1887

Abstract

Chemical modifications of DNA and histone proteins impact the organization of chromatin within the nucleus. Changes in these modifications, catalysed by different chromatin-modifying enzymes, influence chromatin organization, which in turn is thought to impact the spatial and temporal regulation of gene expression. While combinations of different histone modifications, the histone code, have been studied in several model species, we know very little about histone modifications in the fungal genus , whose members are generally well studied due to their importance as models in cell and molecular biology as well as their medical and biotechnological relevance. Here, we used phylogenetic analyses in 94 Aspergilli as well as other fungi to uncover the occurrence and evolutionary trajectories of enzymes and protein complexes with roles in chromatin modifications or regulation. We found that these enzymes and complexes are highly conserved in Aspergilli, pointing towards a complex repertoire of chromatin modifications. Nevertheless, we also observed few recent gene duplications or losses, highlighting species to further study the roles of specific chromatin modifications. SET7 (KMT6) and other components of PRC2 (Polycomb Repressive Complex 2), which is responsible for methylation on histone H3 at lysine 27 in many eukaryotes including fungi, are absent in Aspergilli as well as in closely related species, suggesting that these lost the capacity for this histone modification. We corroborated our computational predictions by performing untargeted MS analysis of histone post-translational modifications in . This systematic analysis will pave the way for future research into the complexity of the histone code and its functional implications on genome architecture and gene regulation in fungi.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000856
2022-09-21
2024-05-14
Loading full text...

Full text loading...

/deliver/fulltext/mgen/8/9/mgen000856.html?itemId=/content/journal/mgen/10.1099/mgen.0.000856&mimeType=html&fmt=ahah

References

  1. Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 2014; 42:D699–704 [View Article] [PubMed]
    [Google Scholar]
  2. Labrador M, Corces VG. Setting the boundaries of chromatin domains and nuclear organization. Cell 2002; 111:151–154 [View Article] [PubMed]
    [Google Scholar]
  3. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389:251–260 [View Article] [PubMed]
    [Google Scholar]
  4. Luger K. Structure and dynamic behavior of nucleosomes. Curr Opin Genet Dev 2003; 13:127–135 [View Article] [PubMed]
    [Google Scholar]
  5. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074–1080 [View Article] [PubMed]
    [Google Scholar]
  6. Peterson CL, Laniel M-A. Histones and histone modifications. Curr Biol 2004; 14:R546–51 [View Article] [PubMed]
    [Google Scholar]
  7. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE et al. Active genes are tri-methylated at K4 of histone H3. Nature 2002; 419:407–411 [View Article] [PubMed]
    [Google Scholar]
  8. Grewal SIS, Jia S. Heterochromatin revisited. Nat Rev Genet 2007; 8:35–46 [View Article] [PubMed]
    [Google Scholar]
  9. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447:407–412 [View Article] [PubMed]
    [Google Scholar]
  10. Xiao B, Wilson JR, Gamblin SJ. SET domains and histone methylation. Curr Opin Struct Biol 2003; 13:699–705 [View Article] [PubMed]
    [Google Scholar]
  11. Collemare J, Seidl MF. Chromatin-dependent regulation of secondary metabolite biosynthesis in fungi: is the picture complete?. FEMS Microbiol Rev 2019; 43:591–607 [View Article] [PubMed]
    [Google Scholar]
  12. Helmlinger D, Papai G, Devys D, Tora L. What do the structures of GCN5-containing complexes teach us about their function?. Biochim Biophys Acta Gene Regul Mech 2021; 1864:194614 [View Article] [PubMed]
    [Google Scholar]
  13. Hajheidari M, Koncz C, Bucher M. Chromatin evolution-key innovations underpinning Morphological complexity. Front Plant Sci 2019; 10:1–12 [View Article]
    [Google Scholar]
  14. Gates LA, Foulds CE, O’Malley BW. Histone Marks in the ‘Driver’s Seat’: functional roles in steering the transcription cycle. Trends Biochem Sci 2017; 42:977–989 [View Article]
    [Google Scholar]
  15. Jamieson K, Wiles ET, McNaught KJ, Sidoli S, Leggett N et al. Loss of HP1 causes depletion of H3K27me3 from facultative heterochromatin and gain of H3K27me2 at constitutive heterochromatin. Genome Res 2016; 26:97–107 [View Article] [PubMed]
    [Google Scholar]
  16. Jamieson K, Rountree MR, Lewis ZA, Stajich JE, Selker EU. Regional control of histone H3 lysine 27 methylation in Neurospora. Proc Natl Acad Sci U S A 2013; 110:6027–6032 [View Article] [PubMed]
    [Google Scholar]
  17. Freitag M. Histone methylation by SET domain proteins in Fungi. Annu Rev Microbiol 2017; 71:413–439 [View Article] [PubMed]
    [Google Scholar]
  18. Kamei M, Ameri AJ, Ferraro AR, Bar-Peled Y, Zhao F et al. Imitation switch is required for normal chromatin structure and gene repression in PRC2 target domains. Proc Natl Acad Sci U S A 2021; 118:e2010003118 [View Article] [PubMed]
    [Google Scholar]
  19. Weiner AKM, Cerón-Romero MA, Yan Y, Katz LA. Phylogenomics of the Epigenetic toolkit reveals punctate retention of genes across Eukaryotes. Genome Biol Evol 2020; 12:2196–2210 [View Article] [PubMed]
    [Google Scholar]
  20. Choi J, Kim S-H. A genome tree of life for the fungi kingdom. Proc Natl Acad Sci U S A 2017; 114:9391–9396 [View Article] [PubMed]
    [Google Scholar]
  21. Bewick AJ, Hofmeister BT, Powers RA, Mondo SJ, Grigoriev IV et al. Diversity of cytosine methylation across the fungal tree of life. Nat Ecol Evol 2019; 3:479–490 [View Article] [PubMed]
    [Google Scholar]
  22. Kouzminova E, Selker EU. Dim-2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO J 2001; 20:4309–4323 [View Article] [PubMed]
    [Google Scholar]
  23. Nai YS, Huang YC, Yen MR, Chen PY. Diversity of fungal DNA Methyltransferases and their association with DNA Methylation patterns. Front Microbiol 2020; 11:616922 [View Article] [PubMed]
    [Google Scholar]
  24. Samson RA, Visagie CM, Houbraken J, Hong S-B, Hubka V et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 2014; 78:141–173 [View Article] [PubMed]
    [Google Scholar]
  25. Cánovas D, Marcos AT, Gacek A, Ramos MS, Gutiérrez G et al. The histone acetyltransferase GcnE (GCN5) plays a central role in the regulation of Aspergillus asexual development. Genetics 2014; 197:1175–1189 [View Article] [PubMed]
    [Google Scholar]
  26. Palmer JM, Perrin RM, Dagenais TRT, Keller NP. H3K9 methylation regulates growth and development in Aspergillus fumigatus. Eukaryot Cell 2008; 7:2052–2060 [View Article] [PubMed]
    [Google Scholar]
  27. Yang K, Liang L, Ran F, Liu Y, Li Z et al. The DmtA methyltransferase contributes to Aspergillus flavus conidiation, sclerotial production, aflatoxin biosynthesis and virulence. Sci Rep 2016; 6:1–13 [View Article] [PubMed]
    [Google Scholar]
  28. Palmer JM, Bok JW, Lee S, Dagenais TRT, Andes DR et al. Loss of CclA, required for histone 3 lysine 4 methylation, decreases growth but increases secondary metabolite production in Aspergillus fumigatus. PeerJ 2013; 1:1–18 [View Article] [PubMed]
    [Google Scholar]
  29. Georgakopoulos P, Lockington RA, Kelly JM. The Spt-Ada-Gcn5 Acetyltransferase (SAGA) complex in Aspergillus nidulans. PLoS ONE 2013; 8:e65221 [View Article] [PubMed]
    [Google Scholar]
  30. Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol 2011; 7:e1002195 [View Article] [PubMed]
    [Google Scholar]
  31. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  32. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  33. Chernomor O, von Haeseler A, Minh BQ. Terrace aware data structure for Phylogenomic inference from supermatrices. Syst Biol 2016; 65:997–1008 [View Article] [PubMed]
    [Google Scholar]
  34. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  35. Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 2011; 60:685–699 [View Article] [PubMed]
    [Google Scholar]
  36. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  37. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [View Article] [PubMed]
    [Google Scholar]
  38. Boratyn GM, Camacho C, Cooper PS, Coulouris G, Fong A et al. BLAST: a more efficient report with usability improvements. Nucleic Acids Res 2013; 41:W29–33 [View Article] [PubMed]
    [Google Scholar]
  39. Slater GSC, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 2005; 6:31 [View Article] [PubMed]
    [Google Scholar]
  40. Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000; 16:276–277 [View Article] [PubMed]
    [Google Scholar]
  41. Hunter JD. Matplotlib: a 2D graphics environment. Comput Sci Eng 2011; 9:90–95 [View Article]
    [Google Scholar]
  42. Waskom ML. Seaborn: statistical data visualization. JOSS 2011; 6:3021 [View Article]
    [Google Scholar]
  43. Noberini R, Restellini C, Savoia EO, Bonaldi T. Enrichment of histones from patient samples for mass spectrometry-based analysis of post-translational modifications. Methods 2020; 184:19–28 [View Article] [PubMed]
    [Google Scholar]
  44. He F. Bradford protein assay. BIO Protoc 2011; 1: [View Article]
    [Google Scholar]
  45. Noberini R, Savoia EO, Brandini S, Greco F, Marra F et al. Spatial epi-proteomics enabled by histone post-translational modification analysis from low-abundance clinical samples. Clin Epigenetics 2021; 13:1–16 [View Article] [PubMed]
    [Google Scholar]
  46. Prudhomme N, Gianetto-Hill C, Pastora R, Cheung W-F, Allen-Vercoe E et al. Quantitative proteomic profiling of shake flask versus bioreactor growth reveals distinct responses of Agrobacterium tumefaciens for preparation in molecular pharming. Can J Microbiol 2021; 67:75–84 [View Article] [PubMed]
    [Google Scholar]
  47. Bremang M, Cuomo A, Agresta AM, Stugiewicz M, Spadotto V et al. Mass spectrometry-based identification and characterisation of lysine and arginine methylation in the human proteome. Mol Biosyst 2013; 9:2231–2247 [View Article] [PubMed]
    [Google Scholar]
  48. Yuan Z-F, Sidoli S, Marchione DM, Simithy J, Janssen KA et al. EpiProfile 2.0: a computational platform for processing Epi-Proteomics mass spectrometry data. J Proteome Res 2018; 17:2533–2541 [View Article] [PubMed]
    [Google Scholar]
  49. Pesavento JJ, Mizzen CA, Kelleher NL. Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: human histone H4. Anal Chem 2006; 78:4271–4280 [View Article] [PubMed]
    [Google Scholar]
  50. Wade PA, Pruss D, Wolffe AP. Histone acetylation: chromatin in action. Trends Biochem Sci 1997; 22:128–132 [View Article] [PubMed]
    [Google Scholar]
  51. Binda O. On your histone mark, SET, methylate!. Epigenetics 2013; 8:457–463 [View Article] [PubMed]
    [Google Scholar]
  52. Wolffe AP, Matzke MA. Epigenetics: regulation through repression. Science 1999; 286:481–486 [View Article] [PubMed]
    [Google Scholar]
  53. James TY, Stajich JE, Hittinger CT, Rokas A. Toward a fully resolved fungal tree of life. Annu Rev Microbiol 2020; 74:291–313 [View Article] [PubMed]
    [Google Scholar]
  54. Sun BD, Houbraken J, Frisvad JC, Jiang XZ, Chen AJ et al. New species in Aspergillus section Usti and an overview of Aspergillus section Cavernicolarum. Int J Syst Evol Microbiol 2020; 70:5401–5416 [View Article] [PubMed]
    [Google Scholar]
  55. Chen AJ, Frisvad JC, Sun BD, Varga J, Kocsubé S et al. Aspergillus section Nidulantes (formerly Emericella): polyphasic taxonomy, chemistry and biology. Stud Mycol 2016; 84:1–118
    [Google Scholar]
  56. Steenwyk JL, Shen X-X, Lind AL, Goldman GH, Rokas A. A robust phylogenomic time tree for biotechnologically and medically important fungi in the genera Aspergillus and Penicillium. mBio 2019; 10:1–25 [View Article] [PubMed]
    [Google Scholar]
  57. Vesth TC, Nybo JL, Theobald S, Frisvad JC, Larsen TO et al. Investigation of inter- and intraspecies variation through genome sequencing of Aspergillus section Nigri. Nat Genet 2018; 50:1688–1695 [View Article] [PubMed]
    [Google Scholar]
  58. Kjærbølling I, Vesth T, Frisvad JC, Nybo JL, Theobald S et al. A comparative genomics study of 23 Aspergillus species from section Flavi. Nat Commun 2020; 11:1106 [View Article] [PubMed]
    [Google Scholar]
  59. Souza SC, Pereira VM, Moreira SI, Costa SS, Moreira GM et al. Aspergillus trisporus: a new jani section species from Brazilian soil. CREAM 2019; 9:175–186 [View Article]
    [Google Scholar]
  60. Grunstein M, Gasser SM. Epigenetics in Saccharomyces cerevisiae. Cold Spring Harb Perspect Biol 2013; 5:a017491 [View Article] [PubMed]
    [Google Scholar]
  61. Nielsen JC, Grijseels S, Prigent S, Ji B, Dainat J et al. Global analysis of biosynthetic gene clusters reveals vast potential of secondary metabolite production in Penicillium species. Nat Microbiol 2017; 2:April [View Article]
    [Google Scholar]
  62. Ko Y-H, So K-K, Chun J, Kim D-H, Kronstad JW. Distinct roles of two DNA Methyltransferases from Cryphonectria parasitica in fungal virulence, responses to hypovirus infection, and viral clearance. mBio 2017; 12:1–16 [View Article]
    [Google Scholar]
  63. Jurkowski TP, Jeltsch A, Lyko F. On the evolutionary origin of Eukaryotic DNA Methyltransferases and Dnmt2. PLoS ONE 2017; 6:e28104 [View Article]
    [Google Scholar]
  64. Bestor T. Structure of mammalian DNA methyltransferase as deduced from the inferred amino acid sequence and direct studies of the protein. Biochemical Society Transactions 2017; 16:944–947 [View Article]
    [Google Scholar]
  65. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998; 19:219–220 [View Article] [PubMed]
    [Google Scholar]
  66. Zhang Z, He C, Chen Y, Li B, Tian S. DNA Methyltransferases regulate pathogenicity of Botrytis cinerea to horticultural crops. J Fungi (Basel) 2021; 7:659 [View Article] [PubMed]
    [Google Scholar]
  67. Möller M, Habig M, Lorrain C, Feurtey A, Haueisen J et al. Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen. PLoS Genet 2021; 17:1–27 [View Article] [PubMed]
    [Google Scholar]
  68. Delmas V, Stokes DG, Perry RP. A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain. Proc Natl Acad Sci U S A 1993; 90:2414–2418 [View Article] [PubMed]
    [Google Scholar]
  69. Capuano F, Mülleder M, Kok R, Blom HJ, Ralser M. Cytosine DNA methylation is found in Drosophila melanogaster but absent in Saccharomyces cerevisiae, Schizosaccharomyces pombe, and other yeast species. Anal Chem 2014; 86:3697–3702 [View Article] [PubMed]
    [Google Scholar]
  70. Huff JT, Zilberman D. Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes. Cell 2014; 156:1286–1297 [View Article] [PubMed]
    [Google Scholar]
  71. Proffitt JH, Davie JR, Swinton D, Hattman S. 5-Methylcytosine is not detectable in Saccharomyces cerevisiae DNA. Mol Cell Biol 1984; 4:985–988 [View Article] [PubMed]
    [Google Scholar]
  72. Rountree MR, Selker EU. DNA methylation and the formation of heterochromatin in Neurospora crassa. Heredity (Edinb) 2010; 105:38–44 [View Article] [PubMed]
    [Google Scholar]
  73. Grognet P, Timpano H, Carlier F, Aït-Benkhali J, Berteaux-Lecellier V et al. A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina. PLoS Genet 2019; 15:e1008086 [View Article] [PubMed]
    [Google Scholar]
  74. Catania S, Dumesic PA, Pimentel H, Nasif A, Stoddard CI et al. Evolutionary persistence of DNA Methylation for millions of years after ancient loss of a De Novo Methyltransferase. Cell 2020; 180:263–277 [View Article] [PubMed]
    [Google Scholar]
  75. Madhani HD. Unbelievable but true: epigenetics and chromatin in fungi. Trends Genet 2021; 37:12–20 [View Article] [PubMed]
    [Google Scholar]
  76. Liu S-Y, Lin J-Q, Wu H-L, Wang C-C, Huang S-J et al. Bisulfite sequencing reveals that Aspergillus flavus holds a hollow in DNA Methylation. PLoS ONE 2012; 7:e30349 [View Article]
    [Google Scholar]
  77. Spellmon N, Holcomb J, Trescott L, Sirinupong N, Yang Z. Structure and function of SET and MYND domain-containing proteins. Int J Mol Sci 2015; 16:1406–1428 [View Article] [PubMed]
    [Google Scholar]
  78. Raunser S, Magnani R, Huang Z, Houtz RL, Trievel RC et al. Rubisco in complex with Rubisco large subunit methyltransferase. Proc Natl Acad Sci U S A 2009; 106:3160–3165 [View Article] [PubMed]
    [Google Scholar]
  79. Trievel RC, Flynn EM, Houtz RL, Hurley JH. Mechanism of multiple lysine methylation by the SET domain enzyme Rubisco LSMT. Nat Struct Biol 2003; 10:545–552 [View Article] [PubMed]
    [Google Scholar]
  80. Porras Y, Whitelegge JP, Clarke S. Yeast ribosomal/cytochrome c SET domain methyltransferase subfamily: identification of Rpl23ab methylation sites and recognition motifs. J Biol Chem 2007; 282:12368–12376 [View Article] [PubMed]
    [Google Scholar]
  81. Roguev A, Schaft D, Shevchenko A, Pijnappel WW, Wilm M et al. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 2001; 20:7137–7148 [View Article] [PubMed]
    [Google Scholar]
  82. Zhang X, Tamaru H, Khan SI, Horton JR, Keefe LJ et al. Structure of the Neurospora SET domain protein DIM-5, a Histone H3 Lysine Methyltransferase. Cell 2002; 111:117–127 [View Article]
    [Google Scholar]
  83. Marina DB, Shankar S, Natarajan P, Finn KJ, Madhani HD. A conserved ncRNA-binding protein recruits silencing factors to heterochromatin through an RNAi-independent mechanism. Genes Dev 2013; 27:1851–1856 [View Article]
    [Google Scholar]
  84. Strahl BD, Grant PA, Briggs SD, Sun Z-W, Bone JR et al. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 2002; 22:1298–1306 [View Article] [PubMed]
    [Google Scholar]
  85. Xiao T, Hall H, Kizer KO, Shibata Y, Hall MC et al. Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev 2003; 17:654–663 [View Article] [PubMed]
    [Google Scholar]
  86. Li M, Phatnani HP, Guan Z, Sage H, Greenleaf AL et al. Solution structure of the Set2-Rpb1 interacting domain of human Set2 and its interaction with the hyperphosphorylated C-terminal domain of Rpb1. Proc Natl Acad Sci U S A 2005; 102:17636–17641 [View Article] [PubMed]
    [Google Scholar]
  87. Bicocca VT, Ormsby T, Adhvaryu KK, Honda S, Selker EU. ASH1-catalyzed H3K36 methylation drives gene repression and marks H3K27me2/3-competent chromatin. Elife 2018; 7:1–19 [View Article] [PubMed]
    [Google Scholar]
  88. Janevska S, Baumann L, Sieber CMK, Münsterkötter M, Ulrich J et al. Elucidation of the two H3K36me3 histone Methyltransferases Set2 and Ash1 in Fusarium fujikuroi unravels their different chromosomal targets and a major impact of Ash1 on genome stability. Genetics 2018; 208:153–171 [View Article] [PubMed]
    [Google Scholar]
  89. Wang Y, Reddy B, Thompson J, Wang H, Noma K et al. Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol Cell 2009; 33:428–437 [View Article] [PubMed]
    [Google Scholar]
  90. Veerappan CS, Avramova Z, Moriyama EN. Evolution of SET-domain protein families in the unicellular and multicellular Ascomycota fungi. BMC Evol Biol 2008; 8:1–20 [View Article] [PubMed]
    [Google Scholar]
  91. Gacek-Matthews A, Noble LM, Gruber C, Berger H, Sulyok M et al. KdmA, a histone H3 demethylase with bipartite function, differentially regulates primary and secondary metabolism in Aspergillus nidulans. Mol Microbiol 2015; 96:839–860 [View Article] [PubMed]
    [Google Scholar]
  92. Bachleitner S, Sørensen JL, Gacek-Matthews A, Sulyok M, Studt L et al. Evidence of a Demethylase-independent role for the H3K4-specific Histone Demethylases in Aspergillus nidulans and Fusarium graminearum secondary metabolism. Front Microbiol 2019; 10:1759 [View Article] [PubMed]
    [Google Scholar]
  93. Sneeringer CJ, Scott MP, Kuntz KW, Knutson SK, Pollock RM et al. Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. Proc Natl Acad Sci U S A 2010; 107:20980–20985 [View Article] [PubMed]
    [Google Scholar]
  94. Tao Y, Neppl RL, Huang Z-P, Chen J, Tang R-H et al. The histone methyltransferase Set7/9 promotes myoblast differentiation and myofibril assembly. J Cell Biol 2011; 194:551–565 [View Article] [PubMed]
    [Google Scholar]
  95. Kramer HM, Seidl MF, Thomma B, Cook DE. Local rather than Global H3K27me3 dynamics are associated with differential gene expression in Verticillium dahliae. mBio 2022e0356621 [View Article] [PubMed]
    [Google Scholar]
  96. Carrozza MJ, Utley RT, Workman JL, Côté J. The diverse functions of histone acetyltransferase complexes. Trends Genet 2003; 19:321–329 [View Article]
    [Google Scholar]
  97. Torchia J, Glass C, Rosenfeld MG. Co-activators and co-repressors in the integration of transcriptional responses. Curr Opin Cell Biol 1998; 10:373–383 [View Article]
    [Google Scholar]
  98. Sterner DE, Berger SL. Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 2000; 64:435–459 [View Article]
    [Google Scholar]
  99. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem 2001; 70:81–120 [View Article]
    [Google Scholar]
  100. Kawahara T, Siegel TN, Ingram AK, Alsford S, Cross GAM et al. Two essential MYST-family proteins display distinct roles in histone H4K10 acetylation and telomeric silencing in trypanosomes. Mol Microbiol 2008; 69:1054–1068 [View Article]
    [Google Scholar]
  101. Takechi S, Nakayama T. Sas3 is a histone acetyltransferase and requires a zinc finger motif. Biochem Biophys Res Commun 1999; 266:405–410 [View Article] [PubMed]
    [Google Scholar]
  102. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H et al. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 2006; 24:785–796 [View Article] [PubMed]
    [Google Scholar]
  103. Gómez EB, Espinosa JM, Forsburg SL. Schizosaccharomyces pombe mst2+ encodes a MYST family histone acetyltransferase that negatively regulates telomere silencing. Mol Cell Biol 2005; 25:8887–8903 [View Article] [PubMed]
    [Google Scholar]
  104. Nugent RL, Johnsson A, Fleharty B, Gogol M, Xue-Franzén Y et al. Expression profiling of S. pombe acetyltransferase mutants identifies redundant pathways of gene regulation. BMC Genomics 2010; 11:59 [View Article] [PubMed]
    [Google Scholar]
  105. Kim J, Park S, Lee JS. Epigenetic control of oxidative stresses by Histone Acetyltransferases in Candida albicans. J Microbiol Biotechnol 2018; 28:181–189 [View Article] [PubMed]
    [Google Scholar]
  106. Millar CB, Xu F, Zhang K, Grunstein M. Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev 2006; 20:711–722 [View Article] [PubMed]
    [Google Scholar]
  107. Searle NE, Torres-Machorro AL, Pillus L. Chromatin regulation by the NuA4 Acetyltransferase complex is mediated by essential interactions between enhancer of Polycomb (Epl1) and Esa1. Genetics 2017; 205:1125–1137 [View Article] [PubMed]
    [Google Scholar]
  108. Allard S, Utley RT, Savard J, Clarke A, Grant P et al. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 1999; 18:5108–5119 [View Article] [PubMed]
    [Google Scholar]
  109. Wang X, Chang P, Ding J, Chen J. Distinct and redundant roles of the two MYST histone acetyltransferases Esa1 and Sas2 in cell growth and morphogenesis of Candida albicans. Eukaryot Cell 2013; 12:438–449 [View Article] [PubMed]
    [Google Scholar]
  110. Meijsing SH, Ehrenhofer-Murray AE. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev 2001; 15:3169–3182 [View Article] [PubMed]
    [Google Scholar]
  111. Balasubramanian R, Pray-Grant MG, Selleck W, Grant PA, Tan S. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J Biol Chem 2002; 277:7989–7995 [View Article] [PubMed]
    [Google Scholar]
  112. Winkler GS, Kristjuhan A, Erdjument-Bromage H, Tempst P, Svejstrup JQ. Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc Natl Acad Sci U S A 2002; 99:3517–3522 [View Article] [PubMed]
    [Google Scholar]
  113. Krogan NJ, Greenblatt JF. Characterization of a six-subunit holo-elongator complex required for the regulated expression of a group of genes in Saccharomyces cerevisiae. Mol Cell Biol 2001; 21:8203–8212 [View Article] [PubMed]
    [Google Scholar]
  114. Wittschieben BO, Otero G, de Bizemont T, Fellows J, Erdjument-Bromage H et al. A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol Cell 1999; 4:123–128 [View Article] [PubMed]
    [Google Scholar]
  115. Okada Y, Yamagata K, Hong K, Wakayama T, Zhang Y. A role for the elongator complex in zygotic paternal genome demethylation. Nature 2010; 463:554–558 [View Article] [PubMed]
    [Google Scholar]
  116. Booker SJ, Grove TL. Mechanistic and functional versatility of radical SAM enzymes. F1000 Biol Rep 2010; 2:52 [View Article] [PubMed]
    [Google Scholar]
  117. Yuan Y, Yuan H, Yang G, Yun H, Zhao M et al. IFN-α confers epigenetic regulation of HBV cccDNA minichromosome by modulating GCN5-mediated succinylation of histone H3K79 to clear HBV cccDNA. Clin Epigenetics 2020; 12:1–16 [View Article] [PubMed]
    [Google Scholar]
  118. Kollenstart L, de Groot AJL, Janssen GMC, Cheng X, Vreeken K et al. Gcn5 and Esa1 function as histone crotonyltransferases to regulate crotonylation-dependent transcription. J Biol Chem 2019; 294:20122–20134 [View Article] [PubMed]
    [Google Scholar]
  119. Jones R. Identification and verification of lysine propionylation and butyrylation in yeast core histones using ptmap software. Bone 2014; 23:1–7
    [Google Scholar]
  120. Liu B, Lin Y, Darwanto A, Song X, Xu G et al. Identification and characterization of propionylation at histone H3 lysine 23 in mammalian cells. J Biol Chem 2009; 284:32288–32295 [View Article] [PubMed]
    [Google Scholar]
  121. Papanicolaou KN, O’Rourke B, Foster DB. Metabolism leaves its mark on the powerhouse: recent progress in post-translational modifications of lysine in mitochondria. Front Physiol 2014; 5:301 [View Article] [PubMed]
    [Google Scholar]
  122. Ekwall K. Genome-wide analysis of HDAC function. Trends Genet 2005; 21:608–615 [View Article] [PubMed]
    [Google Scholar]
  123. Bernstein BE, Tong JK, Schreiber SL. Genomewide studies of histone deacetylase function in yeast. Proc Natl Acad Sci U S A 2000; 97:13708–13713 [View Article] [PubMed]
    [Google Scholar]
  124. Honda S, Bicocca VT, Gessaman JD, Rountree MR, Yokoyama A et al. Dual chromatin recognition by the histone deacetylase complex HCHC is required for proper DNA methylation in Neurospora crassa. Proc Natl Acad Sci U S A 2016; 113:E6135–E6144 [View Article] [PubMed]
    [Google Scholar]
  125. Job G, Brugger C, Xu T, Lowe BR, Pfister Y et al. SHREC Silences Heterochromatin via Distinct Remodeling and Deacetylation Modules. Mol Cell 2016; 62:207–221 [View Article] [PubMed]
    [Google Scholar]
  126. Wu J, Suka N, Carlson M, Grunstein M. TUP1 utilizes histone H3/H2B-specific HDA1 deacetylase to repress gene activity in yeast. Mol Cell 2001; 7:117–126 [View Article] [PubMed]
    [Google Scholar]
  127. Kurdistani SK, Grunstein M. Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 2003; 4:276–284 [View Article] [PubMed]
    [Google Scholar]
  128. Li X, Pan L, Wang B, Pan L. The Histone Deacetylases HosA and HdaA affect the phenotype and transcriptomic and metabolic profiles of Aspergillus niger. Toxins (Basel) 2019; 11:E520 [View Article] [PubMed]
    [Google Scholar]
  129. Lee I, Oh J-H, Shwab EK, Dagenais TRT, Andes D et al. HdaA, a class 2 histone deacetylase of Aspergillus fumigatus, affects germination and secondary metabolite production. Fungal Genet Biol 2009; 46:782–790 [View Article] [PubMed]
    [Google Scholar]
  130. Brosch G, Loidl P, Graessle S. Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol Rev 2008; 32:409–439 [View Article] [PubMed]
    [Google Scholar]
  131. Carmen AA, Griffin PR, Calaycay JR, Rundlett SE, Suka Y et al. Yeast HOS3 forms a novel trichostatin A-insensitive homodimer with intrinsic histone deacetylase activity. Proc Natl Acad Sci U S A 1999; 96:12356–12361 [View Article] [PubMed]
    [Google Scholar]
  132. Pérez-Martínez ME, Benet M, Alepuz P, Tordera V. Nut1/Hos1 and Sas2/Rpd3 control the H3 acetylation of two different sets of osmotic stress-induced genes. Epigenetics 2020; 15:251–271 [View Article] [PubMed]
    [Google Scholar]
  133. Li S, Yue Z, Tanaka TU. Smc3 deacetylation by Hos1 facilitates efficient dissolution of sister chromatid cohesion during early anaphase. Mol Cell 2017; 68:605–614 [View Article] [PubMed]
    [Google Scholar]
  134. Wang A, Kurdistani SK, Grunstein M. Requirement of Hos2 histone deacetylase for gene activity in yeast. Science 2002; 298:1412–1414 [View Article] [PubMed]
    [Google Scholar]
  135. Suka N, Suka Y, Carmen AA, Wu J, Grunstein M. Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell 2001; 8:473–479 [View Article] [PubMed]
    [Google Scholar]
  136. De Nadal E, Zapater M, Alepuz PM, Sumoy L, Mas G et al. The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 2004; 427:370–374 [View Article] [PubMed]
    [Google Scholar]
  137. Tribus M, Bauer I, Galehr J, Rieser G, Trojer P et al. A novel motif in fungal class 1 histone deacetylases is essential for growth and development of Aspergillus. Mol Biol Cell 2010; 21:345–353 [View Article] [PubMed]
    [Google Scholar]
  138. Kawauchi M, Nishiura M, Iwashita K. Fungus-specific sirtuin HstD coordinates secondary metabolism and development through control of LaeA. Eukaryot Cell 2013; 12:1087–1096 [View Article] [PubMed]
    [Google Scholar]
  139. Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H et al. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 2006; 442:312–316 [View Article] [PubMed]
    [Google Scholar]
  140. Tamaru H. Confining euchromatin/heterochromatin territory: jumonji crosses the line. Genes Dev 2010; 24:1465–1478 [View Article] [PubMed]
    [Google Scholar]
  141. Isaac S, Walfridsson J, Zohar T, Lazar D, Kahan T et al. Interaction of epe1 with the heterochromatin assembly pathway in Schizosaccharomyces pombe. Genetics 2007; 175:1549–1560
    [Google Scholar]
  142. Turberfield AH, Kondo T, Nakayama M, Koseki Y, King HW et al. KDM2 proteins constrain transcription from CpG island gene promoters independently of their histone demethylase activity. Nucleic Acids Res 2019; 47:9005–9023 [View Article]
    [Google Scholar]
  143. Qian S, Wang Y, Ma H, Zhang L. Expansion and Functional Divergence of Jumonji C-Containing Histone Demethylases: Significance of Duplications in Ancestral Angiosperms and Vertebrates. Plant Physiol 2015; 168:1321–1337 [View Article]
    [Google Scholar]
  144. Hong SH, Cho YW, Yu LR, Yu H, Veenstra TD et al. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci U S A 2007; 104:18439–18444 [View Article]
    [Google Scholar]
  145. Agger K, Cloos PAC, Christensen J, Pasini D, Rose S et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007; 449:731–734 [View Article]
    [Google Scholar]
  146. Dehé P-M, Dichtl B, Schaft D, Roguev A, Pamblanco M et al. Protein interactions within the Set1 complex and their roles in the regulation of histone 3 lysine 4 methylation. J Biol Chem 2006; 281:35404–35412 [View Article]
    [Google Scholar]
  147. Lewis ZA, Adhvaryu KK, Honda S, Shiver AL, Knip M et al. DNA Methylation and normal chromosome behavior in Neurospora depend on five components of a histone Methyltransferase complex, DCDC. PLoS Genet 2010; 6:e1001196 [View Article]
    [Google Scholar]
  148. Eberharter A, Sterner DE, Schieltz D, Hassan A, Yates JR et al. The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae. Mol Cell Biol 1999; 19:6621–6631
    [Google Scholar]
  149. Doyon Y, Côté J. The highly conserved and multifunctional NuA4 HAT complex. Curr Opin Genet Dev 2004; 14:147–154 [View Article]
    [Google Scholar]
  150. Verzijlbergen KF, van Welsem T, Sie D, Lenstra TL, Turner DJ et al. A barcode screen for epigenetic regulators reveals a role for the NuB4/HAT-B Histone Acetyltransferase complex in Histone turnover. PLoS Genet 2011; 7:e1002284 [View Article]
    [Google Scholar]
  151. Sendra R, Tse C, Hansen JC. The yeast histone acetyltransferase A2 complex, but not free Gcn5p, binds stably to nucleosomal arrays. J Biol Chem 2000; 275:24928–24934 [View Article]
    [Google Scholar]
  152. Grant PA, Duggan L, Côté J, Roberts SM, Brownell JE et al. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an ada complex and the SAGA(spt/ada) complex. Genes Dev 1997; 11:1640–1650
    [Google Scholar]
  153. Erlendson AA, Friedman S, Freitag M, Heitman J, Stukenbrock EH. A matter of scale and dimensions: chromatin of chromosome landmarks in the fungi. Microbiol Spectr 2017; 5:4–5 [View Article]
    [Google Scholar]
  154. Buscaino A. Chromatin-Mediated Regulation of Genome Plasticity in Human Fungal Pathogens. Genes (Basel) 2019; 10:E855 [View Article]
    [Google Scholar]
  155. Steenwyk JL, Mead ME, Knowles SL, Raja HA, Roberts CD et al. Variation among biosynthetic gene clusters, secondary metabolite profiles, and cards of virulence across Aspergillus species. Genetics 2020; 216:481–497
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000856
Loading
/content/journal/mgen/10.1099/mgen.0.000856
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error