Skip to main content

Centrochromatin of Fungi

  • Chapter
  • First Online:
Centromeres and Kinetochores

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 56))

Abstract

The centromere is an essential chromosomal locus that dictates the nucleation point for assembly of the kinetochore and subsequent attachment of spindle microtubules during chromosome segregation. Research over the last decades demonstrated that centromeres are defined by a combination of genetic and epigenetic factors. Recent work showed that centromeres are quite diverse and flexible and that many types of centromere sequences and centromeric chromatin (“centrochromatin”) have evolved. The kingdom of the fungi serves as an outstanding example of centromere plasticity, including organisms with centromeres as diverse as 0.15–300 kb in length, and with different types of chromatin states for most species examined thus far. Some of the species in the less familiar taxa provide excellent opportunities to help us better understand centromere biology in all eukaryotes, which may improve treatment options against fungal infection, and biotechnologies based on fungi. This review summarizes the current knowledge of fungal centromeres and centrochromatin, including an outlook for future research.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

  • Aldrup-MacDonald ME, Kuo ME, Sullivan LL, Chew K, Sullivan BA (2016) Genomic variation within alpha satellite DNA influences centromere location on human chromosomes with metastable epialleles. Genome Res 26:1301–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aleksenko A, Nielsen ML, Clutterbuck AJ (2001) Genetic and physical mapping of two centromere-proximal regions of chromosome IV in Aspergillus nidulans. Fungal Genet Biol 32:45–54

    Article  CAS  PubMed  Google Scholar 

  • Allshire RC, Ekwall K (2015) Epigenetic regulation of chromatin states in schizosaccharomyces pombe. Cold Spring Harb Perspect Biol 7:a018770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Badouin H, Hood ME, Gouzy J, Aguileta G, Siguenza S, Perlin MH, Cuomo CA, Fairhead C, Branca A, Giraud T (2015) Chaos of rearrangements in the mating-type chromosomes of the anther-smut fungus microbotryum lychnidis-dioicae. Genetics 200:1275–1284

    Article  PubMed  PubMed Central  Google Scholar 

  • Baker RE, Rogers K (2006) Phylogenetic analysis of fungal centromere H3 proteins. Genetics 174:1481–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basenko EY, Sasaki T, Ji L, Prybol CJ, Burckhardt RM, Schmitz RJ, Lewis ZA (2015) Genome-wide redistribution of H3K27me3 is linked to genotoxic stress and defective growth. Proc Natl Acad Sci U S A 112:E6339–E6348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beadle GW (1932) A possible influence of the spindle fibre on crossing-over in drosophila. Proc Natl Acad Sci U S A 18:160–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542

    Article  CAS  PubMed  Google Scholar 

  • Biggins S (2013) The composition, functions, and regulation of the budding yeast kinetochore. Genetics 194:817–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloom KS (2014) Centromeric heterochromatin: the primordial segregation machine. Annu Rev Genet 48:457–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, Zelter A, Kalkman ER, ORourke R, Bowring F, Yeadon J, Ishii C, Suzuki K, Sakai W, Pratt R (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burrack LS, Applen SE, Berman J (2011) The requirement for the dam1 complex is dependent upon the number of kinetochore proteins and microtubules. Curr Biol 21:889–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burrack LS, Berman J (2012) Neocentromeres and epigenetically inherited features of centromeres. Chromosome Res 20:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burrack LS, Hutton HF, Matter KJ, Clancey SA, Liachko I, Plemmons AE, Saha A, Power EA, Turman B, Thevandavakkam MA, Ay F, Dunham MJ, Berman J (2016) Neocentromeres provide chromosome segregation accuracy and centromere clustering to multiple loci along a candida albicans chromosome. PLoS Genet 12:e1006317

    Article  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Cambareri EB, Aisner R, Carbon J (1998) Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats. Mol Cell Biol 18:5465–5477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carroll CW, Milks KJ, Straight AF (2010) Dual recognition of CENP-A nucleosomes is required for centromere assembly. J Cell Biol 189:1143–1155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Centola M, Carbon J (1994) Cloning and characterization of centromeric DNA from Neurospora crassa. Mol Cell Biol 14:1510–1519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatterjee G, Sankaranarayanan SR, Guin K, Thattikota Y, Padmanabhan S, Siddharthan R, Sanyal K (2016) Repeat-associated fission yeast-like regional centromeres in the ascomycetous budding yeast candida tropicalis. PLoS Genet 12:e1005839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi ES, Stralfors A, Castillo AG, Durand-Dubief M, Ekwall K, Allshire RC (2011) Identification of noncoding transcripts from within CENP-A chromatin at fission yeast centromeres. J Biol Chem 286:23600–23607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choo KH (1998) Why is the centromere so cold? Genome Res 8:81–82

    Article  CAS  PubMed  Google Scholar 

  • Clarke L (1998) Centromeres: proteins, protein complexes, and repeated domains at centromeres of simple eukaryotes. Curr Opin Genet Dev 8:212–218

    Article  CAS  PubMed  Google Scholar 

  • Clarke L, Carbon J (1980) Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504–509

    Article  CAS  PubMed  Google Scholar 

  • Clarke L (1985) The structure and function of yeast centromeres. Ann Rev Genet 19:29–55

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  PubMed Central  CAS  Google Scholar 

  • Coughlan AY, Hanson SJ, Byrne KP, Wolfe KH (2016) Centromeres of the yeast komagataella phaffii (pichia pastoris) have a simple inverted-repeat structure. Genome Biol Evol 8:2482–2492

    Article  PubMed  PubMed Central  Google Scholar 

  • D’Archivio S, Wickstead B (2017) Trypanosome outer kinetochore proteins suggest conservation of chromosome segregation machinery across eukaryotes. J Cell Biol 216:379–391

    Google Scholar 

  • Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pohlmann R, Luedi P, Choi S, Wing RA, Flavier A, Gaffney TD, Philippsen P (2004) The Ashbya gossypii genome as a tool for mapping the ancient saccharomyces cerevisiae genome. Science 304:304–307

    Article  CAS  PubMed  Google Scholar 

  • Djupedal I, Kos-Braun IC, Mosher RA, Soderholm N, Simmer F, Hardcastle TJ, Fender A, Heidrich N, Kagansky A, Bayne E, Wagner EG, Baulcombe DC, Allshire RC, Ekwall K (2009) Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. EMBO J 28:3832–3844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drinnenberg IA, deYoung D, Henikoff S, Malik HS (2014) Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife 3

    Google Scholar 

  • Du Y, Topp CN, Dawe RK (2010) DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 6:e1000835

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, Shendure J, Fields S, Blau CA, Noble WS (2010) A three-dimensional model of the yeast genome. Nature 465:363–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumesic PA, Homer CM, Moresco JJ, Pack LR, Shanle EK, Coyle SM, Strahl BD, Fujimori DG, Yates JR 3rd, Madhani HD (2015) Product binding enforces the genomic specificity of a yeast polycomb repressive complex. Cell 160:204–218

    Article  CAS  PubMed  Google Scholar 

  • Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321

    Article  CAS  PubMed  Google Scholar 

  • Fachinetti D, Folco HD, Nechemia-Arbely Y, Valente LP, Nguyen K, Wong AJ, Zhu Q, Holland AJ, Desai A, Jansen LE, Cleveland DW (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nat Cell Biol 15:1056–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faino L, Seidl MF, Datema E, van den Berg GC, Janssen A, Wittenberg AH, Thomma BP (2015) Single-molecule real-time sequencing combined with optical mapping yields completely finished fungal genome. MBio 6

    Google Scholar 

  • Fang J, Liu Y, Wei Y, Deng W, Yu Z, Huang L, Teng Y, Yao T, You Q, Ruan H, Chen P, Xu RM, Li G (2015) Structural transitions of centromeric chromatin regulate the cell cycle-dependent recruitment of CENP-N. Genes Dev 29:1058–1073

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  CAS  Google Scholar 

  • Folco HD, Campbell CS, May KM, Espinoza CA, Oegema K, Hardwick KG, Grewal SI, Desai A (2015) The CENP-A N-tail confers epigenetic stability to centromeres via the CENP-T branch of the CCAN in fission yeast. Curr Biol 25:348–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:394–397

    Article  CAS  Google Scholar 

  • Fournier P, Abbas A, Chasles M, Kudla B, Ogrydziak DM, Yaver D, Xuan JW, Peito A, Ribet AM, Feynerol C et al (1993) Colocalization of centromeric and replicative functions on autonomously replicating sequences isolated from the yeast Yarrowia lipolytica. Proc Natl Acad Sci U S A 90:4912–4916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freitag M (2016) The kinetochore interaction network (KIN) of ascomycetes. Mycologia 108:485–505

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Freitag M, Lee DW, Kothe GO, Pratt RJ, Aramayo R, Selker EU (2004b) DNA methylation is independent of RNA interference in Neurospora. Science 304:1939

    Article  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 U S A 99:8802–8807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukagawa T, Earnshaw WC (2014) The centromere: chromatin foundation for the kinetochore machinery. Dev Cell 30:496–508

    Article  CAS  PubMed  PubMed Central  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 422:859–868

    Article  CAS  PubMed  Google Scholar 

  • Galazka JM, Klocko AD, Uesaka M, Honda S, Selker EU, Freitag M (2016) Neurospora chromosomes are organized by blocks of importin alpha-dependent heterochromatin that are largely independent of H3K9me3. Genome Res 26:1069–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gladyshev E, Kleckner N (2016) Recombination-independent recognition of DNA homology for repeat-induced point mutation (rip) is modulated by the underlying nucleotide sequence. PLoS Genet 12:e1006015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gonen S, Akiyoshi B, Iadanza MG, Shi D, Duggan N, Biggins S, Gonen T (2012) The structure of purified kinetochores reveals multiple microtubule-attachment sites. Nat Struct Mol Biol 19:925–929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon JL, Byrne KP, Wolfe KH (2011) Mechanisms of chromosome number evolution in yeast. PLoS Genet 7:e1002190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall IM, Shankaranarayana GD, Noma KI, Ayoub N, Cohen A, Grewal SI (2002) Establishment and maintenance of a heterochromatin domain. Science 297:2232–2237

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  CAS  PubMed  Google Scholar 

  • Heus JJ, Zonneveld BJ, Steensma HY, Van den Berg JA (1994) Mutational analysis of centromeric DNA elements of Kluyveromyces lactis and their role in determining the species specificity of the highly homologous centromeres from K. lactis and Saccharomyces cerevisiae. Mol Gen Genet 243:325–333

    Article  CAS  PubMed  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schussler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    Article  PubMed  Google Scholar 

  • James TY, Toledo LF, Rodder D, da Silva Leite D, Belasen AM, Betancourt-Roman CM, Jenkinson TS, Soto-Azat C, Lambertini C, Longo AV, Ruggeri J, Collins JP, Burrowes PA, Lips KR, Zamudio KR, Longcore JE (2015) Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol Evol 5:4079–4097

    Article  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Jamieson K, Wiles ET, McNaught KJ, Sidoli S, Leggett N, Shao Y, Garcia BA, Selker EU (2016) Loss of HP1 causes depletion of H3K27me3 from facultative heterochromatin and gain of H3K27me2 at constitutive heterochromatin. Genome Res 26:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janbon G, Ormerod KL, Paulet D, Byrnes EJ 3rd, Yadav V, Chatterjee G, Mullapudi N, Hon CC, Billmyre RB, Brunel F, Bahn YS, Chen W, Chen Y, Chow EW, Coppee JY, Floyd-Averette A, Gaillardin C, Gerik KJ, Goldberg J, Gonzalez-Hilarion S, Gujja S, Hamlin JL, Hsueh YP, Ianiri G, Jones S, Kodira CD, Kozubowski L, Lam W, Marra M, Mesner LD, Mieczkowski PA, Moyrand F, Nielsen K, Proux C, Rossignol T, Schein JE, Sun S, Wollschlaeger C, Wood IA, Zeng Q, Neuveglise C, Newlon CS, Perfect JR, Lodge JK, Idnurm A, Stajich JE, Kronstad JW, Sanyal K, Heitman J, Fraser JA, Cuomo CA, Dietrich FS (2014) Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet 10:e1004261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, Berman J, He X, Salmon ED, Bloom KS (2008) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181:587–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, Simmer F, Urano T, Hamilton GL, Allshire RC (2009) Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324:1716–1719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrugge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101

    Article  PubMed  CAS  Google Scholar 

  • Ketel C, Wang HS, McClellan M, Bouchonville K, Selmecki A, Lahav T, Gerami-Nejad M, Berman J (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5:e1000400

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kilani J, Fillinger S (2016) Phenylpyrroles: 30 years, two molecules and (nearly) no resistance. Front Microbiol 7:2014

    Article  PubMed  PubMed Central  Google Scholar 

  • Kitada K, Yamaguchi E, Hamada K, Arisawa M (1997) Structural analysis of a Candida glabrata centromere and its functional homology to the Saccharomyces cerevisiae centromere. Curr Genet 31:122–127

    Article  CAS  PubMed  Google Scholar 

  • Klocko AD, Ormsby T, Galazka JM, Leggett NA, Uesaka M, Honda S, Freitag M, Selker EU (2016) Normal chromosome conformation depends on subtelomeric facultative heterochromatin in Neurospora crassa. Proc Natl Acad Sci U S A 113(52):15048–15053

    Google Scholar 

  • Klocko AD, Rountree MR, Grisafi PL, Hays SM, Adhvaryu KK, Selker EU (2015) Neurospora importin alpha is required for normal heterochromatic formation and DNA methylation. PLoS Genet 11:e1005083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kobayashi N, Suzuki Y, Schoenfeld LW, Muller CA, Nieduszynski C, Wolfe KH, Tanaka TU (2015) Discovery of an unconventional centromere in budding yeast redefines evolution of point centromeres. Curr Biol 25:2026–2033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koo DH, Zhao H, Jiang J (2016) Chromatin-associated transcripts of tandemly repetitive DNA sequences revealed by RNA-FISH. Chromosome Res 24(4):467–480

    Google Scholar 

  • Koren A, Tsai HJ, Tirosh I, Burrack LS, Barkai N, Berman J (2010) Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 6:e1001068

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lam AL, Boivin CD, Bonney CF, Rudd MK, Sullivan BA (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci U S A 103:4186–4191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawrimore J, Aicher JK, Hahn P, Fulp A, Kompa B, Vicci L, Falvo M, Taylor RM 2nd, Bloom K (2016) ChromoShake: a chromosome dynamics simulator reveals that chromatin loops stiffen centromeric chromatin. Mol Biol Cell 27:153–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ledesma-Amaro R, Dulermo T, Nicaud JM (2015) Engineering Yarrowia lipolytica to produce biodiesel from raw starch. Biotechnol Biofuels 8:148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA, Allen JE, Bosdet IE, Brent MR, Chiu R, Doering TL, Donlin MJ, DSouza CA, Fox DS, Grinberg V, Fu J, Fukushima M, Haas BJ, Huang JC, Janbon G, Jones SJ, Koo HL, Krzywinski MI, Kwon-Chung JK, Lengeler KB, Maiti R, Marra MA, Marra RE, Mathewson CA, Mitchell TG, Pertea M, Riggs FR, Salzberg SL, Schein JE, Shvartsbeyn A, Shin H, Shumway M, Specht CA, Suh BB, Tenney A, Utterback TR, Wickes BL, Wortman JR, Wye NH, Kronstad JW, Lodge JK, Heitman J, Davis RW, Fraser CM, Hyman RW (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321–1324

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch DB, Logue ME, Butler G, Wolfe KH (2010) Chromosomal G + C content evolution in yeasts: systematic interspecies differences, and GC-poor troughs at centromeres. Genome Biol Evol 2:572–583

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Malik HS, Henikoff S (2002) Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev 12:711–718

    Article  CAS  PubMed  Google Scholar 

  • Malik HS, Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138:1067–1082

    Article  CAS  PubMed  Google Scholar 

  • Marie-Nelly H, Marbouty M, Cournac A, Flot JF, Liti G, Parodi DP, Syan S, Guillen N, Margeot A, Zimmer C, Koszul R (2014) High-quality genome (re)assembly using chromosomal contact data. Nat Commun 5:5695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, de Leon AL, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A, Schoch CL, Yao J, Barabote R, Nelson MA, Detter C, Bruce D, Kuske CR, Xie G, Richardson P, Rokhsar DS, Lucas SM, Rubin EM, Dunn-Coleman N, Ward M, Brettin TS (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26:553–560

    Article  CAS  PubMed  Google Scholar 

  • Meksem K, Shultz J, Tebbji F, Jamai A, Henrich J, Kranz H, Arenz M, Schlueter T, Ishihara H, Jyothi LN, Zhang HB, Lightfoot DA (2005) A bacterial artificial chromosome based physical map of the Ustilago maydis genome. Genome 48:207–216

    Article  CAS  PubMed  Google Scholar 

  • Mendoza L, Vilela R, Voelz K, Ibrahim AS, Voigt K, Lee SC (2014) Human fungal pathogens of mucorales and entomophthorales. Cold Spring Harb Perspect Med 5

    Google Scholar 

  • Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7:R23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miller DE, Smith CB, Kazemi NY, Cockrell AJ, Arvanitakas AV, Blumenstiel JP, Jaspersen SL, Hawley RS (2016) Whole-genome analysis of individual meiotic events in drosophila melanogaster reveals that noncrossover gene conversions are insensitive to interference and the centromere Effect. Genetics 203:159–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Mishra PK, Baum M, Carbon J (2007) Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Mol Genet Genomics 278:455–465

    Article  CAS  PubMed  Google Scholar 

  • Mizuguchi T, Fudenberg G, Mehta S, Belton JM, Taneja N, Folco HD, FitzGerald P, Dekker J, Mirny L, Barrowman J, Grewal SI (2014) Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature 516(7531):432–435

    Google Scholar 

  • Morales L, Noel B, Porcel B, Marcet-Houben M, Hullo MF, Sacerdot C, Tekaia F, Leh-Louis V, Despons L, Khanna V, Aury JM, Barbe V, Couloux A, Labadie K, Pelletier E, Souciet JL, Boekhout T, Gabaldon T, Wincker P, Dujon B (2013) Complete DNA sequence of Kuraishia capsulata illustrates novel genomic features among budding yeasts (Saccharomycotina). Genome Biol Evol 5:2524–2539

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM (2013) Trichoderma research in the genome era. Annu Rev Phytopathol 51:105–129

    Article  CAS  PubMed  Google Scholar 

  • Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y (2002) Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4:89–93

    Article  CAS  PubMed  Google Scholar 

  • Ohzeki J, Larionov V, Earnshaw WC, Masumoto H (2015) Genetic and epigenetic regulation of centromeres: a look at HAC formation. Chromosome Res 23:87–103

    Article  CAS  PubMed  Google Scholar 

  • Padmanabhan S, Thakur J, Siddharthan R, Sanyal K (2008) Rapid evolution of Cse4p-rich centromeric DNA sequences in closely related pathogenic yeasts, Candida albicans and Candida dubliniensis. Proc Natl Acad Sci U S A 105:19797–19802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer DK, ODay K, Trong HL, Charbonneau H, Margolis RL (1991) Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc Natl Acad Sci U S A 88:3734–3738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer DK, ODay 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  CAS  PubMed  Google Scholar 

  • Pidoux AL, Allshire RC (2005) The role of heterochromatin in centromere function. Philos Trans R Soc Lond B Biol Sci 360:569–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pombert JF, Xu J, Smith DR, Heiman D, Young S, Cuomo CA, Weiss LM, Keeling PJ (2013) Complete genome sequences from three genetically distinct strains reveal high intraspecies genetic diversity in the microsporidian Encephalitozoon cuniculi. Eukaryot Cell 12:503–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pomraning KR, Smith KM, Freitag M (2011) Bulk segregant analysis followed by high-throughput sequencing reveals the Neurospora cell cycle gene, ndc-1, to be allelic with the gene for ornithine decarboxylase, spe-1. Eukaryot Cell 10:724–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravin NV, Eldarov MA, Kadnikov VV, Beletsky AV, Schneider J, Mardanova ES, Smekalova EM, Zvereva MI, Dontsova OA, Mardanov AV, Skryabin KG (2013) Genome sequence and analysis of methylotrophic yeast Hansenula polymorpha DL1. BMC Genom 14:837

    Article  CAS  Google Scholar 

  • Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, Habib N, Wapinski I, Roy S, Lin MF, Heiman DI, Young SK, Furuya K, Guo Y, Pidoux A, Chen HM, Robbertse B, Goldberg JM, Aoki K, Bayne EH, Berlin AM, Desjardins CA, Dobbs E, Dukaj L, Fan L, FitzGerald MG, French C, Gujja S, Hansen K, Keifenheim D, Levin JZ, Mosher RA, Muller CA, Pfiffner J, Priest M, Russ C, Smialowska A, Swoboda P, Sykes SM, Vaughn M, Vengrova S, Yoder R, Zeng Q, Allshire R, Baulcombe D, Birren BW, Brown W, Ekwall K, Kellis M, Leatherwood J, Levin H, Margalit H, Martienssen R, Nieduszynski CA, Spatafora JW, Friedman N, Dalgaard JZ, Baumann P, Niki H, Regev A, Nusbaum C (2011) Comparative functional genomics of the fission yeasts. Science 332:930–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley TT, Muzny CA, Swiatlo E, Legendre DP (2016) Breaking the mold: a review of mucormycosis and current pharmacological treatment options. Ann Pharmacother 50:747–757

    Article  PubMed  Google Scholar 

  • Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, Eastman JM, Richards-Hrdlicka K, Joneson S, Jenkinson TS, Longcore JE, Parra Olea G, Toledo LF, Arellano ML, Medina EM, Restrepo S, Flechas SV, Berger L, Briggs CJ, Stajich JE (2013) Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc Natl Acad Sci U S A 110:9385–9390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosic S, Erhardt S (2016) No longer a nuisance: long non-coding RNAs join CENP-A in epigenetic centromere regulation. Cell Mol Life Sci 73:1387–1398

    Article  CAS  PubMed  Google Scholar 

  • Rosic S, Kohler F, Erhardt S (2014) Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol 207:335–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanyal K (2012) How do microbial pathogens make CENs? PLoS Pathog 8:e1002463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanyal K, Baum M, Carbon J (2004) Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci U S A 101:11374–11379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmoll M, Dattenbock C, Carreras-Villasenor N, Mendoza-Mendoza A, Tisch D, Aleman MI, Baker SE, Brown C, Cervantes-Badillo MG, Cetz-Chel J, Cristobal-Mondragon GR, Delaye L, Esquivel-Naranjo EU, Frischmann A, Gallardo-Negrete Jde J, Garcia-Esquivel M, Gomez-Rodriguez EY, Greenwood DR, Hernandez-Onate M, Kruszewska JS, Lawry R, Mora-Montes HM, Munoz-Centeno T, Nieto-Jacobo MF, Nogueira Lopez G, Olmedo-Monfil V, Osorio-Concepcion M, Pilsyk S, Pomraning KR, Rodriguez-Iglesias A, Rosales-Saavedra MT, Sanchez-Arreguin JA, Seidl-Seiboth V, Stewart A, Uresti-Rivera EE, Wang CL, Wang TF, Zeilinger S, Casas-Flores S, Herrera-Estrella A (2016) The genomes of three uneven siblings: Footprints of the lifestyles of three trichoderma species. Microbiol Mol Biol Rev 80:205–327

    Article  PubMed  PubMed Central  Google Scholar 

  • Schotanus K, Soyer JL, Connolly LR, Grandaubert J, Happel P, Smith KM, Freitag M, Stukenbrock EH (2015) Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenetics Chromatin 8:41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scott KC (2013) Transcription and ncRNAs: at the cent(rome)re of kinetochore assembly and maintenance. Chromosome Res 21:643–651

    Article  CAS  PubMed  Google Scholar 

  • Seidl MF, Faino L, Shi-Kunne X, van den Berg GC, Bolton MD, Thomma BP (2015) The genome of the saprophytic fungus verticillium tricorpus reveals a complex effector repertoire resembling that of its pathogenic relatives. Mol Plant Microbe Interact 28:362–373

    Article  CAS  PubMed  Google Scholar 

  • Selker EU, Tountas NA, Cross SH, Margolin BS, Murphy JG, Bird AP, Freitag M (2003) The methylated component of the Neurospora crassa genome. Nature 422:893–897

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Wolf SE, Burke JM, Presting GG, Ross-Ibarra J, Dawe RK (2010) Widespread gene conversion in centromere cores. PLoS Biol 8:e1000327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, ODonnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    Article  PubMed  Google Scholar 

  • Steiner NC, Hahnenberger KM, Clarke L (1993) Centromeres of the fission yeast Schizosaccharomyces pombe are highly variable genetic loci. Mol Cell Biol 13:4578–4587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Studt L, Rosler SM, Burkhardt, Arndt B, Freitag M, Humpf HU, Dickschat JS, Tudzynski B (2016) Knock-down of the methyltransferase Kmt6 relieves H3K27me3 and results in induction of cryptic and otherwise silent secondary metabolite gene clusters in Fusarium fujikuroi. Environ Microbiol 18(11):4037–4054

    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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tanizawa H, Iwasaki O, Tanaka A, Capizzi JR, Wickramasinghe P, Lee M, Fu Z, Noma K (2010) Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation. Nucleic Acids Res 38:8164–8177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur J, Sanyal K (2013) Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res 23:638–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur J, Talbert PB, Henikoff S (2015) Inner kinetochore protein interactions with regional centromeres of fission yeast. Genetics 201:543–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma BP, Seidl MF, Shi-Kunne X, Cook DE, Bolton MD, van Kan JA, Faino L (2016) Mind the gap; seven reasons to close fragmented genome assemblies. Fungal Genet Biol 90:24–30

    Article  CAS  PubMed  Google Scholar 

  • Thon MR, Pan H, Diener S, Papalas J, Taro A, Mitchell TK, Dean RA (2006) The role of transposable element clusters in genome evolution and loss of synteny in the rice blast fungus Magnaporthe oryzae. Genome Biol 7:R16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verdaasdonk JS, Gardner R, Stephens AD, Yeh E, Bloom K (2012) Tension-dependent nucleosome remodeling at the pericentromere in yeast. Mol Biol Cell 23:2560–2570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernis L, Chasles M, Pasero P, Lepingle A, Gaillardin C, Fournier P (1999) Short DNA fragments without sequence similarity are initiation sites for replication in the chromosome of the yeast Yarrowia lipolytica. Mol Biol Cell 10:757–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernis L, Poljak L, Chasles M, Uchida K, Casaregola S, Kas E, Matsuoka M, Gaillardin C, Fournier P (2001) Only centromeres can supply the partition system required for ARS function in the yeast Yarrowia lipolytica. J Mol Biol 305:203–217

    Article  CAS  PubMed  Google Scholar 

  • Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA (2002) Regulation of heterochromatic silencing and histone h3 lysine-9 methylation by RNAi. Science 297:1833–1837

    Article  CAS  PubMed  Google Scholar 

  • Westhorpe FG, Fuller CJ, Straight AF (2015) A cell-free CENP-A assembly system defines the chromatin requirements for centromere maintenance. J Cell Biol 209:789–801

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Winey M, Mamay CL, OToole ET, Mastronarde DN, Giddings TH, McDonald JrKL, McIntosh JR (1995) Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle. J Cell Biol 129:1601–1615

    Article  CAS  PubMed  Google Scholar 

  • Zinkowski RP, Meyne J, Brinkley BR (1991) The centromere-kinetochore complex: a repeat subunit model. J Cell Biol 113:1091–1110

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Freitag .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Friedman, S., Freitag, M. (2017). Centrochromatin of Fungi. In: Black, B. (eds) Centromeres and Kinetochores. Progress in Molecular and Subcellular Biology, vol 56. Springer, Cham. https://doi.org/10.1007/978-3-319-58592-5_4

Download citation

Publish with us

Policies and ethics