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A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

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  • Authors: Allyson A. Erlendson1, Steven Friedman2, Michael Freitag3
  • Editors: Joseph Heitman4, Eva Holtgrewe Stukenbrock5
    Affiliations: 1: Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR 97331; 2: Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR 97331; 3: Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR 97331; 4: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 5: Environmental Genomics, Christian-Albrechts University of Kiel, Kiel, Germany, and Max Planck Institute for Evolutionary Biology, Plön, Germany
  • Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
  • Received 06 June 2017 Accepted 11 June 2017 Published 28 July 2017
  • Michael Freitag, freitagm@cgrb.oregonstate.edu
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  • Abstract:

    Chromatin and chromosomes of fungi are highly diverse and dynamic, even within species. Much of what we know about histone modification enzymes, RNA interference, DNA methylation, and cell cycle control was first addressed in , , , and . Here, we examine the three landmark regions that are required for maintenance of stable chromosomes and their faithful inheritance, namely, origins of DNA replication, telomeres and centromeres. We summarize the state of recent chromatin research that explains what is required for normal function of these specialized chromosomal regions in different fungi, with an emphasis on the silencing mechanism associated with subtelomeric regions, initiated by sirtuin histone deacetylases and histone H3 lysine 27 (H3K27) methyltransferases. We explore mechanisms for the appearance of “accessory” or “conditionally dispensable” chromosomes and contrast what has been learned from studies on genome-wide chromosome conformation capture in , , , and . While most of the current knowledge is based on work in a handful of genetically and biochemically tractable model organisms, we suggest where major knowledge gaps remain to be closed. Fungi will continue to serve as facile organisms to uncover the basic processes of life because they make excellent model organisms for genetics, biochemistry, cell biology, and evolutionary biology.

  • Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi. Microbiol Spectrum 5(4):FUNK-0054-2017. doi:10.1128/microbiolspec.FUNK-0054-2017.

Key Concept Ranking

Chromosome Structure
Chromosome Types
Sister Chromatids


1. Beadle GW, Tatum EL. 1941. Genetic control of biochemical reactions in Neurospora. Proc Natl Acad Sci USA 27:499–506 http://dx.doi.org/10.1073/pnas.27.11.499. [PubMed]
2. Allis CD. 2015. Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Brownell JE, Allis CD. 1995. An activity gel assay detects a single, catalytically active histone acetyltransferase subunit in Tetrahymena macronuclei. Proc Natl Acad Sci USA 92:6364–6368 http://dx.doi.org/10.1073/pnas.92.14.6364.
4. Grunstein M, Gasser SM. 2013. Epigenetics in Saccharomyces cerevisiae. Cold Spring Harb Perspect Biol 5:a017491 http://dx.doi.org/10.1101/cshperspect.a017491. [PubMed]
5. Allshire RC, Ekwall K. 2015. Epigenetic regulation of chromatin states in Schizosaccharomyces pombe. Cold Spring Harb Perspect Biol 7:a018770 http://dx.doi.org/10.1101/cshperspect.a018770. [PubMed]
6. Rando OJ, Winston F. 2012. Chromatin and transcription in yeast. Genetics 190:351–387 http://dx.doi.org/10.1534/genetics.111.132266. [PubMed]
7. 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. doi:10.1371/journal.pbio.1001369.
8. Goto DB, Nakayama J. 2012. RNA and epigenetic silencing: insight from fission yeast. Dev Growth Differ 54:129–141 http://dx.doi.org/10.1111/j.1440-169X.2011.01310.x. [PubMed]
9. Grewal SI. 2010. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20:134–141. doi:10.1016/j.gde.2010.02.003.
10. Gartenberg MR, Smith JS. 2016. The nuts and bolts of transcriptionally silent chromatin in Saccharomyces cerevisiae. Genetics 203:1563–1599 http://dx.doi.org/10.1534/genetics.112.145243. [PubMed]
11. Hickman MA, Froyd CA, Rusche LN. 2011. Reinventing heterochromatin in budding yeasts: Sir2 and the origin recognition complex take center stage. Eukaryot Cell 10:1183–1192. doi:10.1128/EC.05123-11.
12. Harr JC, Gonzalez-Sandoval A, Gasser SM. 2016. Histones and histone modifications in perinuclear chromatin anchoring: from yeast to man. EMBO Rep 17:139–155 http://dx.doi.org/10.15252/embr.201541809.
13. Mizuguchi T, Barrowman J, Grewal SI. 2015. Chromosome domain architecture and dynamic organization of the fission yeast genome. FEBS Lett 589(20 Pt A):2975–2986 http://dx.doi.org/10.1016/j.febslet.2015.06.008. [PubMed]
14. 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, O’Rourke 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 http://dx.doi.org/10.1128/MMBR.68.1.1-108.2004.
15. Aramayo R, Selker EU. 2013. Neurospora crassa, a model system for epigenetics research. Cold Spring Harb Perspect Biol 5:a017921. doi:10.1101/cshperspect.a017921.
16. Cuperlovic-Culf M, Culf AS. 2014. Role of histone deacetylases in fungal phytopathogenesis: a review. Int J Modern Bot 4:48–60 10.5923/j.ijmb.20140402.03.
17. Jeon J, Kwon S, Lee YH. 2014. Histone acetylation in fungal pathogens of plants. Plant Pathol J 30:1–9. 10.5423/PPJ.RW.01.2014.0003 [PubMed]
18. Smith KM, Phatale PA, Bredeweg EL, Connolly LR, Pomraning KR, Freitag M. 2012. Epigenetics of filamentous fungi, p 1063–1105. In Myers RA (ed), Epigenetic Regulation and Epigenomics. Wiley-VCH Verlag, Weinheim, Germany.
19. Rountree MR, Selker EU. 2010. DNA methylation and the formation of heterochromatin in Neurospora crassa. Heredity 105:38–44. 10.1038/hdy.2010.44. [PubMed]
20. Chang SS, Zhang Z, Liu Y. 2012. RNA interference pathways in fungi: mechanisms and functions. Annu Rev Microbiol 66:305–323 http://dx.doi.org/10.1146/annurev-micro-092611-150138. [PubMed]
21. Brosch G, Loidl P, Graessle S. 2008. Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol Rev 32:409–439. 10.1111/j.1574-6976.2007.00100.x. [PubMed]
22. Galazka JM, Freitag M. 2014. Variability of chromosome structure in pathogenic fungi: of “ends and odds.” Curr Opin Microbiol 20:19–26. 10.1016/j.mib.2014.04.002. [PubMed]
23. Wiles ET, Selker EU. 2017. H3K27 methylation: a promiscuous repressive chromatin mark. Curr Opin Genet Dev 43:31–37 http://dx.doi.org/10.1016/j.gde.2016.11.001. [PubMed]
24. Lewis ZA. 2017. Polycomb group systems in fungi: new models for understanding polycomb repressive complex 2. Trends Genet 33:220–231 http://dx.doi.org/10.1016/j.tig.2017.01.006.
25. Garnaud C, Champleboux M, Maubon D, Cornet M, Govin J. 2016. Histone deacetylases and their inhibition in Candida species. Front Microbiol 7:1238 http://dx.doi.org/10.3389/fmicb.2016.01238. [PubMed]
26. Schmoll M, Dattenböck C, Carreras-Villaseñor N, Mendoza-Mendoza A, Tisch D, Alemán MI, Baker SE, Brown C, Cervantes-Badillo MG, Cetz-Chel J, Cristobal-Mondragon GR, Delaye L, Esquivel-Naranjo EU, Frischmann A, Gallardo-Negrete JJ, García-Esquivel M, Gomez-Rodriguez EY, Greenwood DR, Hernández-Oñate M, Kruszewska JS, Lawry R, Mora-Montes HM, Muñoz-Centeno T, Nieto-Jacobo MF, Nogueira Lopez G, Olmedo-Monfil V, Osorio-Concepcion M, Piłsyk S, Pomraning KR, Rodriguez-Iglesias A, Rosales-Saavedra MT, Sánchez-Arreguín 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 http://dx.doi.org/10.1128/MMBR.00040-15.
27. Janicki SM, Tsukamoto T, Salghetti SE, Tansey WP, Sachidanandam R, Prasanth KV, Ried T, Shav-Tal Y, Bertrand E, Singer RH, Spector DL. 2004. From silencing to gene expression: real-time analysis in single cells. Cell 116:683–698 http://dx.doi.org/10.1016/S0092-8674(04)00171-0. [PubMed]
28. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293. 10.1126/science.1181369. [PubMed]
29. Freitag M. 2014. Fungal chromatin and its role in regulation of gene expression, p 99–120. In Nowrousian M (ed), Fungal Genomics. Springer, Heidelberg, Germany. http://dx.doi.org/10.1007/978-3-642-45218-5_5.
30. Mondo SJ, Dannebaum RO, Kuo RC, Louie KB, Bewick AJ, LaButti K, Haridas S, Kuo A, Salamov A, Ahrendt SR, Lau R, Bowen BP, Lipzen A, Sullivan W, Andreopoulos BB, Clum A, Lindquist E, Daum C, Northen TR, Kunde-Ramamoorthy G, Schmitz RJ, Gryganskyi A, Culley D, Magnuson J, James TY, O’Malley MA, Stajich JE, Spatafora JW, Visel A, Grigoriev IV. 2017. Widespread adenine N6-methylation of active genes in fungi. Nat Genet 49:964–968 http://dx.doi.org/10.1038/ng.3859.
31. Bell SP, Dutta A. 2002. DNA replication in eukaryotic cells. Annu Rev Biochem 71:333–374 http://dx.doi.org/10.1146/annurev.biochem.71.110601.135425. [PubMed]
32. Prioleau MN, MacAlpine DM. 2016. DNA replication origins: where do we begin? Genes Dev 30:1683–1697 http://dx.doi.org/10.1101/gad.285114.116.
33. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, Lockhart DJ, Davis RW, Brewer BJ, Fangman WL. 2001. Replication dynamics of the yeast genome. Science 294:115–121 http://dx.doi.org/10.1126/science.294.5540.115. [PubMed]
34. Wyrick JJ, Aparicio JG, Chen T, Barnett JD, Jennings EG, Young RA, Bell SP, Aparicio OM. 2001. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 294:2357–2360 http://dx.doi.org/10.1126/science.1066101.
35. Xu W, Aparicio JG, Aparicio OM, Tavaré S. 2006. Genome-wide mapping of ORC and Mcm2p binding sites on tiling arrays and identification of essential ARS consensus sequences in S. cerevisiae. BMC Genomics 7:276 http://dx.doi.org/10.1186/1471-2164-7-276.
36. Eaton ML, Galani K, Kang S, Bell SP, MacAlpine DM. 2010. Conserved nucleosome positioning defines replication origins. Genes Dev 24:748–753 http://dx.doi.org/10.1101/gad.1913210.
37. Segurado M, de Luis A, Antequera F. 2003. Genome-wide distribution of DNA replication origins at A+T-rich islands in Schizosaccharomyces pombe. EMBO Rep 4:1048–1053 http://dx.doi.org/10.1038/sj.embor.7400008.
38. Cvetic C, Walter JC. 2005. Eukaryotic origins of DNA replication: could you please be more specific? Semin Cell Dev Biol 16:343–353 http://dx.doi.org/10.1016/j.semcdb.2005.02.009. [PubMed]
39. Chuang RY, Kelly TJ. 1999. The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. Proc Natl Acad Sci USA 96:2656–2661 http://dx.doi.org/10.1073/pnas.96.6.2656.
40. Brewer BJ, Fangman WL. 1987. The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51:463–471 http://dx.doi.org/10.1016/0092-8674(87)90642-8. [PubMed]
41. Brewer BJ, Fangman WL. 1991. Mapping replication origins in yeast chromosomes. BioEssays 13:317–322 http://dx.doi.org/10.1002/bies.950130702.
42. Theis JF, Newlon CS. 1997. The ARS309 chromosomal replicator of Saccharomyces cerevisiae depends on an exceptional ARS consensus sequence. Proc Natl Acad Sci USA 94:10786–10791 http://dx.doi.org/10.1073/pnas.94.20.10786.
43. 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 http://dx.doi.org/10.1371/journal.pgen.1001068. (Errata, 7: 10.1371/annotation/2aba8d24-7a24-4bbc-91f7-9b9e228cc84d; 7: 10.1371/annotation/d4e8b4eb-2385-4a46-938e-19bbae4fcf89.)
44. Tsai HJ, Baller JA, Liachko I, Koren A, Burrack LS, Hickman MA, Thevandavakkam MA, Rusche LN, Berman J. 2014. Origin replication complex binding, nucleosome depletion patterns, and a primary sequence motif can predict origins of replication in a genome with epigenetic centromeres. MBio 5:e01703-14 http://dx.doi.org/10.1128/mBio.01703-14.
45. 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. 10.1371/journal.pgen.1004261 [PubMed]
46. Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I, Sionov E, Falk R, Parnmen S, Lumbsch HT, Boekhout T. 2015. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol 78:16–48 http://dx.doi.org/10.1016/j.fgb.2015.02.009.
47. Paietta J, Marzluf GA. 1985. Plasmid recovery from transformants and the isolation of chromosomal DNA segments improving plasmid replication in Neurospora crassa. Curr Genet 9:383–388 http://dx.doi.org/10.1007/BF00421609.
48. Powell WA, Kistler HC. 1990. In vivo rearrangement of foreign DNA by Fusarium oxysporum produces linear self-replicating plasmids. J Bacteriol 172:3163–3171 http://dx.doi.org/10.1128/jb.172.6.3163-3171.1990.
49. Aleksenko A, Gems D, Clutterbuck J. 1996. Multiple copies of MATE elements support autonomous plasmid replication in Aspergillus nidulans. Mol Microbiol 20:427–434 http://dx.doi.org/10.1111/j.1365-2958.1996.tb02629.x.
50. Aleksenko A, Clutterbuck AJ. 1996. The plasmid replicator AMA1 in Aspergillus nidulans is an inverted duplication of a low-copy-number dispersed genomic repeat. Mol Microbiol 19:565–574 http://dx.doi.org/10.1046/j.1365-2958.1996.400937.x.
51. Garcia-Pedrajas MD, Roncero MI. 1996. A homologous and self-replicating system for efficient transformation of Fusarium oxysporum. Curr Genet 29:191–198 http://dx.doi.org/10.1007/BF02221584.
52. Kusakabe T, Sugimoto Y, Hirota Y, Toné S, Kawaguchi Y, Koga K, Ohyama T. 2000. Isolation of replicational cue elements from a library of bent DNAs of Aspergillus oryzae. Mol Biol Rep 27:13–19 http://dx.doi.org/10.1023/A:1007076511814.
53. Bok JW, Ye R, Clevenger KD, Mead D, Wagner M, Krerowicz A, Albright JC, Goering AW, Thomas PM, Kelleher NL, Keller NP, Wu CC. 2015. Fungal artificial chromosomes for mining of the fungal secondary metabolome. BMC Genomics 16:343. 10.1186/s12864-015-1561-x. [PubMed]
54. Woods JP, Goldman WE. 1993. Autonomous replication of foreign DNA in Histoplasma capsulatum: role of native telomeric sequences. J Bacteriol 175:636–641 http://dx.doi.org/10.1128/jb.175.3.636-641.1993.
55. Varma A, Kwon-Chung KJ. 1998. Construction of stable episomes in Cryptococcus neoformans. Curr Genet 34:60–66 http://dx.doi.org/10.1007/s002940050366.
56. Takahashi S, Nakajima Y, Imaizumi T, Furuta Y, Ohshiro Y, Abe K, Yamada RH, Kera Y. 2011. Development of an autonomously replicating linear vector of the yeast Cryptococcus humicola by using telomere-like sequence repeats. Appl Microbiol Biotechnol 89:1213–1221 http://dx.doi.org/10.1007/s00253-010-2985-5.
57. Blackburn EH, Gall JG. 1978. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120:33–53 http://dx.doi.org/10.1016/0022-2836(78)90294-2.
58. Allshire RC, Dempster M, Hastie ND. 1989. Human telomeres contain at least three types of G-rich repeat distributed non-randomly. Nucleic Acids Res 17:4611–4627 http://dx.doi.org/10.1093/nar/17.12.4611.
59. Kusumoto KI, Suzuki S, Kashiwagi Y. 2003. Telomeric repeat sequence of Aspergillus oryzae consists of dodeca-nucleotides. Appl Microbiol Biotechnol 61:247–251 http://dx.doi.org/10.1007/s00253-002-1193-3.
60. Wang N, Rizvydeen S, Vahedi M, Vargas Gonzalez DM, Allred AL, Perry DW, Mirabito PM, Kirk KE. 2014. Novel telomere-anchored PCR approach for studying sexual stage telomeres in Aspergillus nidulans. PLoS One 9:e99491. 10.1371/journal.pone.0099491.
61. Wu C, Kim YS, Smith KM, Li W, Hood HM, Staben C, Selker EU, Sachs MS, Farman ML. 2009. Characterization of chromosome ends in the filamentous fungus Neurospora crassa. Genetics 181:1129–1145 http://dx.doi.org/10.1534/genetics.107.084392. [PubMed]
62. 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. 10.1186/s13072-015-0033-5.
63. Szostak JW, Blackburn EH. 1982. Cloning yeast telomeres on linear plasmid vectors. Cell 29:245–255 http://dx.doi.org/10.1016/0092-8674(82)90109-X.
64. Larrivée M, LeBel C, Wellinger RJ. 2004. The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev 18:1391–1396 http://dx.doi.org/10.1101/gad.1199404.
65. McEachern MJ, Blackburn EH. 1994. A conserved sequence motif within the exceptionally diverse telomeric sequences of budding yeasts. Proc Natl Acad Sci USA 91:3453–3457 http://dx.doi.org/10.1073/pnas.91.8.3453.
66. McEachern MJ, Hicks JB. 1993. Unusually large telomeric repeats in the yeast Candida albicans. Mol Cell Biol 13:551–560 http://dx.doi.org/10.1128/MCB.13.1.551.
67. Fujita I, Tanaka M, Kanoh J. 2012. Identification of the functional domains of the telomere protein Rap1 in Schizosaccharomyces pombe. PLoS One 7:e49151 http://dx.doi.org/10.1371/journal.pone.0049151.
68. Sepsiova R, Necasova I, Willcox S, Prochazkova K, Gorilak P, Nosek J, Hofr C, Griffith JD, Tomaska L. 2016. Evolution of telomeres in Schizosaccharomyces pombe and its possible relationship to the diversification of telomere binding proteins. PLoS One 11:e0154225 http://dx.doi.org/10.1371/journal.pone.0154225.
69. Underwood AP, Louis EJ, Borts RH, Wakefield AE. 1994. A technique for cloning the telomeres and subtelomeric regions from Pneumocystis carinii. J Eukaryot Microbiol 41:113S. [PubMed]
70. Underwood AP, Louis EJ, Borts RH, Stringer JR, Wakefield AE. 1996. Pneumocystis carinii telomere repeats are composed of TTAGGG and the subtelomeric sequence contains a gene encoding the major surface glycoprotein. Mol Microbiol 19:273–281 http://dx.doi.org/10.1046/j.1365-2958.1996.374904.x.
71. Schechtman MG. 1987. Isolation of telomere DNA from Neurospora crassa. Mol Cell Biol 7:3168–3177 http://dx.doi.org/10.1128/MCB.7.9.3168.
72. Schechtman MG. 1990. Characterization of telomere DNA from Neurospora crassa. Gene 88:159–165 http://dx.doi.org/10.1016/0378-1119(90)90027-O.
73. Connelly JC, Arst HN Jr. 1991. Identification of a telomeric fragment from the right arm of chromosome III of Aspergillus nidulans. FEMS Microbiol Lett 80:295–297 http://dx.doi.org/10.1111/j.1574-6968.1991.tb04678.x. [PubMed]
74. Bhattacharyya A, Blackburn EH. 1997. Aspergillus nidulans maintains short telomeres throughout development. Nucleic Acids Res 25:1426–31. [PubMed]
75. Tang X, Zhao L, Chen H, Chen YQ, Chen W, Song Y, Ratledge C. 2015. Complete genome sequence of a high lipid-producing strain of Mucor circinelloides WJ11 and comparative genome analysis with a low lipid-producing strain CBS 277.49. PLoS One 10:e0137543 http://dx.doi.org/10.1371/journal.pone.0137543.
76. Armstrong CA, Tomita K. 2017. Fundamental mechanisms of telomerase action in yeasts and mammals: understanding telomeres and telomerase in cancer cells. Open Biol 7:160338 http://dx.doi.org/10.1098/rsob.160338.
77. Yu EY. 2012. Telomeres and telomerase in Candida albicans. Mycoses 55:e48–e59 http://dx.doi.org/10.1111/j.1439-0507.2011.02123.x.
78. Rice C, Skordalakes E. 2016. Structure and function of the telomeric CST complex. Comput Struct Biotechnol J 14:161–167 http://dx.doi.org/10.1016/j.csbj.2016.04.002. [PubMed]
79. Kanoh J, Ishikawa F. 2001. spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr Biol 11:1624–1630 http://dx.doi.org/10.1016/S0960-9822(01)00503-6.
80. Miller KM, Ferreira MG, Cooper JP. 2005. Taz1, Rap1 and Rif1 act both interdependently and independently to maintain telomeres. EMBO J 24:3128–3135 http://dx.doi.org/10.1038/sj.emboj.7600779. [PubMed]
81. Kibe T, Ono Y, Sato K, Ueno M. 2007. Fission yeast Taz1 and RPA are synergistically required to prevent rapid telomere loss. Mol Biol Cell 18:2378–2387 http://dx.doi.org/10.1091/mbc.E06-12-1084.
82. Price CM, Boltz KA, Chaiken MF, Stewart JA, Beilstein MA, Shippen DE. 2010. Evolution of CST function in telomere maintenance. Cell Cycle 9:3157–3165. 10.4161/cc.9.16.12547. [PubMed]
83. Kothe GO, Kitamura M, Masutani M, Selker EU, Inoue H. 2010. PARP is involved in replicative aging in Neurospora crassa. Fungal Genet Biol 47:297–309 http://dx.doi.org/10.1016/j.fgb.2009.12.012. [PubMed]
84. Ellahi A, Thurtle DM, Rine J. 2015. The Chromatin and transcriptional landscape of native Saccharomyces cerevisiae telomeres and subtelomeric domains. Genetics 200:505–521 http://dx.doi.org/10.1534/genetics.115.175711.
85. 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 http://dx.doi.org/10.1016/0092-8674(90)90141-Z.
86. Duan YM, Zhou BO, Peng J, Tong XJ, Zhang QD, Zhou JQ. 2016. Molecular dynamics of de novo telomere heterochromatin formation in budding yeast. J Genet Genomics 43:451–465 http://dx.doi.org/10.1016/j.jgg.2016.03.009.
87. Gottschling DE. 2000. Gene silencing: two faces of SIR2. Curr Biol 10:R708–R711 http://dx.doi.org/10.1016/S0960-9822(00)00714-4.
88. Hoppe GJ, Tanny JC, Rudner AD, Gerber SA, Danaie S, Gygi SP, Moazed D. 2002. Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation. Mol Cell Biol 22:4167–4180 http://dx.doi.org/10.1128/MCB.22.12.4167-4180.2002.
89. Rusche LN, Kirchmaier AL, Rine J. 2003. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72:481–516 http://dx.doi.org/10.1146/annurev.biochem.72.121801.161547.
90. Katan-Khaykovich Y, Struhl K. 2005. Heterochromatin formation involves changes in histone modifications over multiple cell generations. EMBO J 24:2138–2149 http://dx.doi.org/10.1038/sj.emboj.7600692.
91. Osborne EA, Dudoit S, Rine J. 2009. The establishment of gene silencing at single-cell resolution. Nat Genet 41:800–806 http://dx.doi.org/10.1038/ng.402.
92. Hernández-Rivas R, Herrera-Solorio AM, Sierra-Miranda M, Delgadillo DM, Vargas M. 2013. Impact of chromosome ends on the biology and virulence of Plasmodium falciparum. Mol Biochem Parasitol 187:121–128 http://dx.doi.org/10.1016/j.molbiopara.2013.01.003.
93. De Las Penas A, Pan SJ, Castano I, Alder J, Cregg R, Cormack BP. 2003. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev 17:2245–2258. 10.1101/gad.1121003. [PubMed]
94. Castaño I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP. 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol Microbiol 55:1246–1258 http://dx.doi.org/10.1111/j.1365-2958.2004.04465.x.
95. Domergue R, Castaño I, De Las Peñas A, Zupancic M, Lockatell V, Hebel JR, Johnson D, Cormack BP. 2005. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308:866–870 http://dx.doi.org/10.1126/science.1108640.
96. Rosas-Hernandez LL, Juarez-Reyes A, Arroyo-Helguera OE, De Las Penas A, Pan SJ, Cormack BP, Castano I. 2008. yKu70/yKu80 and Rif1 regulate silencing differentially at telomeres in Candida glabrata. Eukaryot Cell 7:2168–2178. 10.1128/EC.00228-08. [PubMed]
97. van het Hoog M, Rast TJ, Martchenko M, Grindle S, Dignard D, Hogues H, Cuomo C, Berriman M, Scherer S, Magee BB, Whiteway M, Chibana H, Nantel A, Magee PT. 2007. Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol 8:R52 http://dx.doi.org/10.1186/gb-2007-8-4-r52.
98. Anderson MZ, Baller JA, Dulmage K, Wigen L, Berman J. 2012. The three clades of the telomere-associated TLO gene family of Candida albicans have different splicing, localization, and expression features. Eukaryot Cell 11:1268–1275 http://dx.doi.org/10.1128/EC.00230-12.
99. Haran J, Boyle H, Hokamp K, Yeomans T, Liu Z, Church M, Fleming AB, Anderson MZ, Berman J, Myers LC, Sullivan DJ, Moran GP. 2014. Telomeric ORFs (TLOs) in Candida spp. encode mediator subunits that regulate distinct virulence traits. PLoS Genet 10:e1004658 http://dx.doi.org/10.1371/journal.pgen.1004658.
100. Zhang A, Petrov KO, Hyun ER, Liu Z, Gerber SA, Myers LC. 2012. The Tlo proteins are stoichiometric components of Candida albicans mediator anchored via the Med3 subunit. Eukaryot Cell 11:874–884 http://dx.doi.org/10.1128/EC.00095-12.
101. Liu Z, Moran GP, Sullivan DJ, MacCallum DM, Myers LC. 2016. Amplification of TLO mediator subunit genes facilitate filamentous growth in Candida spp. PLoS Genet 12:e1006373 http://dx.doi.org/10.1371/journal.pgen.1006373.
102. Anderson MZ, Wigen LJ, Burrack LS, Berman J. 2015. Real-time evolution of a subtelomeric gene family in Candida albicans. Genetics 200:907–919 http://dx.doi.org/10.1534/genetics.115.177451. [PubMed]
103. Pérez-Martín J, Uría JA, Johnson AD. 1999. Phenotypic switching in Candida albicans is controlled by a SIR2 gene. EMBO J 18:2580–2592 http://dx.doi.org/10.1093/emboj/18.9.2580.
104. Freire-Benéitez V, Gourlay S, Berman J, Buscaino A. 2016. Sir2 regulates stability of repetitive domains differentially in the human fungal pathogen Candida albicans. Nucleic Acids Res 44:9166–9179 10.1093/nar/gkw594.
105. Freeman-Cook LL, Gómez EB, Spedale EJ, Marlett J, Forsburg SL, Pillus L, Laurenson P. 2005. Conserved locus-specific silencing functions of Schizosaccharomyces pombe sir2+. Genetics 169:1243–1260 http://dx.doi.org/10.1534/genetics.104.032714.
106. Shankaranarayana GD, Motamedi MR, Moazed D, Grewal SI. 2003. Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast. Curr Biol 13:1240–1246 http://dx.doi.org/10.1016/S0960-9822(03)00489-5.
107. Freeman-Cook LL, Sherman JM, Brachmann CB, Allshire RC, Boeke JD, Pillus L. 1999. The Schizosaccharomyces pombe hst4(+) gene is a SIR2 homologue with silencing and centromeric functions. Mol Biol Cell 10:3171–3186 http://dx.doi.org/10.1091/mbc.10.10.3171.
108. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110–113 http://dx.doi.org/10.1126/science.1060118. [PubMed]
109. 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 http://dx.doi.org/10.1126/science.1074973.
110. 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 http://dx.doi.org/10.1038/ng1602.
111. Kanoh J, Sadaie M, Urano T, Ishikawa F. 2005. Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr Biol 15:1808–1819 http://dx.doi.org/10.1016/j.cub.2005.09.041.
112. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, Kobayashi R, Grewal SI. 2007. SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128:491–504. 10.1016/j.cell.2006.12.035 [PubMed]
113. Sugioka-Sugiyama R, Sugiyama T. 2011. Sde2: a novel nuclear protein essential for telomeric silencing and genomic stability in Schizosaccharomyces pombe. Biochem Biophys Res Commun 406:444–448 http://dx.doi.org/10.1016/j.bbrc.2011.02.068.
114. Zofall M, Smith DR, Mizuguchi T, Dhakshnamoorthy J, Grewal SI. 2016. Taz1-shelterin promotes facultative heterochromatin assembly at chromosome-internal sites containing late replication origins. Mol Cell 62:862–874 http://dx.doi.org/10.1016/j.molcel.2016.04.034.
115. Mizuguchi T, Taneja N, Matsuda E, Belton JM, FitzGerald P, Dekker J, Grewal SIS. 2017. Shelterin components mediate genome reorganization in response to replication stress. Proc Natl Acad Sci USA 114:5479–5484 http://dx.doi.org/10.1073/pnas.1705527114.
116. Matsuda A, Chikashige Y, Ding DQ, Ohtsuki C, Mori C, Asakawa H, Kimura H, Haraguchi T, Hiraoka Y. 2015. Highly condensed chromatins are formed adjacent to subtelomeric and decondensed silent chromatin in fission yeast. Nat Commun 6:7753 http://dx.doi.org/10.1038/ncomms8753.
117. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581–592. 10.1016/j.cell.2005.10.023. [PubMed]
118. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ. 2005. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593–605 http://dx.doi.org/10.1016/j.cell.2005.10.025. [PubMed]
119. Rehmeyer C, Li W, Kusaba M, Kim YS, Brown D, Staben C, Dean R, Farman M. 2006. Organization of chromosome ends in the rice blast fungus, Magnaporthe oryzae. Nucleic Acids Res 34:4685–4701. 10.1093/nar/gkl588 [PubMed]
120. Starnes JH, Thornbury DW, Novikova OS, Rehmeyer CJ, Farman ML. 2012. Telomere-targeted retrotransposons in the rice blast fungus Magnaporthe oryzae: agents of telomere instability. Genetics 191:389–406 http://dx.doi.org/10.1534/genetics.111.137950.
121. Wiemann P, Keller NP. 2014. Strategies for mining fungal natural products. J Ind Microbiol Biotechnol 41:301–313 http://dx.doi.org/10.1007/s10295-013-1366-3.
122. 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. 10.1371/journal.ppat.1003475. [PubMed]
123. Zhao C, Waalwijk C, de Wit PJ, Tang D, van der Lee T. 2014. Relocation of genes generates non-conserved chromosomal segments in Fusarium graminearum that show distinct and co-regulated gene expression patterns. BMC Genomics 15:191. 10.1186/1471-2164-15-191.
124. Goodwin SB, M’Barek S B, 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. 10.1371/journal.pgen.1002070. [PubMed]
125. 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 http://dx.doi.org/10.1016/j.fgb.2015.08.010.
126. Faino L, Seidl MF, Shi-Kunne X, Pauper M, van den Berg GC, Wittenberg AH, Thomma BP. 2016. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res 26:1091–1100 http://dx.doi.org/10.1101/gr.204974.116.
127. 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 http://dx.doi.org/10.1094/MPMI-06-14-0173-R. [PubMed]
128. de Jonge R, Bolton MD, Kombrink A, van den Berg GC, Yadeta KA, Thomma BP. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res 23:1271–1282 http://dx.doi.org/10.1101/gr.152660.112.
129. 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 USA 113:15048–15053 http://dx.doi.org/10.1073/pnas.1615546113.
130. 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. 10.1101/gr.194555.115. [PubMed]
131. 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 http://dx.doi.org/10.1101/gr.203182.115.
132. 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. 10.1371/journal.pgen.1005083.
133. 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 USA 112:E6339—E6348. 10.1073/pnas.1511377112. [PubMed]
134. 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 USA 110:6027–6032. 10.1073/pnas.1303750110. [PubMed]
135. 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. doi:genetics.110.123315 (pii) 10.1534/genetics.110.123315. [PubMed]
136. Lewis ZA, Honda S, Khlafallah TK, Jeffress JK, Freitag M, Mohn F, Schübeler D, Selker EU. 2009. Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res 19:427–437 http://dx.doi.org/10.1101/gr.086231.108.
137. 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 http://dx.doi.org/10.1186/1756-8935-1-5.
138. Margueron R, Reinberg D. 2011. The polycomb complex PRC2 and its mark in life. Nature 469:343–349. 10.1038/nature09784 [PubMed]
139. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220. 10.1038/nrg2719. [PubMed]
140. Lewis EB. 1978. A gene complex controlling segmentation in Drosophila. Nature 276:565–570 http://dx.doi.org/10.1038/276565a0.
141. 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. 10.1016/j.cell.2014.11.039. [PubMed]
142. Jiao L, Liu X. 2016. Structural analysis of an active fungal PRC2. Nucleus 7:284–291 http://dx.doi.org/10.1080/19491034.2016.1183849.
143. Jiao L, Liu X. 2015. Structural basis of histone H3K27 trimethylation by an active polycomb repressive complex 2. Science 350:aac4383. 10.1126/science.aac4383.
144. Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ. 2009. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461:762–767. 10.1038/nature08398. [PubMed]
145. 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 http://dx.doi.org/10.1371/journal.pgen.1003916.
146. Studt L, Rösler SM, Burkhardt I, 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 18:4037–4054 http://dx.doi.org/10.1111/1462-2920.13427.
147. Chujo T, Scott B. 2014. Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte-plant symbiosis. Mol Microbiol 92:413–434 http://dx.doi.org/10.1111/mmi.12567.
148. Soyer JL, El Ghalid M, Glaser N, Ollivier B, Linglin J, Grandaubert J, Balesdent MH, Connolly LR, Freitag M, Rouxel T, Fudal I. 2014. Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genet 10:e1004227. 10.1371/journal.pgen.1004227.
149. Gacek-Matthews A, Berger H, Sasaki T, Wittstein K, Gruber C, Lewis ZA, Strauss J. 2016. KdmB, a jumonji histone H3 demethylase, regulates genome-wide H3K4 trimethylation and is required for normal induction of secondary metabolism in Aspergillus nidulans. PLoS Genet 12:e1006222. 10.1371/journal.pgen.1006222. [PubMed]
150. Studt L, Schmidt FJ, Jahn L, Sieber CM, Connolly LR, Niehaus EM, Freitag M, Humpf HU, Tudzynski B. 2013. Two histone deacetylases, FfHda1 and FfHda2, are important for Fusarium fujikuroi secondary metabolism and virulence. Appl Environ Microbiol 79:7719–7734. 10.1128/AEM.01557-13. [PubMed]
151. Cuomo CA, Güldener 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, Münsterkötter 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 http://dx.doi.org/10.1126/science.1143708.
152. Gale LR, Bryant JD, Calvo S, Giese H, Katan T, O’Donnell K, Suga H, Taga M, Usgaard TR, Ward TJ, Kistler HC. 2005. Chromosome complement of the fungal plant pathogen Fusarium graminearum based on genetic and physical mapping and cytological observations. Genetics 171:985–1001 http://dx.doi.org/10.1534/genetics.105.044842.
153. Laurent B, Palaiokostas C, Spataro C, Moinard M, Zehraoui E, Houston RD, Foulongne-Oriol M. 2016. High-resolution mapping of the recombination landscape of the phytopathogen Fusarium graminearum suggests two-speed genome evolution. Mol Plant Pathol 10.1111/mpp.12524.
154. Cleveland DW, Mao Y, Sullivan KF. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407–421 http://dx.doi.org/10.1016/S0092-8674(03)00115-6.
155. 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 http://dx.doi.org/10.1007/s10577-015-9470-z.
156. Freitag M. 2016. The kinetochore interaction network (KIN) of ascomycetes. Mycologia 108:485–505 http://dx.doi.org/10.3852/15-182.
157. Fukagawa T, Earnshaw WC. 2014. The centromere: chromatin foundation for the kinetochore machinery. Dev Cell 30:496–508. 10.1016/j.devcel.2014.08.016 [PubMed]
158. 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 http://dx.doi.org/10.1128/MCB.13.8.4578.
159. Thakur J, Talbert PB, Henikoff S. 2015. Inner kinetochore protein interactions with regional centromeres of fission yeast. Genetics 201:543–561. 10.1534/genetics.115.179788. [PubMed]
160. Clarke L. 1998. Centromeres: proteins, protein complexes, and repeated domains at centromeres of simple eukaryotes. Curr Opin Genet Dev 8:212–218.
161. 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. 10.1126/science.1203357. [PubMed]
162. Folco HD, Pidoux AL, Urano T, Allshire RC. 2008. Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:94–97 http://dx.doi.org/10.1126/science.1150944.
163. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC. 2001. Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542 http://dx.doi.org/10.1126/science.1064027.
164. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI. 2002. Establishment and maintenance of a heterochromatin domain. Science 297:2232–2237 http://dx.doi.org/10.1126/science.1076466.
165. Du Y, Topp CN, Dawe RK. 2010. DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 6:e1000835 http://dx.doi.org/10.1371/journal.pgen.1000835.
166. Rošić 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 http://dx.doi.org/10.1007/s00018-015-2124-7. [PubMed]
167. Clarke L, Carbon J. 1980. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504–509 http://dx.doi.org/10.1038/287504a0.
168. Clarke L, Carbon J. 1985. The structure and function of yeast centromeres. Annu Rev Genet 19:29–55 http://dx.doi.org/10.1146/annurev.ge.19.120185.000333. [PubMed]
169. Biggins S. 2013. The composition, functions, and regulation of the budding yeast kinetochore. Genetics 194:817–846 http://dx.doi.org/10.1534/genetics.112.145276.
170. Gordon JL, Byrne KP, Wolfe KH. 2011. Mechanisms of chromosome number evolution in yeast. PLoS Genet 7:e1002190 http://dx.doi.org/10.1371/journal.pgen.1002190.
171. Malik HS, Henikoff S. 2009. Major evolutionary transitions in centromere complexity. Cell 138:1067–1082. 10.1016/j.cell.2009.08.036. [PubMed]
172. 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 USA 101:11374–11379 http://dx.doi.org/10.1073/pnas.0404318101.
173. 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 http://dx.doi.org/10.1371/journal.pgen.1005839.
174. 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 USA 105:19797–19802. 10.1073/pnas.0809770105. [PubMed]
175. 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 http://dx.doi.org/10.1083/jcb.200803027.
176. 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. 10.1016/j.cub.2011.04.002 [PubMed]
177. 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 http://dx.doi.org/10.1128/MCB.18.9.5465.
178. Centola M, Carbon J. 1994. Cloning and characterization of centromeric DNA from Neurospora crassa. Mol Cell Biol 14:1510–1519 http://dx.doi.org/10.1128/MCB.14.2.1510.
179. Galagan JE, et al. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868 http://dx.doi.org/10.1038/nature01554.
180. Selker EU. 1990. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 24:579–613 http://dx.doi.org/10.1146/annurev.ge.24.120190.003051. [PubMed]
181. 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 http://dx.doi.org/10.1371/journal.pgen.1006015.
182. 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. 10.1128/MCB.01285-10 [PubMed]
183. 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 http://dx.doi.org/10.1038/nature01564.
184. 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. 10.1128/EC.00016-11 [PubMed]
185. 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 http://dx.doi.org/10.1186/gb-2006-7-2-r16.
186. 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:e00936-15 http://dx.doi.org/10.1128/mBio.00936-15.
187. 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 http://dx.doi.org/10.1006/fgbi.2001.1251.
188. 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 http://dx.doi.org/10.1371/journal.pgen.1000046.
189. Loftus BJ, et al. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321–1324 http://dx.doi.org/10.1126/science.1103773.
190. 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 http://dx.doi.org/10.1139/g04-099.
191. Kämper J, et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101 http://dx.doi.org/10.1038/nature05248.
192. 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. 10.1016/j.mycres.2007.03.004. [PubMed]
193. Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell 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 http://dx.doi.org/10.3852/16-042.
194. Marie-Nelly H, Marbouty M, Cournac A, Flot JF, Liti G, Parodi DP, Syan S, Guillén N, Margeot A, Zimmer C, Koszul R. 2014. High-quality genome (re)assembly using chromosomal contact data. Nat Commun 5:5695 http://dx.doi.org/10.1038/ncomms6695.
195. Malik HS, Henikoff S. 2002. Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev 12:711–718 http://dx.doi.org/10.1016/S0959-437X(02)00351-9.
196. Henikoff S, Ahmad K, Malik HS. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102 http://dx.doi.org/10.1126/science.1062939.
197. Earnshaw WC, Rothfield N. 1985. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321 http://dx.doi.org/10.1007/BF00328227.
198. 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 http://dx.doi.org/10.1083/jcb.104.4.805. [PubMed]
199. Palmer DK, O’Day 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 USA 88:3734–3738 http://dx.doi.org/10.1073/pnas.88.9.3734.
200. 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 USA 103:4186–4191 http://dx.doi.org/10.1073/pnas.0507947103. (Erratum, doi:10.1073/pnas.0507947103.)
201. 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 http://dx.doi.org/10.1038/nsmb845.
202. 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. 10.1016/j.cub.2014.11.060. [PubMed]
203. Baker RE, Rogers K. 2006. Phylogenetic analysis of fungal centromere H3 proteins. Genetics 174:1481–1492 http://dx.doi.org/10.1534/genetics.106.062794. [PubMed]
204. 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. 10.1083/jcb.201503132. [PubMed]
205. Carroll CW, Milks KJ, Straight AF. 2010. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J Cell Biol 189:1143–1155. 10.1083/jcb.201001013. [PubMed]
206. 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. 10.1038/ncb2805. [PubMed]
207. 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. 10.1101/gad.259432.115. [PubMed]
208. 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]
209. Burrack LS, Berman J. 2012. Neocentromeres and epigenetically inherited features of centromeres. Chromosome Res 20:607–619 http://dx.doi.org/10.1007/s10577-012-9296-x.
210. 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 http://dx.doi.org/10.1371/journal.pgen.1006317.
211. 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 http://dx.doi.org/10.1371/journal.pgen.1000400.
212. 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. 10.1101/gr.141614.112. [PubMed]
213. Pidoux AL, Allshire RC. 2005. The role of heterochromatin in centromere function. Philos Trans R Soc Lond B Biol Sci 360:569–579 http://dx.doi.org/10.1098/rstb.2004.1611.
214. 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 516:432–435 10.1038/nature13833.
215. 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 http://dx.doi.org/10.1038/ncb739.
216. Smith KM, Galazka JM, Phatale PA, Connolly LR, Freitag M. 2012. Centromeres of filamentous fungi. Chromosome Res 20:635–656 http://dx.doi.org/10.1007/s10577-012-9290-3.
217. Freitag M, Hickey PC, Khlafallah TK, Read ND, Selker EU. 2004. HP1 is essential for DNA methylation in neurospora. Mol Cell 13:427–434 http://dx.doi.org/10.1016/S1097-2765(04)00024-3.
218. Tamaru H, Selker EU. 2001. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277–283 http://dx.doi.org/10.1038/35104508. [PubMed]
219. Freitag M, Lee DW, Kothe GO, Pratt RJ, Aramayo R, Selker EU. 2004. DNA methylation is independent of RNA interference in Neurospora. Science 304:1939 http://dx.doi.org/10.1126/science.1099709.
220. Burt A, Trivers R. 2006. Genes in Conflict. Belknap Press of Harvard University, Cambridge, MA. http://dx.doi.org/10.4159/9780674029118.
221. 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. 10.1038/nature08850. [PubMed]
222. Rep M, Kistler HC. 2010. The genomic organization of plant pathogenicity in Fusarium species. Curr Opin Plant Biol 13:420–426. 10.1016/j.pbi.2010.04.004. [PubMed]
223. Wittenberg AH, van der Lee TA, Ben M’barek S, Ware SB, Goodwin SB, Kilian A, Visser RG, Kema GH, Schouten HJ. 2009. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4:e5863 http://dx.doi.org/10.1371/journal.pone.0005863.
224. Miao VP, Covert SF, VanEtten HD. 1991. A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254:1773–1776 http://dx.doi.org/10.1126/science.1763326.
225. 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, Molnár 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 http://dx.doi.org/10.1371/journal.pgen.1000618.
226. 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. 10.1371/journal.pgen.1003567.
227. Jones RN. 1995. B chromosomes in plants. New Phytol 131:411–434 http://dx.doi.org/10.1111/j.1469-8137.1995.tb03079.x.
228. Camacho JPM. 2005. B chromosomes, p 223–286. In Gregory TR (ed), The Evolution of the Genome. Elsevier, Amsterdam, The Netherlands. http://dx.doi.org/10.1016/B978-012301463-4/50006-1.
229. Grandaubert J, Bhattacharyya A, Stukenbrock EH. 2015. RNA-seq based gene annotation and comparative genomics of four fungal grass pathogens in the genus Zymoseptoria identify novel orphan genes and species-specific invasions of transposable elements. G3 (Bethesda) 5:1323–1333. 10.1534/g3.115.017731. [PubMed]
230. Banaei-Moghaddam AM, Martis MM, Macas J, Gundlach H, Himmelbach A, Altschmied L, Mayer KF, Houben A. 2015. Genes on B chromosomes: old questions revisited with new tools. Biochim Biophys Acta 1849:64–70. 10.1016/j.bbagrm.2014.11.007. [PubMed]
231. Jin W, Lamb JC, Zhang W, Kolano B, Birchler JA, Jiang J. 2008. Histone modifications associated with both A and B chromosomes of maize. Chromosome Res 16:1203–1214 http://dx.doi.org/10.1007/s10577-008-1269-8.
232. Ma LJ. 2014. Horizontal chromosome transfer and rational strategies to manage Fusarium vascular wilt diseases. Mol Plant Pathol 15:763–766 http://dx.doi.org/10.1111/mpp.12171.
233. Ma LJ, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K. 2013. Fusarium pathogenomics. Annu Rev Microbiol 67:399–416 http://dx.doi.org/10.1146/annurev-micro-092412-155650. [PubMed]
234. Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M’barek S, Gohari AM, Jashni MK, Stergiopoulos I, Kema GH, de Wit PJ. 2011. Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 35:542–554 http://dx.doi.org/10.1111/j.1574-6976.2010.00263.x. [PubMed]
235. Akagi Y, Akamatsu H, Otani H, Kodama M. 2009. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738 http://dx.doi.org/10.1128/EC.00135-09.
236. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956 http://dx.doi.org/10.1038/ng1839.
237. Hu J, Chen C, Peever T, Dang H, Lawrence C, Mitchell T. 2012. Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genomics 13:171. 10.1186/1471-2164-13-171.
238. Vlaardingerbroek I, Beerens B, Schmidt SM, Cornelissen BJ, Rep M. 2016. Dispensable chromosomes in Fusarium oxysporum f. sp. lycopersici. Mol Plant Pathol 17:1455–1466 http://dx.doi.org/10.1111/mpp.12440. [PubMed]
239. Vlaardingerbroek I, Beerens B, Rose L, Fokkens L, Cornelissen BJ, Rep M. 2016. Exchange of core chromosomes and horizontal transfer of lineage-specific chromosomes in Fusarium oxysporum. Environ Microbiol 18:3702–3713 http://dx.doi.org/10.1111/1462-2920.13281.
240. van der Does HC, Fokkens L, Yang A, Schmidt SM, Langereis L, Lukasiewicz JM, Hughes TR, Rep M. 2016. Transcription factors encoded on core and accessory chromosomes of Fusarium oxysporum induce expression of effector genes. PLoS Genet 12:e1006401 http://dx.doi.org/10.1371/journal.pgen.1006401. (Erratum, 12:e1006527. doi:10.1371/journal.pgen.1006527.)
241. van Dam P, Fokkens L, Schmidt SM, Linmans JH, Kistler HC, Ma LJ, Rep M. 2016. Effector profiles distinguish formae speciales of Fusarium oxysporum. Environ Microbiol 18:4087–4102 http://dx.doi.org/10.1111/1462-2920.13445.
242. Schmidt SM, Lukasiewicz J, Farrer R, van Dam P, Bertoldo C, Rep M. 2016. Comparative genomics of Fusarium oxysporum f. sp. melonis reveals the secreted protein recognized by the Fom-2 resistance gene in melon. New Phytol 209:307–318 http://dx.doi.org/10.1111/nph.13584.
243. Jonkers W, Xayamongkhon H, Haas M, Olivain C, van der Does HC, Broz K, Rep M, Alabouvette C, Steinberg C, Kistler HC. 2014. EBR1 genomic expansion and its role in virulence of Fusarium species. Environ Microbiol 16:1982–2003 http://dx.doi.org/10.1111/1462-2920.12331.
244. Schmidt SM, Houterman PM, Schreiver I, Ma L, Amyotte S, Chellappan B, Boeren S, Takken FL Rep M. 2013. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum. BMC Genomics 14:119. 10.1186/1471-2164-14-119. [PubMed]
245. Kellner R, Bhattacharyya A, Poppe S, Hsu TY, Brem RB, Stukenbrock EH. 2014. Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biol Evol 6:1353–1365. 10.1093/gbe/evu101. [PubMed]
246. McClintock B. 1938. The production of homozygous deficient tissues with mutant characteristics by means of the aberrant mitotic behavior of ring-shaped chromosomes. Genetics 23:315–376. [PubMed]
247. McClintock B. 1941. The stability of broken ends of chromosomes in Zea mays. Genetics 26:234–282. [PubMed]
248. Croll D, Lendenmann MH, Stewart E, McDonald BA. 2015. The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics 201:1213–1228 http://dx.doi.org/10.1534/genetics.115.180968.
249. Sewitz SA, Fahmi Z, Lipkow K. 2017. Higher order assembly: folding the chromosome. Curr Opin Struct Biol 42:162–168 http://dx.doi.org/10.1016/j.sbi.2017.02.004.
250. van Berkum NL, Lieberman-Aiden E, Williams L, Imakaev M, Gnirke A, Mirny LA, Dekker J, Lander ES. 2010. Hi-C: a method to study the three-dimensional architecture of genomes. J Vis Exp 39:1869. 10.3791/1869. [PubMed]
251. Denker A, de Laat W. 2016. The second decade of 3C technologies: detailed insights into nuclear organization. Genes Dev 30:1357–1382 http://dx.doi.org/10.1101/gad.281964.116.
252. 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 http://dx.doi.org/10.1038/nature08973.
253. 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. 10.1093/nar/gkq955. [PubMed]
254. Iwasaki O, Tanizawa H, Kim KD, Yokoyama Y, Corcoran CJ, Tanaka A, Skordalakes E, Showe LC, Noma K. 2015. Interaction between TBP and condensin drives the organization and faithful segregation of mitotic chromosomes. Mol Cell 59:755–767 http://dx.doi.org/10.1016/j.molcel.2015.07.007.
255. Kim KD, Tanizawa H, Iwasaki O, Noma K. 2016. Transcription factors mediate condensin recruitment and global chromosomal organization in fission yeast. Nat Genet 48:1242–1252 http://dx.doi.org/10.1038/ng.3647.
256. Iwasaki O, Noma KI. 2016. Condensin-mediated chromosome organization in fission yeast. Curr Genet 62:739–743 http://dx.doi.org/10.1007/s00294-016-0601-7.
257. Zemach A, McDaniel IE, Silva P, Zilberman D. 2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919. 10.1126/science.1186366. [PubMed]
258. Huff JT, Zilberman D. 2014. Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes. Cell 156:1286–1297 http://dx.doi.org/10.1016/j.cell.2014.01.029.
259. Florea S, Phillips TD, Panaccione DG, Farman ML, Schardl CL. 2016. Chromosome-end knockoff strategy to reshape alkaloid profiles of a fungal endophyte. G3 (Bethesda) 6:2601–2610 http://dx.doi.org/10.1534/g3.116.029686. [PubMed]
260. Levis C, Giraud T, Dutertre M, Fortini D, Brygoo Y. 1997. Telomeric DNA of Botrytis cinerea: a useful tool for strain identification. FEMS Microbiol Lett 157:267–272 http://dx.doi.org/10.1111/j.1574-6968.1997.tb12783.x.
261. Duffy M, Chambers A. 1996. DNA-protein interactions at the telomeric repeats of Schizosaccharomyces pombe. Nucleic Acids Res 24:1412–1419 http://dx.doi.org/10.1093/nar/24.8.1412.
262. Edman JC. 1992. Isolation of telomerelike sequences from Cryptococcus neoformans and their use in high-efficiency transformation. Mol Cell Biol 12:2777–2783 http://dx.doi.org/10.1128/MCB.12.6.2777.
263. Sánchez-Alonso P, Guzmán P. 1998. Organization of chromosome ends in Ustilago maydis. RecQ-like helicase motifs at telomeric regions. Genetics 148:1043–1054. [PubMed]
264. Ciferri C, Lander GC, Maiolica A, Herzog F, Aebersold R, Nogales E. 2012. Molecular architecture of human polycomb repressive complex 2. eLife 1:e00005 http://dx.doi.org/10.7554/eLife.00005.

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Chromatin and chromosomes of fungi are highly diverse and dynamic, even within species. Much of what we know about histone modification enzymes, RNA interference, DNA methylation, and cell cycle control was first addressed in , , , and . Here, we examine the three landmark regions that are required for maintenance of stable chromosomes and their faithful inheritance, namely, origins of DNA replication, telomeres and centromeres. We summarize the state of recent chromatin research that explains what is required for normal function of these specialized chromosomal regions in different fungi, with an emphasis on the silencing mechanism associated with subtelomeric regions, initiated by sirtuin histone deacetylases and histone H3 lysine 27 (H3K27) methyltransferases. We explore mechanisms for the appearance of “accessory” or “conditionally dispensable” chromosomes and contrast what has been learned from studies on genome-wide chromosome conformation capture in , , , and . While most of the current knowledge is based on work in a handful of genetically and biochemically tractable model organisms, we suggest where major knowledge gaps remain to be closed. Fungi will continue to serve as facile organisms to uncover the basic processes of life because they make excellent model organisms for genetics, biochemistry, cell biology, and evolutionary biology.

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Presence and absence of selected histone H3 and cytosine DNA methylation marks, structure of centromeres, and sequence of telomere repeats in selected fungi. Representative fungi from various clades were selected to show the phylogenetic distribution of chromatin characteristics. Species in which the presence (check) or absence (cross) were experimentally validated are largely found within the Ascomycota, while species for which only genome sequencing-based evidence for the presence (plus) or absence (minus) of genes is available are in the Basidiomycota and the large group of early-diverging lineages. No experimental data on chromatin modifications in chytrids and microsporidia are available; some chytrids have predicted DNA methyltransferases (DNMTs) that are similar to those in animals, while some zygomycetes (e.g., ) have DNMTs similar to those in ascomycetes ( 257 ). has no cytosine methylation, but sister species have intact genes for DNMTs. No obvious DNMTs are found in the genome, yet there have been reports on cytosine DNA methylation. , unlike , appears to have genes to carry out all modifications listed here, suggesting large diversity in the Taphrinomycotina. More recently, an entirely new class of cytosine DNA methyltransferases has been identified in fungi, demonstrating DNA methylation in species that were long thought to be devoid of methylation such as ( 258 ). The overall distribution pattern suggests that genes necessary to catalyze the two major gene silencing histone modifications, H3K9me and H3K27me, are ancient and have been lost in several branches over evolutionary time. The presence of conserved genes does not necessarily mean the presence of the expected chromatin modification. Centromeric DNA segments (Cen) are defined as regions with CENP-A or CENP-C enrichment, are highly variable in size, and even for some of the best-studied fungi such as , we still do not have experimental data. Pericentric regions, flanking the Cen regions, are larger and also of variable size. Most fungi use the mammalian and human () consensus telomeric repeat sequence, 5′-TTAGGG-3′, sometimes with a variable number of Gs like in . Data on telomere repeats were compiled from the literature ( 54 , 61 , 65 , 70 , 72 , 73 , 75 , 119 , 124 , 151 , 194 , 259 263 ).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
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Chromosome landmarks in four model organisms. Characteristics of DNA sequences for replication origins and centromere and telomere repeats are compared between budding yeast (), fission yeast (), , and the basidiomycete yeast . Few origins have been mapped in , so it seems premature to say whether they share specific characteristics ( 45 ). ARS, autonomously replicating sequence.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
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Telomere-repeat binding complexes homologous to mammalian shelterin. The buddding yeast has a CST (Cdc13, Stn1, Ten1) complex that binds to single-stranded 3′-G-rich-tail overhangs. The nucleosome-free double-stranded DNA is bound by Rap1, which in turn forms complexes with Rif1 and Rif2. Subtelomeric regions are transcriptionally silent because of hypoacetylation initiated by Sir2 and propagated by the Sir complex. The fission yeast has poorly conserved proteins serving similar functions as the CST complex, namely Pot1, Tpz1, and Ccq1. Poz1 creates a bridge to the Rap1/Taz1 complex, but Rap1 has different functions than in , even though there is slight sequence conservation. There is no Sir2-3-4 complex; instead, fission yeast uses H3K9me2-mediated silencing catalyzed by the Clr4 complex and recognized by HP1 (called Swi6 in ). The shelterin complex first identified in mammals by purification of the first telomere-repeat factors is very similar to the complex, though Ccq1 is apparently missing. In both and mammals, HP1 acts on the CST complex homologues, and in a histone deacetylase complex (SHREC) is involved.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
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Polycomb repressive complex 2 (PRC2) from three fungi has different components. Facultative heterochromatin, enriched with H3K27me2/3, is generated by PRC2 complexes. Approximate arrangement of complex subunits is based on published structures of human ( 264 ) and PRC2 ( 143 ). has a core PRC2 complex that lacks a homologue of the Msi1 homologue (crossed out MSL1) that is found in PRC2 of (NPF) and (Msl1). While genes for KMT6, EED, and SUZ12 homologues are found in many taxa, the CnCcc1 and CnBnd1 proteins are restricted in distribution, suggesting diversification of PRC2 across the fungi. Ezh ( KMT6, E(z), human EZH2, SET-7, Ezh) contains 10 structurally distinct motifs (adapted from reference 143 ): (i) SBD (SANT1L-binding domain), (ii) EBD (Eed-binding domain), (iii) BAM (b-addition motif), (iv) SAL (SET activation loop), (v) SRM (stimulation-responsive motif), (vi) SANT1L (SANT1-like), (vii) MCSS (motif connecting SANT1L and SANT2L), (viii) SANT2L (SANT2-like), (ix) CXC (cysteine-rich pre-SET domain), and (x) the catalytic SET domain. The SANT motifs are the least conserved surfaces in the crystal structure. Fungal EED proteins ( Esc) contain WD40 (WD) domains that generate a seven-bladed propeller structure, for which the C-terminus folds back toward the N-terminus to generate propeller 1. The function of the extended C-terminal insertion domain is unknown. The accessory Msl1/NPF subunit of and is conserved in humans (RBAp46/48); all Msi1-like proteins share the WD40 propeller structure with EED. SUZ12 [ Su(z)12] contains an Eed-binding domain ( 2 ), a Zn-finger region (Z), and a conserved VEFS domain that in the crystal structure is wedged between KMT6 and EED.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
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Histone modifications associated with transcriptionally active euchromatin and transcriptionally silent heterochromatin on four types of chromosomes found in many fungi. Core or “A” chromosomes have a mixture of transcriptionally active euchromatin (green), constitutively silent heterochromatin (gray) that remains densely packaged even in interphase, and facultative heterochromatin (orange) that becomes transcriptionally active upon external or internal cues. Modifications on core chromosomes most often correlated with euchromatin are H3K4 di- and trimethylation (H3K4me2/3), which are usually found in sharp peaks around the nucleosome-free transcriptional start sites or in the 5′ regions of genes. In constitutive heterochromatin, which is often found in repetitive DNA sequences such as centromeric regions that also contain CenH3 nucleosomes (purple), in pericentric (dark gray) regions, or in transposable elements (light gray), H3K9 is di- or trimethylated (H3K9me2/3) and DNA is often methylated at cytosines. In facultative heterochromatin, H3K27 is di- or trimethylated (H3K27me2/3) and controls the expression of genes in a time- and space-dependent manner. Telomeric repeats (blue) have specialized chromatin structures in many fungi; some are free of nucleosomes and bound by shelterin-like complexes. In addition to the histone modifications shown here, lysines in the H3 and H4 tails of euchromatic regions are hyperacetylated (H3ac, H4ac), H3K79 and H3K36 are trimethylated (H3K79me3, H3K36me3), and H2BK120 is mono-ubiquitylated (H2BK120ub1); canonical H2A is replaced by the variant H2AZ. In heterochromatin, H3 and H4 lysines are hypoacetylated and H2AK119 is mono-ubiquitylated (H2A119ub1). In several species and in , complete chromosomes or segments of chromosome arms from accessory chromosomes that are enriched for H3K27 methylation have translocated onto core chromosomes, generating bipartite chromosomes with different histone modification environments. Most accessory chromosomes from and species that have been studied show almost complete coverage with H3K27me3. A very minor fraction of genes is active and enriched with H3K4me2/3, while pericentric regions and centromeric regions in species are enriched with H3K9me3. In , H3K9me3 and H3K27me3 are partially overlapping in repeat-rich regions, but H3K27me3 is mostly found at silent genes. In this species no clear correlation with centromeric chromatin and any tested histone modification has been found. The shortest accessory chromosomes have no active genes and show equal fractions of H3K27me3 and H3K9me3. Predicted structure of true “B” chromosomes similar to those that have been found in plants and animals. These simplest chromosomes are completely gene-free and have only constitutive H3K9me3-enriched heterochromatin, centromeres, and telomeres. No such true B chromosomes have been documented in fungi.

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
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Three-dimensional models of linkage group (LG) VII based on Hi-C data. Chromosomes are represented as wire diagrams, where the wire path runs through the center of a series of 50-kb “spheres” determined by the contact frequencies calculated from Hi-C datasets for the wild type and three chromatin mutants (, , ). The chromosome path is calculated by attractive or repulsive forces between each sphere so that the system relaxes to a low energy state. Regions that are enriched with one heterochromatic mark, H3K9me3, in the wild type are shaded in red. Centromeres and subtelomeres are separated, but telomeres are closer to each other than to the centromere (adapted from reference 131 ).

Source: microbiolspec July 2017 vol. 5 no. 4 doi:10.1128/microbiolspec.FUNK-0054-2017
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