Epigenetic regulation of nuclear processes in fungal plant pathogens

Through the association of protein complexes to DNA, the eukaryotic nuclear genome is broadly organized into open euchromatin that is accessible for enzymes acting on DNA and condensed heterochromatin that is inaccessible. Chemical and physical alterations to chromatin may impact its organization and functionality and are therefore important regulators of nuclear processes. Studies in various fungal plant pathogens have uncovered an association between chromatin organization and expression of in planta-induced genes that are important for pathogenicity. This review discusses chromatin-based regulation mechanisms as determined in the fungal plant pathogen Verticillium dahliae and relates the importance of epigenetic transcriptional regulation and other nuclear processes more broadly in fungal plant pathogens.

[1]  B. Snel,et al.  Uncoupled evolution of the Polycomb system and deep origin of non-canonical PRC1 , 2023, bioRxiv.

[2]  Michael F. Seidl,et al.  Nuclear genome organization in fungi: from gene folding to Rabl chromosomes , 2023, FEMS microbiology reviews.

[3]  B. Thomma,et al.  Three-dimensional chromatin organization promotes genome evolution in a fungal plant pathogen , 2023, bioRxiv.

[4]  B. Henrissat,et al.  Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi , 2023, Nature Communications.

[5]  J. Ibeas,et al.  Systematic characterization of Ustilago maydis sirtuins shows Sir2 as a modulator of pathogenic gene expression , 2023, bioRxiv.

[6]  Mariana Villalba de la Peña,et al.  Chromatin structure influences rate and spectrum of spontaneous mutations in Neurospora crassa , 2023, bioRxiv.

[7]  David E. Cook,et al.  CRISPR-Cas12a induced DNA double-strand breaks are repaired by multiple pathways with different mutation profiles in Magnaporthe oryzae , 2022, Nature Communications.

[8]  Lauren S. Ryder,et al.  Rgs1 is a regulator of effector gene expression during plant infection by the rice blast fungus Magnaporthe oryzae , 2022, bioRxiv.

[9]  Lauren S. Ryder,et al.  The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors , 2022, bioRxiv.

[10]  David E. Cook,et al.  The contribution of DNA repair pathways to genome editing and evolution in filamentous pathogens , 2022, FEMS microbiology reviews.

[11]  Andrew D. Klocko,et al.  The genome organization of Neurospora crassa at high resolution uncovers principles of fungal chromosome topology , 2022, G3.

[12]  R. Allshire,et al.  Establishment of centromere identity is dependent on nuclear spatial organization , 2021, Current Biology.

[13]  Chaozu He,et al.  The histone acetyltransferase FocGCN5 regulates growth, conidiation, and pathogenicity of the banana wilt disease causal agent Fusarium oxysporum f.sp. cubense tropical race 4. , 2021, Research in microbiology.

[14]  E. Stukenbrock,et al.  Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus , 2021, Nature Communications.

[15]  Youfu Zhao,et al.  Fusarium BP1 is a reader of H3K27 methylation , 2021, Nucleic acids research.

[16]  Ursula Oggenfuss,et al.  A devil's bargain with transposable elements in plant pathogens. , 2021, Trends in genetics : TIG.

[17]  H. Kimura,et al.  Recent advance in single-cell epigenomics. , 2021, Current opinion in structural biology.

[18]  A. Dean,et al.  Enhancers navigate the three-dimensional genome to direct cell fate decisions. , 2021, Current opinion in structural biology.

[19]  Chenwu Xu,et al.  Genome-wide DNA mutations in Arabidopsis plants after multigenerational exposure to high temperatures , 2021, Genome biology.

[20]  D. Noordermeer,et al.  Loss of EZH2-like or SU(VAR)3–9-like proteins causes simultaneous perturbations in H3K27 and H3K9 tri-methylation and associated developmental defects in the fungus Podospora anserina , 2021, Epigenetics & chromatin.

[21]  Michael F. Seidl,et al.  Local Rather than Global H3K27me3 Dynamics Are Associated with Differential Gene Expression in Verticillium dahliae , 2021, bioRxiv.

[22]  Michael F. Seidl,et al.  Three putative DNA methyltransferases of Verticillium dahliae differentially contribute to DNA methylation that is dispensable for growth, development and virulence , 2021, Epigenetics & Chromatin.

[23]  Michael F. Seidl,et al.  Three putative DNA methyltransferases of Verticillium dahliae differentially contribute to DNA methylation that is dispensable for growth, development and virulence , 2021, Epigenetics & chromatin.

[24]  S. Henikoff,et al.  Histone variants at a glance , 2021, Journal of Cell Science.

[25]  C. Toseland,et al.  Regulation of Nuclear Mechanics and the Impact on DNA Damage , 2021, International journal of molecular sciences.

[26]  Wei Zhang,et al.  Histone modification dynamics at H3K27 are associated with altered transcription of in planta induced genes in Magnaporthe oryzae , 2021, PLoS genetics.

[27]  Michael F. Seidl,et al.  Transposable Elements Contribute to Genome Dynamics and Gene Expression Variation in the Fungal Plant Pathogen Verticillium dahliae , 2021, bioRxiv.

[28]  E. Furlong,et al.  To loop or not to loop: what is the role of TADs in enhancer function and gene regulation? , 2021, Current opinion in genetics & development.

[29]  M. Lorincz,et al.  Transcription shapes genome-wide histone acetylation patterns , 2021, Nature Communications.

[30]  M. Cox,et al.  Regulation of host-infection ability in the grass-symbiotic fungus Epichloë festucae by histone H3K9 and H3K36 methyltransferases. , 2020, Environmental microbiology.

[31]  Michael F. Seidl,et al.  A unique chromatin profile defines adaptive genomic regions in a fungal plant pathogen , 2020, eLife.

[32]  J. Heitman,et al.  Epigenetic dynamics of centromeres and neocentromeres in Cryptococcus deuterogattii , 2021, PLoS genetics.

[33]  Michael F. Seidl,et al.  Repetitive Elements Contribute to the Diversity and Evolution of Centromeres in the Fungal Genus Verticillium , 2020, mBio.

[34]  Michael F. Seidl,et al.  Genome evolution in fungal plant pathogens: looking beyond the two-speed genome model , 2020 .

[35]  Dushan N. Wadduwage,et al.  Advances in Chromatin and Chromosome Research: Perspectives from Multiple Fields. , 2020, Molecular cell.

[36]  M. Achrem,et al.  The epigenetic regulation of centromeres and telomeres in plants and animals , 2020, Comparative cytogenetics.

[37]  Elizabeth T. Wiles,et al.  Evolutionarily ancient BAH–PHD protein mediates Polycomb silencing , 2020, Proceedings of the National Academy of Sciences.

[38]  R. Schmitz,et al.  Histone variants in archaea and the evolution of combinatorial chromatin complexity , 2020, Proceedings of the National Academy of Sciences.

[39]  C. Ellison,et al.  3D genome evolution and reorganization in the Drosophila melanogaster species group , 2020, bioRxiv.

[40]  Z. Lewis,et al.  The histone variant H2A.Z is required to establish normal patterns of H3K27 methylation in Neurospora crassa , 2020, bioRxiv.

[41]  E. Stukenbrock,et al.  Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen , 2020, bioRxiv.

[42]  Yad Ghavi-Helm Functional consequences of chromosomal rearrangements on gene expression: not so deleterious after all? , 2020, Journal of molecular biology.

[43]  Prim B. Singh,et al.  On the relations of phase separation and Hi-C maps to epigenetics , 2020, Royal Society Open Science.

[44]  Boqiang Li,et al.  The Pattern and Function of DNA Methylation in Fungal Plant Pathogens , 2020, Microorganisms.

[45]  Jennifer E. Phillips-Cremins,et al.  On the existence and functionality of topologically associating domains , 2020, Nature Genetics.

[46]  Elizabeth T. Wiles,et al.  Evolutionarily ancient BAH-PHD protein mediates Polycomb silencing , 2019, bioRxiv.

[47]  Darcy A. B. Jones,et al.  A specific fungal transcription factor controls effector gene expression and orchestrates the establishment of the necrotrophic pathogen lifestyle on wheat , 2019, Scientific Reports.

[48]  M. Furlan-Magaril,et al.  In situ dissection of domain boundaries affect genome topology and gene transcription in Drosophila , 2019, Nature Communications.

[49]  Kyle M. Douglass,et al.  EZH2 oncogenic mutations drive epigenetic, transcriptional, and structural changes within chromatin domains , 2019, Nature Genetics.

[50]  J. Heitman,et al.  Centromere deletion in Cryptococcus deuterogattii leads to neocentromere formation and chromosome fusions , 2019, bioRxiv.

[51]  Robert J. Schmitz,et al.  Diversity of cytosine methylation across the fungal tree of life , 2019, Nature Ecology & Evolution.

[52]  T. Itoh,et al.  3D genomic architecture reveals that neocentromeres associate with heterochromatin regions , 2019, The Journal of cell biology.

[53]  R. Panstruga,et al.  The need for speed: compartmentalized genome evolution in filamentous phytopathogens. , 2018, Molecular plant pathology.

[54]  Haobin Wang,et al.  Nuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation , 2018, The Journal of Biological Chemistry.

[55]  E. Selker,et al.  ASH1-catalyzed H3K36 methylation drives gene repression and marks H3K27me2/3-competent chromatin , 2018, eLife.

[56]  V. Corces,et al.  Organizational principles of 3D genome architecture , 2018, Nature Reviews Genetics.

[57]  E. Stukenbrock,et al.  Destabilization of chromosome structure by histone H3 lysine 27 methylation , 2018, bioRxiv.

[58]  Lloyd M. Smith,et al.  EBS is a bivalent histone reader that regulates floral phase transition in Arabidopsis , 2018, Nature Genetics.

[59]  K. Sanyal,et al.  Five pillars of centromeric chromatin in fungal pathogens , 2018, PLoS pathogens.

[60]  S. Mundlos,et al.  Structural variation in the 3D genome , 2018, Nature Reviews Genetics.

[61]  S. Cesari,et al.  Multiple strategies for pathogen perception by plant immune receptors. , 2018, The New phytologist.

[62]  K. Rippe,et al.  Formation of Chromatin Subcompartments by Phase Separation. , 2018, Biophysical journal.

[63]  Xiangji Kong,et al.  The Fusarium graminearum Histone Acetyltransferases Are Important for Morphogenesis, DON Biosynthesis, and Pathogenicity , 2018, Front. Microbiol..

[64]  C. Sansam,et al.  A mechanism for epigenetic control of DNA replication , 2018, Genes & development.

[65]  Bram Henneman,et al.  Structure and function of archaeal histones , 2018, PLoS genetics.

[66]  S. Reissmann,et al.  The Biotrophic Development of Ustilago maydis Studied by RNA-Seq Analysis[OPEN] , 2018, Plant Cell.

[67]  S. Zhong,et al.  3D Chromatin Architecture of Large Plant Genomes Determined by Local A/B Compartments. , 2017, Molecular plant.

[68]  U. Güldener,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 , 2017, Genetics.

[69]  Michael F. Seidl,et al.  Transposable Elements Direct The Coevolution between Plants and Microbes. , 2017, Trends in genetics : TIG.

[70]  C. Cruaud,et al.  Different waves of effector genes with contrasted genomic location are expressed by Leptosphaeria maculans during cotyledon and stem colonization of oilseed rape. , 2017, Molecular plant pathology.

[71]  G. Schotta,et al.  Histone H4K20 tri‐methylation at late‐firing origins ensures timely heterochromatin replication , 2017, The EMBO journal.

[72]  Alma L. Burlingame,et al.  Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin , 2017, Nature.

[73]  Z. Lewis,et al.  Polycomb Group Systems in Fungi: New Models for Understanding Polycomb Repressive Complex 2. , 2017, Trends in genetics : TIG.

[74]  K. Rybak,et al.  A functionally conserved Zn2Cys6 binuclear cluster transcription factor class regulates necrotrophic effector gene expression and host‐specific virulence of two major Pleosporales fungal pathogens of wheat , 2017, Molecular plant pathology.

[75]  E. Selker,et al.  Normal chromosome conformation depends on subtelomeric facultative heterochromatin in Neurospora crassa , 2016, Proceedings of the National Academy of Sciences.

[76]  Kirti Prakash,et al.  Histone Code and Higher-Order Chromatin Folding: A Hypothesis , 2016, bioRxiv.

[77]  Michael F. Seidl,et al.  Chromatin Biology Impacts Adaptive Evolution of Filamentous Plant Pathogens , 2016, PLoS pathogens.

[78]  Jeroen S. Dickschat,et al.  Knock-down of the methyltransferase Kmt6 relieves H3K27me3 and results in induction of cryptic and otherwise silent secondary metabolite gene clusters in Fusarium fujikuroi. , 2016, Environmental microbiology.

[79]  Tao Chen,et al.  Histone H3 Lysine 9 Methyltransferase DIM5 Is Required for the Development and Virulence of Botrytis cinerea , 2016, Front. Microbiol..

[80]  S. Gasser,et al.  On TADs and LADs: Spatial Control Over Gene Expression. , 2016, Trends in genetics : TIG.

[81]  Michael F. Seidl,et al.  Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen , 2016, Genome research.

[82]  M. Dundr,et al.  Nuclear bodies: Built to boost , 2016, The Journal of cell biology.

[83]  E. Selker,et al.  Neurospora chromosomes are organized by blocks of importin alpha-dependent heterochromatin that are largely independent of H3K9me3 , 2016, Genome research.

[84]  M. Freitag The kinetochore interaction network (KIN) of ascomycetes , 2016, Mycologia.

[85]  U. Güldener,et al.  A Tale of Genome Compartmentalization: The Evolution of Virulence Clusters in Smut Fungi , 2016, Genome biology and evolution.

[86]  S. Raffaele,et al.  The two-speed genomes of filamentous pathogens: waltz with plants. , 2015, Current opinion in genetics & development.

[87]  Robert J. Schmitz,et al.  Genome-wide redistribution of H3K27me3 is linked to genotoxic stress and defective growth , 2015, Proceedings of the National Academy of Sciences.

[88]  E. Stukenbrock,et al.  Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes , 2015, Epigenetics & Chromatin.

[89]  Michael F. Seidl,et al.  Single-Molecule Real-Time Sequencing Combined with Optical Mapping Yields Completely Finished Fungal Genome , 2015, mBio.

[90]  B. Thomma,et al.  Understanding plant immunity as a surveillance system to detect invasion. , 2015, Annual review of phytopathology.

[91]  H. Ohkura Meiosis: an overview of key differences from mitosis. , 2015, Cold Spring Harbor perspectives in biology.

[92]  John J. Wyrick,et al.  The amino-terminal tails of histones H2A and H3 coordinate efficient base excision repair, DNA damage signaling and postreplication repair in Saccharomyces cerevisiae , 2015, Nucleic acids research.

[93]  E. Stukenbrock,et al.  Chromatin analyses of Zymoseptoria tritici: Methods for chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq). , 2015, Fungal genetics and biology : FG & B.

[94]  Neva C. Durand,et al.  A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping , 2014, Cell.

[95]  J. Ruiz-Herrera,et al.  The UmGcn5 gene encoding histone acetyltransferase from Ustilago maydis is involved in dimorphism and virulence. , 2014, Fungal genetics and biology : FG & B.

[96]  M. Pellegrini,et al.  Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content , 2014, Genome Biology.

[97]  M. Busman,et al.  Fusarium verticillioides SGE1 is required for full virulence and regulates expression of protein effector and secondary metabolite biosynthetic genes. , 2014, Molecular plant-microbe interactions : MPMI.

[98]  Z. Lewis,et al.  Heterochromatin Controls γH2A Localization in Neurospora crassa , 2014, Eukaryotic Cell.

[99]  B. Scott,et al.  Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte–plant symbiosis , 2014, Molecular microbiology.

[100]  Giacomo Cavalli,et al.  Polycomb silencing: from linear chromatin domains to 3D chromosome folding. , 2014, Current opinion in genetics & development.

[101]  M. Freitag,et al.  Epigenetic Control of Effector Gene Expression in the Plant Pathogenic Fungus Leptosphaeria maculans , 2014, PLoS genetics.

[102]  Sven Bilke,et al.  A chromatin structure‐based model accurately predicts DNA replication timing in human cells , 2014, Molecular systems biology.

[103]  M. Freitag,et al.  The Fusarium graminearum Histone H3 K27 Methyltransferase KMT6 Regulates Development and Expression of Secondary Metabolite Gene Clusters , 2013, PLoS genetics.

[104]  B. Thomma,et al.  Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen , 2013, Genome research.

[105]  D. MacAlpine,et al.  Chromatin and DNA replication. , 2013, Cold Spring Harbor perspectives in biology.

[106]  Yangrae Cho,et al.  Fungal-specific transcription factor AbPf2 activates pathogenicity in Alternaria brassicicola. , 2013, The Plant journal : for cell and molecular biology.

[107]  C. Boerkoel,et al.  The Role of Nuclear Bodies in Gene Expression and Disease , 2013, Biology.

[108]  J. Stajich,et al.  Regional control of histone H3 lysine 27 methylation in Neurospora , 2013, Proceedings of the National Academy of Sciences.

[109]  Stephen H. Hughes,et al.  H3K4me3 Interactions with TAF3 Regulate Preinitiation Complex Assembly and Selective Gene Activation , 2013, Cell.

[110]  B. Thomma,et al.  Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. , 2013, Molecular plant-microbe interactions : MPMI.

[111]  Jacques Côté,et al.  Perceiving the epigenetic landscape through histone readers , 2012, Nature Structural &Molecular Biology.

[112]  Pamela A Silver,et al.  Designing biological compartmentalization. , 2012, Trends in cell biology.

[113]  N. Fedoroff Transposable Elements, Epigenetics, and Genome Evolution , 2012 .

[114]  M. Freitag,et al.  Centromeres of filamentous fungi , 2012, Chromosome Research.

[115]  S. Raffaele,et al.  Genome evolution in filamentous plant pathogens: why bigger can be better , 2012, Nature Reviews Microbiology.

[116]  W. Jonkers,et al.  The Wor1-like Protein Fgp1 Regulates Pathogenicity, Toxin Synthesis and Reproduction in the Phytopathogenic Fungus Fusarium graminearum , 2012, PLoS pathogens.

[117]  Jesse R. Dixon,et al.  Topological Domains in Mammalian Genomes Identified by Analysis of Chromatin Interactions , 2012, Nature.

[118]  Jiayu Wen,et al.  Prediction of RNA Polymerase II recruitment, elongation and stalling from histone modification data , 2011, BMC Genomics.

[119]  G. Bourque,et al.  CpG Deamination Creates Transcription Factor–Binding Sites with High Efficiency , 2011, Genome biology and evolution.

[120]  K. Sanyal,et al.  Diversity in Requirement of Genetic and Epigenetic Factors for Centromere Function in Fungi , 2011, Eukaryotic Cell.

[121]  Corella S. Casas-Delucchi,et al.  Histone hypoacetylation is required to maintain late replication timing of constitutive heterochromatin , 2011, Nucleic acids research.

[122]  P. Tudzynski,et al.  The Botrytis cinerea Reg1 protein, a putative transcriptional regulator, is required for pathogenicity, conidiogenesis, and the production of secondary metabolites. , 2011, Molecular plant-microbe interactions : MPMI.

[123]  Bin Zhang,et al.  Biogenesis and function of nuclear bodies. , 2011, Trends in genetics : TIG.

[124]  Christina A. Cuomo,et al.  Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens , 2011, PLoS pathogens.

[125]  C. Sullivan,et al.  Heterochromatin Is Required for Normal Distribution of Neurospora crassa CenH3 , 2011, Molecular and Cellular Biology.

[126]  Bing Li,et al.  Readers of histone modifications , 2011, Cell Research.

[127]  Andrew J. Bannister,et al.  Regulation of chromatin by histone modifications , 2011, Cell Research.

[128]  Rhys A. Farrer,et al.  Genome Evolution Following Host Jumps in the Irish Potato Famine Pathogen Lineage , 2010, Science.

[129]  Michael B. Stadler,et al.  Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome. , 2010, Genome research.

[130]  C. Vieira,et al.  Jumping genes and epigenetics: Towards new species. , 2010, Gene.

[131]  E. Manders,et al.  The Nuclear Protein Sge1 of Fusarium oxysporum Is Required for Parasitic Growth , 2009, PLoS pathogens.

[132]  Jonathan D. G. Jones,et al.  Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans , 2009, Nature.

[133]  T. Boller,et al.  A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. , 2009, Annual review of plant biology.

[134]  P. Muñoz,et al.  Chromatin dynamics coupled to DNA repair , 2009, Epigenetics.

[135]  J. Palmer,et al.  H3K9 Methylation Regulates Growth and Development in Aspergillus fumigatus , 2008, Eukaryotic Cell.

[136]  W. J. Dickinson,et al.  A genome-wide view of the spectrum of spontaneous mutations in yeast , 2008, Proceedings of the National Academy of Sciences.

[137]  Marco Foiani,et al.  Regulation of DNA repair throughout the cell cycle , 2008, Nature Reviews Molecular Cell Biology.

[138]  C. Scazzocchio,et al.  Nucleosome Positioning and Histone H3 Acetylation Are Independent Processes in the Aspergillus nidulans prnD-prnB Bidirectional Promoter , 2008, Eukaryotic Cell.

[139]  E. Seto,et al.  The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men , 2008, Nature Reviews Molecular Cell Biology.

[140]  Matthias Mann,et al.  Selective Anchoring of TFIID to Nucleosomes by Trimethylation of Histone H3 Lysine 4 , 2007, Cell.

[141]  Jerry L. Workman,et al.  Histone acetyltransferase complexes: one size doesn't fit all , 2007, Nature Reviews Molecular Cell Biology.

[142]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[143]  Anjanabha Saha,et al.  ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression , 2006, Nature.

[144]  B. Thomma,et al.  Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. , 2006, Molecular plant pathology.

[145]  D. Reinberg,et al.  Histone variants meet their match , 2005, Nature Reviews Molecular Cell Biology.

[146]  B. Calvi,et al.  Chromatin regulates origin activity in Drosophila follicle cells , 2004, Nature.

[147]  Saeed Tavazoie,et al.  Mapping Global Histone Acetylation Patterns to Gene Expression , 2004, Cell.

[148]  E. Selker,et al.  HP1 is essential for DNA methylation in neurospora. , 2004, Molecular cell.

[149]  D. Angelov,et al.  The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. , 2003, Molecular cell.

[150]  J. Huberman,et al.  Early-replicating heterochromatin. , 2003, Genes & development.

[151]  J. Dekker,et al.  Capturing Chromosome Conformation , 2002, Science.

[152]  E. Selker,et al.  A histone H3 methyltransferase controls DNA methylation in Neurospora crassa , 2001, Nature.

[153]  E. Selker,et al.  dim‐2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora , 2001, The EMBO journal.

[154]  K. J. Fryxell,et al.  Cytosine deamination plays a primary role in the evolution of mammalian isochores. , 2000, Molecular biology and evolution.

[155]  J. T. Kadonaga Eukaryotic Transcription: An Interlaced Network of Transcription Factors and Chromatin-Modifying Machines , 1998, Cell.

[156]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[157]  J. Widom,et al.  Nucleosome packaging and nucleosome positioning of genomic DNA. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[158]  Alan P. Wolffe,et al.  A positive role for histone acetylation in transcription factor access to nucleosomal DNA , 1993, Cell.

[159]  Michael F. Seidl,et al.  Local rather than global H3K27me3 dynamics associates 1 with differential gene expression in Verticillium dahliae 2 , 2021 .

[160]  C. Carlberg,et al.  Histone Modifications , 2019, Human Epigenetics: How Science Works.

[161]  T. Rouxel,et al.  Evolutionary and Adaptive Role of Transposable Elements in Fungal Genomes , 2014 .

[162]  R. Meyers Epigenetic regulation and epigenomics , 2012 .

[163]  S. Grewal,et al.  Heterochromatin revisited , 2007, Nature Reviews Genetics.

[164]  B. Alberts,et al.  How Genomes Evolve , 2002 .

[165]  R Holliday,et al.  DNA methylation and mutation. , 1993, Mutation research.