene in the premeiotic inactivation process acting in Ascobolus immersus? Genetics 124:585–591

    PubMed Central  PubMed  CAS  Google Scholar 

  • Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, Anderson MJ, Crabtree J, Silva JC, Badger JH, Albarraq A, Angiuoli S, Bussey H, Bowyer P, Cotty PJ, Dyer PS, Egan A, Galens K, Fraser-Liggett CM, Haas BJ, Inman JM, Kent R, Lemieux S, Malavazi I, Orvis J, Roemer T, Ronning CM, Sundaram JP, Sutton G, Turner G, Venter JC, White OR, Whitty BR, Youngman P, Wolfe KH, Goldman GH, Wortman JR, Jiang B, Denning DW, Nierman WC (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Feng Q, Wang H, Ng HH, Erdjument-Bromage H, Tempst P, Struhl K, Zhang Y (2002) Methylation of H3-lysine 79 is mediated by a new family of HMTases without a SET domain. Curr Biol 12:1052–1058

    Article  PubMed  CAS  Google Scholar 

  • Fisch KM, Gillaspy AF, Gipson M, Henrikson JC, Hoover AR, Jackson L, Najar FZ, Wagele H, Cichewicz RH (2009) Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger. J Ind Microbiol Biotechnol 36:1199–1213

    Article  PubMed  CAS  Google Scholar 

  • Fischle W, Wang Y, Allis CD (2003) Binary switches and modification cassettes in histone biology and beyond. Nature 425:475–479

    Article  PubMed  CAS  Google Scholar 

  • Folco HD, Freitag M, Ramon A, Temporini ED, Alvarez ME, Garcia I, Scazzocchio C, Selker EU, Rosa AL (2003) Histone H1 is required for proper regulation of pyruvate decarboxylase gene expression in Neurospora crassa. Eukaryot Cell 2:341–350

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Freedman T, Pukkila PJ (1993) De novo methylation of repeated sequences in Coprinus cinereus. Genetics 135:357–366

    PubMed Central  PubMed  CAS  Google Scholar 

  • Freeman L, Kurumizaka H, Wolffe AP (1996) Functional domains for assembly of histones H3 and H4 into the chromatin of Xenopus embryos. Proc Natl Acad Sci U S A 93:12780–12785

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Freidkin I, Katcoff DJ (2001) Specific distribution of the Saccharomyces cerevisiae linker histone homolog HHO1p in the chromatin. Nucleic Acids Res 29:4043–4051

    PubMed Central  PubMed  CAS  Google Scholar 

  • Freitag M, Hickey PC, Khlafallah TK, Read ND, Selker EU (2004) HP1 is essential for DNA methylation in Neurospora. Mol Cell 13:427–434

    Article  PubMed  CAS  Google Scholar 

  • Frisvad JC (2012) Media and growth conditions for induction of secondary metabolite production. Methods Mol Biol 944:47–58

    PubMed  CAS  Google Scholar 

  • Gacek A, Strauss J (2012) The chromatin code of fungal secondary metabolite gene clusters. Appl Microbiol Biotechnol 95:1389–1404

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Penalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115

    Article  PubMed  CAS  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 197:1236–1249

    Article  PubMed  CAS  Google Scholar 

  • Gary JD, Clarke S (1998) RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol 61:65–131

    Article  PubMed  CAS  Google Scholar 

  • Gasser SM, Cockell MM (2001) The molecular biology of the SIR proteins. Gene 279:1–16

    Article  PubMed  CAS  Google Scholar 

  • Gibbons JG, Rokas A (2013) The function and evolution of the Aspergillus genome. Trends Microbiol 21:14–22

    Article  PubMed Central  PubMed  CAS  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:e1002070

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Goto DB, Nakayama J (2012) RNA and epigenetic silencing: insight from fission yeast. Dev Growth Differ 54:129–141

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gottschling DE (2007) Epigenetics: from phenomenon to field. In: Allis CD, Jenuwein T, Reinberg D (eds) Epigenetics. Cold Spring Harbor Laboratory Press, New York, pp 1–14

    Google Scholar 

  • Gottschling DE, Aparicio OM, Billington BL, Zakian VA (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751–762

    Article  PubMed  CAS  Google Scholar 

  • Goyon C, Faugeron G (1989) Targeted transformation of Ascobolus immersus and de novo methylation of the resulting duplicated DNA sequences. Mol Cell Biol 9:2818–2827

    PubMed Central  PubMed  CAS  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 39:1–11

    Article  Google Scholar 

  • Grewal SI (2010) RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20:134–141

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Grewal SI, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8:35–46

    Article  PubMed  CAS  Google Scholar 

  • Grunstein M (1990) Histone function in transcription. Annu Rev Cell Biol 6:643–678

    Article  PubMed  CAS  Google Scholar 

  • Haber JE (2012) Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191:33–64

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hall LE, Mitchell SE, O’Neill RJ (2012) Pericentric and centromeric transcription: a perfect balance required. Chromosome Res 20:535–546

    Article  PubMed  CAS  Google Scholar 

  • Hays SM, Swanson J, Selker EU (2002) Identification and characterization of the genes encoding the core histones and histone variants of Neurospora crassa. Genetics 160:961–973

    PubMed Central  PubMed  CAS  Google Scholar 

  • Henikoff S (1990) Position-effect variegation after 60 years. Trends Genet 6:422–426

    Article  PubMed  CAS  Google Scholar 

  • Henrikson JC, Hoover AR, Joyner PM, Cichewicz RH (2009) A chemical epigenetics approach for engineering the in situ biosynthesis of a cryptic natural product from Aspergillus niger. Org Biomol Chem 7:435–438

    Article  PubMed  CAS  Google Scholar 

  • Hollick JB (2012) Paramutation: a trans-homolog interaction affecting heritable gene regulation. Curr Opin Plant Biol 15:536–543

    Article  PubMed  CAS  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 28:6044–6055

    Article  PubMed Central  PubMed  CAS  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 24:443–454

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Honda S, Lewis ZA, Shimada K, Fischle W, Sack R, Selker EU (2012) Heterochromatin protein 1 forms distinct complexes to direct histone deacetylation and DNA methylation. Nat Struct Mol Biol 19(471–477):S1

    Google Scholar 

  • Hori T, Fukagawa T (2012) Establishment of the vertebrate kinetochores. Chromosome Res 20:547–561

    Article  PubMed  CAS  Google Scholar 

  • Hou H, Wang Y, Kallgren SP, Thompson J, Yates JR 3rd, Jia S (2010) Histone variant H2A.Z regulates centromere silencing and chromosome segregation in fission yeast. J Biol Chem 285:1909–1918

    Article  PubMed Central  PubMed  CAS  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 39:31–37

    Article  PubMed  CAS  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 45:1355–1364

    Article  PubMed  CAS  Google Scholar 

  • Inglis DO, Binkley J, Skrzypek MS, Arnaud MB, Cerqueira GC, Shah P, Wymore F, Wortman JR, Sherlock G (2013) Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae. BMC Microbiol 13:91

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560

    Article  PubMed  CAS  Google Scholar 

  • Jamieson K, Rountree MR, Lewis ZA, Stajich JE, Selker EU (2013) Regional control of histone H3 lysine 27 methylation in Neurospora. Proc Natl Acad Sci U S A 110:6027–6032

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jeon Y, Sarma K, Lee JT (2012) New and Xisting regulatory mechanisms of X chromosome inactivation. Curr Opin Genet Dev 22:62–71

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jiang J, Liu X, Yin Y, Ma Z (2011) Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PLoS One 6:e28291

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kalashnikova AA, Winkler DD, McBryant SJ, Henderson RK, Herman JA, DeLuca JG, Luger K, Prenni JE, Hansen JC (2013) Linker histone H1.0 interacts with an extensive network of proteins found in the nucleolus. Nucleic Acids Res 41:4026–4035

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kale SP, Milde L, Trapp MK, Frisvad JC, Keller NP, Bok JW (2008) Requirement of LaeA for secondary metabolism and sclerotial production in Aspergillus flavus. Fungal Genet Biol 45:1422–1429

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Karimi-Aghcheh R, Bok JW, Phatale PA, Smith KM, Baker SE, Lichius A, Omann M, Zeilinger S, Seiboth B, Rhee C, Keller NP, Freitag M, Kubicek CP (2013) Functional analyses of Trichoderma reesei LAE1 reveal conserved and contrasting roles of this regulator. G3 (Bethesda) 3:369–378

    Article  CAS  Google Scholar 

  • Kasinsky HE, Lewis JD, Dacks JB, Ausio J (2001) Origin of H1 linker histones. Faseb J 15:34–42

    Article  PubMed  CAS  Google Scholar 

  • Kennison JA, Southworth JW (2002) Transvection in Drosophila. Adv Genet 46:399–420

    Article  PubMed  CAS  Google Scholar 

  • Klose RJ, Zhang Y (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8:307–318

    Article  PubMed  CAS  Google Scholar 

  • Knuf C, Nielsen J (2012) Aspergilli: systems biology and industrial applications. Biotechnol J 7:1147–1155

    Article  PubMed  CAS  Google Scholar 

  • Koerner MV, Barlow DP (2010) Genomic imprinting-an epigenetic gene-regulatory model. Curr Opin Genet Dev 20:164–170

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kouzminova EA, Selker EU (2001) Dim-2 encodes a DNA-methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO J 20:4309–4323

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kowalski A, Palyga J (2012) Linker histone subtypes and their allelic variants. Cell Biol Int 36:981–996

    Article  PubMed  CAS  Google Scholar 

  • Kruesi WS, Core LJ, Waters CT, Lis JT, Meyer BJ (2013) Condensin controls recruitment of RNA polymerase II to achieve nematode X-chromosome dosage compensation. Elife 2:e00808

    Article  PubMed Central  PubMed  Google Scholar 

  • Kuo MH, Xu XJ, Bolck HA, Guo D (2009) Functional connection between histone acetyltransferase Gcn5p and methyltransferase Hmt1p. Biochim Biophys Acta 1789:395–402

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120

    Article  PubMed  CAS  Google Scholar 

  • Lachner M, O’Sullivan RJ, Jenuwein T (2003) An epigenetic road map for histone lysine methylation. J Cell Sci 116:2117–2124

    Article  PubMed  CAS  Google Scholar 

  • Lacoste N, Utley RT, Hunter JM, Poirier GG, Cote J (2002) Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. J Biol Chem 277:30421–30424

    Article  PubMed  CAS  Google Scholar 

  • Lee JT, Bartolomei MS (2013) X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 152:1308–1323

    Article  PubMed  CAS  Google Scholar 

  • Lee I, Oh JH, Shwab EK, Dagenais TR, Andes D, Keller NP (2009) HdaA, a class 2 histone deacetylase of Aspergillus fumigatus, affects germination and secondary metabolite production. Fungal Genet Biol 46:782–790

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK, Pertsemlidis A, Lewis ZA, Freitag M, Selker EU, Mello CC, Liu Y (2010) Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol Cell 38:803–814

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH (2003) Suv39h-mediated histone h3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13:1192–1200

    Article  PubMed  CAS  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 19:427–437

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lewis ZA, Adhvaryu KK, Honda S, Shiver AL, Knip M, Sack R, Selker EU (2010a) DNA methylation and normal chromosome behavior in Neurospora depend on five components of a histone methyltransferase complex, DCDC. PLoS Genet 6:e1001196

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lewis ZA, Adhvaryu KK, Honda S, Shiver AL, Selker EU (2010b) Identification of DIM-7, a protein required to target the DIM-5 H3 methyltransferase to chromatin. Proc Natl Acad Sci U S A 107:8310–8315

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li KK, Luo C, Wang D, Jiang H, Zheng YG (2010) Chemical and biochemical approaches in the study of histone methylation and demethylation. Med Res Rev. doi:10.1002/med.20228:1-53

    PubMed Central  Google Scholar 

  • Li Y, Wang C, Liu W, Wang G, Kang Z, Kistler HC, Xu JR (2011) The HDF1 histone deacetylase gene is important for conidiation, sexual reproduction, and pathogenesis in Fusarium graminearum. Mol Plant Microbe Interact 24:487–496

    Article  PubMed  CAS  Google Scholar 

  • Ling X, Harkness TA, Schultz MC, Fisher Adams G, Grunstein M (1996) Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. Genes Dev 10:686–699

    Article  PubMed  CAS  Google Scholar 

  • Lu X, Wontakal SN, Emelyanov AV, Morcillo P, Konev AY, Fyodorov DV, Skoultchi AI (2009) Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure. Genes Dev 23:452–465

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lu X, Wontakal SN, Kavi H, Kim BJ, Guzzardo PM, Emelyanov AV, Xu N, Hannon GJ, Zavadil J, Fyodorov DV, Skoultchi AI (2013) Drosophila H1 regulates the genetic activity of heterochromatin by recruitment of Su(var)3–9. Science 340:78–81

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ma J, Wing RA, Bennetzen JL, Jackson SA (2007) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 23:134–139

    Article  PubMed  CAS  Google Scholar 

  • Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, Rep M (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161

    Article  PubMed  Google Scholar 

  • Maloisel L, Rossignol JL (1998) Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev 12:1381–1389

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Manning VA, Pandelova I, Dhillon B, Wilhelm LJ, Goodwin SB, Berlin AM, Figueroa M, Freitag M, Hane JK, Henrissat B, Holman WH, Kodira CD, Martin J, Oliver RP, Robbertse B, Schackwitz W, Schwartz DC, Spatafora JW, Turgeon BG, Yandava C, Young S, Zhou S, Zeng Q, Grigoriev IV, Ma LJ, Ciuffetti LM (2013) 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) 3:41–63

    Article  CAS  Google Scholar 

  • Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343–349

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martienssen RA, Zaratiegui M, Goto DB (2005) RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet 21:450–456

    Article  PubMed  CAS  Google Scholar 

  • McStay B, Grummt I (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol 24:131–157

    Article  PubMed  CAS  Google Scholar 

  • Mellone BG, Ball L, Suka N, Grunstein MR, Partridge JF, Allshire RC (2003) Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr Biol 13:1748–1757

    Article  PubMed  CAS  Google Scholar 

  • Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112:725–736

    Article  PubMed  CAS  Google Scholar 

  • Meyer BJ (2010) Targeting X chromosomes for repression. Curr Opin Genet Dev 20:179–189

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Miura A, Nakamura M, Inagaki S, Kobayashi A, Saze H, Kakutani T (2009) An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J 28:1078–1086

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nakanishi S, Sanderson BW, Delventhal KM, Bradford WD, Staehling-Hampton K, Shilatifard A (2008) A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat Struct Mol Biol 15:881–888

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, Garcia JL, Garcia MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, Gwilliam R, Haas B, Haas H, Harris D, Horiuchi H, Huang J, Humphray S, Jimenez J, Keller N, Khouri H, Kitamoto K, Kobayashi T, Konzack S, Kulkarni R, Kumagai T, Lafon A, Latge JP, Li W, Lord A, Lu C, Majoros WH, May GS, Miller BL, Mohamoud Y, Molina M, Monod M, Mouyna I, Mulligan S, Murphy L, O’Neil S, Paulsen I, Penalva MA, Pertea M, Price C, Pritchard BL, Quail MA, Rabbinowitsch E, Rawlins N, Rajandream MA, Reichard U, Renauld H, Robson GD, Rodriguez de Cordoba S, Rodriguez-Pena JM, Ronning CM, Rutter S, Salzberg SL, Sanchez M, Sanchez-Ferrero JC, Saunders D, Seeger K, Squares R, Squares S, Takeuchi M, Tekaia F, Turner G, Vazquez de Aldana CR, Weidman J, White O, Woodward J, Yu JH, Fraser C, Galagan JE, Asai K, Machida M, Hall N, Barrell B, Denning DW (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151–1156

    Article  PubMed  CAS  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:e1000891

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nutzmann HW, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, Gacek A, Schumann J, Hertweck C, Strauss J, Brakhage AA (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci U S A 108:14282–14287

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Oppikofer M, Kueng S, Gasser SM (2013) SIR-nucleosome interactions: structure-function relationships in yeast silent chromatin. Gene 527:10–25

    Article  PubMed  CAS  Google Scholar 

  • Palmer JM, Keller NP (2010) Secondary metabolism in fungi: does chromosomal location matter? Curr Opin Microbiol 13:431–436

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Palmer DK, O’Day K, Wener MH, Andrews BS, Margolis RL (1987) A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J Cell Biol 104:805–815

    Article  PubMed  CAS  Google Scholar 

  • Palmer JM, Bok JW, Lee S, Dagenais TR, Andes DR, Kontoyiannis DP, Keller NP (2013a) Loss of CclA, required for histone 3 lysine 4 methylation, decreases growth but increases secondary metabolite production in Aspergillus fumigatus. PeerJ 1:e4

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Palmer JM, Theisen JM, Duran RM, Grayburn WS, Calvo AM, Keller NP (2013b) Secondary metabolism and development is mediated by LlmF control of VeA subcellular localization in Aspergillus nidulans. PLoS Genet 9:e1003193

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Patterton HG, Landel CC, Landsman D, Peterson CL, Simpson RT (1998) The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J Biol Chem 273:7268–7276

    Article  PubMed  CAS  Google Scholar 

  • Perrin RM, Fedorova ND, Bok JW, Cramer RA, Wortman JR, Kim HS, Nierman WC, Keller NP (2007) Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog 3:e50

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9–20

    Article  PubMed  CAS  Google Scholar 

  • Pomraning KR, Connolly LR, Whalen JP, Smith KM, Freitag M (2013) Repeat-induced point mutation, DNA methylation and heterochromatin in Gibberella zeae (anamorph: Fusarium graminearum). In: Brown D, Proctor RH (eds) Fusarium genomics and molecular and cellular biology. Horizon Scientific Press, Norwich, p 93

    Google Scholar 

  • Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ptashne M (2013a) Epigenetics: core misconcept. Proc Natl Acad Sci U S A 110:7101–7103

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ptashne M (2013b) Faddish stuff: epigenetics and the inheritance of acquired characteristics. FASEB J 27:1–2

    Article  PubMed  CAS  Google Scholar 

  • Rando OJ, Winston F (2012) Chromatin and transcription in yeast. Genetics 190:351–387

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rep M, Kistler HC (2010) The genomic organization of plant pathogenicity in Fusarium species. Curr Opin Plant Biol 13:420–426

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Dominguez Y, Bok JW, Berger H, Shwab EK, Basheer A, Gallmetzer A, Scazzocchio C, Keller N, Strauss J (2010) Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Mol Microbiol 76:1376–1386

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rhounim L, Rossignol J-L, Faugeron G (1992) Epimutation of repeated genes in Ascobolus immersus. EMBO J 11:4451–4457

    PubMed Central  PubMed  CAS  Google Scholar 

  • Rine J, Herskowitz I (1987) Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics 116:9–22

    PubMed Central  PubMed  CAS  Google Scholar 

  • Rine J, Strathern JN, Hicks JB, Herskowitz I (1979) A suppressor of mating-type locus mutations in Saccharomyces cerevisiae: evidence for and identification of cryptic mating-type loci. Genetics 93:877–901

    PubMed Central  PubMed  CAS  Google Scholar 

  • Robyr D, Suka Y, Xenarios I, Kurdistani SK, Wang A, Suka N, Grunstein M (2002) Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109:437–446

    Article  PubMed  CAS  Google Scholar 

  • Rountree MR, Selker EU (2010) DNA methylation and the formation of heterochromatin in Neurospora crassa. Heredity 105:38–44

    Article  PubMed  CAS  Google Scholar 

  • Rudolph T, Beuch S, Reuter G (2013) Lysine-specific histone demethylase LSD1 and the dynamic control of chromatin. Biol Chem 394:1019–1028

    Article  PubMed  CAS  Google Scholar 

  • Rusche LN, Kirchmaier AL, Rine J (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72:481–516

    Article  PubMed  CAS  Google Scholar 

  • Salminen A, Kaarniranta K (2009) SIRT1 regulates the ribosomal DNA locus: epigenetic candles twinkle longevity in the Christmas tree. Biochem Biophys Res Commun 378:6–9

    Article  PubMed  CAS  Google Scholar 

  • Santoro R (2005) The silence of the ribosomal RNA genes. Cell Mol Life Sci 62:2067–2079

    Article  PubMed  CAS  Google Scholar 

  • Saze H, Shiraishi A, Miura A, Kakutani T (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319:462–465

    Article  PubMed  CAS  Google Scholar 

  • Schuettengruber B, Martinez AM, Iovino N, Cavalli G (2011) Trithorax group proteins: switching genes on and keeping them active. Nat Rev Mol Cell Biol 12:799–814

    Article  PubMed  CAS  Google Scholar 

  • Seiboth B, Karimi RA, Phatale PA, Linke R, Hartl L, Sauer DG, Smith KM, Baker SE, Freitag M, Kubicek CP (2012) The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol 84:1150–1164

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Selker EU (1998) Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc Natl Acad Sci U S A 95:9430–9435

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Selker EU, Stevens JN (1987) Signal for DNA methylation associated with tandem duplication in Neurospora crassa. Mol Cell Biol 7:1032–1038

    PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shen X, Yu L, Weir JW, Gorovsky MA (1995) Linker histones are not essential and affect chromatin condensation in vivo. Cell 82:47–56

    Article  PubMed  CAS  Google Scholar 

  • Shwab EK, Keller NP (2008) Regulation of secondary metabolite production in filamentous ascomycetes. Mycol Res 112:225–230

    Article  PubMed  CAS  Google Scholar 

  • Shwab EK, Bok JW, Tribus M, Galehr J, Graessle S, Keller NP (2007) Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot Cell 6:1656–1664

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10:697–708

    PubMed  CAS  Google Scholar 

  • Simon MD, Wang CI, Kharchenko PV, West JA, Chapman BA, Alekseyenko AA, Borowsky ML, Kuroda MI, Kingston RE (2011) The genomic binding sites of a noncoding RNA. Proc Natl Acad Sci U S A 108:20497–20502

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sims RJ 3rd, Nishioka K, Reinberg D (2003) Histone lysine methylation: a signature for chromatin function. Trends Genet 19:629–639

    Article  PubMed  CAS  Google Scholar 

  • Singer MJ, Marcotte BA, Selker EU (1995) DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol Cell Biol 15:5586–5597

    PubMed Central  PubMed  CAS  Google Scholar 

  • Smith KM, Kothe GO, Matsen CB, Khlafallah TK, Adhvaryu KK, Hemphill M, Freitag M, Motamedi MR, Selker EU (2008) The fungus Neurospora crassa displays telomeric silencing mediated by multiple sirtuins and by methylation of histone H3 lysine 9. Epigenetics Chromatin 1:5

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smith KM, Dobosy JR, Reifsnyder JE, Rountree MR, Anderson DC, Green GR, Selker EU (2010) H2B- and H3-specific histone deacetylases are required for DNA methylation in Neurospora crassa. Genetics 186:1207–1216

    Article  PubMed Central  PubMed  CAS  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 31:2528–2542

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smith KM, Galazka JM, Phatale PA, Connolly LR, Freitag M (2012a) Centromeres of filamentous fungi. Chromosome Res 20:635–656

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smith KM, Phatale PA, Bredeweg EL, Connolly LR, Pomraning KR, Freitag M (2012b) Epigenetics of filamentous fungi. In: Myers RA (ed) Epigenetic regulation and epigenomics. Wiley-VCH, Weinheim, pp 1063–1105

    Google Scholar 

  • Soukup AA, Chiang YM, Bok JW, Reyes-Dominguez Y, Oakley BR, Wang CC, Strauss J, Keller NP (2012) Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production. Mol Microbiol 86:314–330

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stam M (2009) Paramutation: a heritable change in gene expression by allelic interactions in trans. Mol Plant 2:578–588

    Article  PubMed  CAS  Google Scholar 

  • Straub T, Zabel A, Gilfillan GD, Feller C, Becker PB (2013) Different chromatin interfaces of the Drosophila dosage compensation complex revealed by high-shear ChIP-seq. Genome Res 23:473–485

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Strauss J, Reyes-Dominguez Y (2011) Regulation of secondary metabolism by chromatin structure and epigenetic codes. Fungal Genet Biol 48:62–69

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stukenbrock EH, Dutheil JY (2012) Comparing fungal genomes: insight into functional and evolutionary processes. Methods Mol Biol 835:531–548

    Article  PubMed  CAS  Google Scholar 

  • Stukenbrock EH, Bataillon T, Dutheil JY, Hansen TT, Li R, Zala M, McDonald BA, Wang J, Schierup MH (2011) The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res 21:2157–2166

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH (2012) Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc Natl Acad Sci U S A 109:10954–10959

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sullivan BA, Karpen GH (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11:1076–1083

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sun JQ, Hatanaka A, Oki M (2011) Boundaries of transcriptionally silent chromatin in Saccharomyces cerevisiae. Genes Genet Syst 86:73–81

    Article  PubMed  CAS  Google Scholar 

  • Talbert PB, Henikoff S (2010) Histone variants – ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11:264–275

    Article  PubMed  CAS  Google Scholar 

  • Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277–283

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34:75–79

    Article  PubMed  CAS  Google Scholar 

  • Tennen RI, Chua KF (2011) Chromatin regulation and genome maintenance by mammalian SIRT6. Trends Biochem Sci 36:39–46

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tormo JR, Asensio FJ, Bills GF (2012) Manipulating filamentous fungus chemical phenotypes by growth on nutritional arrays. Methods Mol Biol 944:59–78

    PubMed  CAS  Google Scholar 

  • Tribus M, Galehr J, Trojer P, Brosch G, Loidl P, Marx F, Haas H, Graessle S (2005) HdaA, a major class 2 histone deacetylase of Aspergillus nidulans, affects growth under conditions of oxidative stress. Eukaryot Cell 4:1736–1745

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tribus M, Bauer I, Galehr J, Rieser G, Trojer P, Brosch G, Loidl P, Haas H, Graessle S (2010) A novel motif in fungal class 1 histone deacetylases is essential for growth and development of Aspergillus. Mol Biol Cell 21:345–353

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Trojer P, Brandtner EM, Brosch G, Loidl P, Galehr J, Linzmaier R, Haas H, Mair K, Tribus M, Graessle S (2003) Histone deacetylases in fungi: novel members, new facts. Nucleic Acids Res 31:3971–3981

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Umemura M, Koyama Y, Takeda I, Hagiwara H, Ikegami T, Koike H, Machida M (2013) Fine de novo sequencing of a fungal genome using only SOLiD short read data: verification on Aspergillus oryzae RIB40. PLoS One 8:e63673

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Upadhyay AK, Cheng X (2011) Dynamics of histone lysine methylation: structures of methyl writers and erasers. Prog Drug Res 67:107–124

    PubMed Central  PubMed  CAS  Google Scholar 

  • van Holde K (1988) Chromatin. Springer, New York

    Google Scholar 

  • van Leeuwen F, Gafken PR, Gottschling DE (2002) Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109:745–756

    Article  PubMed  Google Scholar 

  • Verdaasdonk JS, Bloom K (2011) Centromeres: unique chromatin structures that drive chromosome segregation. Nat Rev Mol Cell Biol 12:320–332

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Voigt P, Reinberg D (2011) Histone tails: ideal motifs for probing epigenetics through chemical biology approaches. Chembiochem 12:236–252

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vujatovic O, Zaragoza K, Vaquero A, Reina O, Bernues J, Azorin F (2012) Drosophila melanogaster linker histone dH1 is required for transposon silencing and to preserve genome integrity. Nucleic Acids Res 40:5402–5414

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Waddington CH (1952) The epigenetics of birds. Cambridge University Press, Cambridge

    Google Scholar 

  • Wang X, Sena Filho JG, Hoover AR, King JB, Ellis TK, Powell DR, Cichewicz RH (2010) Chemical epigenetics alters the secondary metabolite composition of guttate excreted by an atlantic-forest-soil-derived Penicillium citreonigrum. J Nat Prod 73:942–948

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Weiner A, Chen HV, Liu CL, Rahat A, Klien A, Soares L, Gudipati M, Pfeffner J, Regev A, Buratowski S, Pleiss JA, Friedman N, Rando OJ (2012) Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10:e1001369

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Whetstine JR, Nottke A, Lan F, Huarte M, Smolikov S, Chen Z, Spooner E, Li E, Zhang G, Colaiacovo M, Shi Y (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125:467–481

    Article  PubMed  CAS  Google Scholar 

  • Wiemann P, Brown DW, Kleigrewe K, Bok JW, Keller NP, Humpf HU, Tudzynski B (2010) FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence. Mol Microbiol 77:972–994

    CAS  Google Scholar 

  • Wiemann P, Sieber CM, von Bargen KW, Studt L, Niehaus EM, Espino JJ, Huss K, Michielse CB, Albermann S, Wagner D, Bergner SV, Connolly LR, Fischer A, Reuter G, Kleigrewe K, Bald T, Wingfield BD, Ophir R, Freeman S, Hippler M, Smith KM, Brown DW, Proctor RH, Munsterkotter M, Freitag M, Humpf HU, Guldener U, Tudzynski B (2013) Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathog 9:e1003475

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Williams SC (2013) Epigenetics. Proc Natl Acad Sci U S A 110:3209

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Williams RB, Henrikson JC, Hoover AR, Lee AE, Cichewicz RH (2008) Epigenetic remodeling of the fungal secondary metabolome. Org Biomol Chem 6:1895–1897

    Article  PubMed  CAS  Google Scholar 

  • Wolffe AP, Khochbin S, Dimitrov S (1997) What do linker histones do in chromatin? Bioessays 19:249–255

    Article  PubMed  CAS  Google Scholar 

  • Wyrick JJ, Parra MA (2009) The role of histone H2A and H2B post-translational modifications in transcription: a genomic perspective. Biochim Biophys Acta 1789:37–44

    Article  PubMed  CAS  Google Scholar 

  • Xhemalce B, Dawson MA, Bannister AJ (2012) Histone modifications. In: Myers RA (ed) Epigenetic regulation and epigenomics. Wiley-VCH, Weinheim

    Google Scholar 

  • Xiong L, Wang Y (2011) Mapping post-translational modifications of histones H2A, H2B and H4 in Schizosaccharomyces pombe. Int J Mass Spectrom 301:159–165

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xiong L, Adhvaryu KK, Selker EU, Wang Y (2010) Mapping of lysine methylation and acetylation in core histones of Neurospora crassa. Biochemistry 49:5236–5243

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xu H, Wang J, Hu Q, Quan Y, Chen H, Cao Y, Li C, Wang Y, He Q (2010) DCAF26, an adaptor protein of Cul4-based E3, is essential for DNA methylation in Neurospora crassa. PLoS Genet 6:e1001132

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yan H, Jin W, Nagaki K, Tian S, Ouyang S, Buell CR, Talbert PB, Henikoff S, Jiang J (2005) Transcription and histone modifications in the recombination-free region spanning a rice centromere. Plant Cell 17:3227–3238

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang SM, Kim BJ, Norwood Toro L, Skoultchi AI (2013) H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation. Proc Natl Acad Sci U S A 110:1708–1713

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yankulov K (2011) Dare to challenge the silence? Telomeric gene silencing revisited. Nucleus 2:513–516

    Article  PubMed  Google Scholar 

  • Young TJ, Kirchmaier AL (2012) Cell cycle regulation of silent chromatin formation. Biochim Biophys Acta 1819:303–312

    Article  PubMed  CAS  Google Scholar 

  • Yun M, Wu J, Workman JL, Li B (2011) Readers of histone modifications. Cell Res 21:564–578

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zaidi SK, Young DW, Montecino M, van Wijnen AJ, Stein JL, Lian JB, Stein GS (2011) Bookmarking the genome: maintenance of epigenetic information. J Biol Chem 286:18355–18361

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhao Y, Shen Y, Yang S, Wang J, Hu Q, Wang Y, He Q (2010) Ubiquitin ligase components Cullin4 and DDB1 are essential for DNA methylation in Neurospora crassa. J Biol Chem 285:4355–4365

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhao C, Waalwijk C, de Wit PJ, Tang D, van der Lee T (2013) RNA-Seq analysis reveals new gene models and alternative splicing in the fungal pathogen Fusarium graminearum. BMC Genomics 14:21

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhou VW, Goren A, Bernstein BE (2011) Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12:7–18

    Article  PubMed  CAS  Google Scholar 

  • Zofall M, Fischer T, Zhang K, Zhou M, Cui B, Veenstra TD, Grewal SI (2009) Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature 461:419–422

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zolan ME, Pukkila PJ (1986) Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6:195–200

    PubMed Central  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Biophysics, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR, 97331-7305, USA

    Michael Freitag

Authors
  1. Michael Freitag
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Freitag .

Editor information

Editors and Affiliations

  1. Department of General and Molecular Bota, Ruhr-University of Bochum, Bochum, Germany

    Minou Nowrousian

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Freitag, M. (2014). 5 Fungal Chromatin and Its Role in Regulation of Gene Expression. In: Nowrousian, M. (eds) Fungal Genomics. The Mycota, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-45218-5_5

Download citation

Publish with us

Policies and ethics

Search

Navigation