2,706
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Comparative analysis of genome-wide DNA methylation in Neurospora

, , , & ORCID Icon
Pages 972-987 | Received 20 Sep 2019, Accepted 27 Feb 2020, Published online: 31 Mar 2020

References

  • Feng SH, Cokus SJ, Zhang XY, et al. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA. 2010;107:8689–8694.
  • Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet. 2008;9:465.
  • Zemach A, McDaniel IE, Silva P, et al. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science. 2010;328:916–919.
  • Heard E, Disteche CM. Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev. 2006;20:1848–1867.
  • Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001;293:1068–1070.
  • Lister R, O’Malley RC, Tonti-Filippini J, et al. Highly integrated single-base resolution maps of the epigenome in arabidopsis. Cell. 2008;133:523–536.
  • Lister R, Pelizzola M, Dowen RH, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315–322.
  • Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2:21–32.
  • Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8:272–285.
  • Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11:204.
  • Wang X, Wheeler D, Avery A, et al. Function and evolution of DNA methylation in nasonia vitripennis. PLoS Genet. 2013;9:e1003872.
  • Zilberman D, Gehring M, Tran RK, et al. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet. 2007;39:61–69.
  • Doolittle WF, Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980;284:601–603.
  • Lonnig WE, Saedler H. Chromosome rearrangements and transposable elements. Annu Rev Genet. 2002;36:389–410.
  • Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem. 2005;74:481–514.
  • Selker EU. Genome defense and DNA methylation in Neurospora. Cold Spring Harb Sym. 2004;69: 119–124.
  • Zhang X. The epigenetic landscape of plants. Science. 2008;320:482–492.
  • Lippman Z, Gendrel AV, Black M, et al. Role of transposable elements in heterochromatin and epigenetic control. Nature. 2004;430:471–476.
  • Borgognone A, Castanera R, Morselli M, et al. Transposon-associated epigenetic silencing during Pleurotus ostreatus life cycle. DNA Res. 2018;25:451–464.
  • Choi JY, Purugganan MD. Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice. Mol Biol Evol. 2018;35:365–382.
  • Eichten SR, Ellis NA, Makarevitch I, et al. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet. 2012;8. DOI:10.1371/journal.pgen.1003127.
  • Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009;19:1419–1428.
  • Lee YCG. The role of piRNA-mediated epigenetic silencing in the population dynamics of transposable elements in Drosophila melanogaster. PLoS Genet. 2015;11. DOI:10.1371/journal.pgen.1005269
  • Lee YCG, Karpen GH. Pervasive epigenetic effects of Drosophila euchromatic transposable elements impact their evolution. Elife. 2017;6. DOI:10.7554/eLife.25762
  • Li E, Zhang Y. DNA methylation in mammals. Csh Perspect Biol. 2014; 6a019133.
  • Seymour DK, Koenig D, Hagmann J, et al. Evolution of DNA methylation patterns in the brassicaceae is driven by differences in genome organization. PLoS Genet. 2014;10:e1004785.
  • Legrand S, Caron T, Maumus F, et al. Differential retention of transposable element-derived sequences in outcrossing Arabidopsis genomes. Mob DNA. 2019;10:30.
  • Aramayo R, Selker EU. Neurospora crassa, a model system for epigenetics research. Csh Perspect Biol. 2013;5: a017921.
  • Rountree MR, Selker EU. DNA methylation and the formation of heterochromatin in Neurospora crassa. Heredity (Edinb). 2010;105:38.
  • Foss HM, Roberts CJ, Claeys KM, et al. Abnormal chromosome behavior in Neurospora mutants defective in DNA methylation. Science. 1993;262:1737.
  • Russell PJ, Rodland KD, Rachlin EM, et al. Differential DNA methylation during the vegetative life cycle of Neurospora crassa. J Bacteriol. 1987;169:2902.
  • Lewis ZA, Honda S, Khlafallah TK, et al. Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res. 2009;19:427–437.
  • Selker EU, Fritz DY, Singer MJ. Dense nonsymmetrical DNA methylation resulting from repeat-induced point mutation in Neurospora. Science. 1993;262:1724.
  • Tamaru H, Selker EU. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa.. Nature. 2001;414:277–283.
  • Tamaru H, Zhang X, McMillen D, et al. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet. 2003;34:75.
  • Montanini B, Chen P-Y, Morselli M, et al. Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content. Genome Biol. 2014;15:411.
  • Castanera R, López-Varas L, Borgognone A, et al. Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLoS Genet. 2016;12:e1006108.
  • Corcoran P, Anderson JL, Jacobson DJ, et al. Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma. Genome Res. 2016;26:486–498.
  • Corcoran P, Dettman JR, Sun Y, et al. A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system. Mol Phylogenet Evol. 2014;78:136–147.
  • Smith KM, Phatale PA, Sullivan CM, et al. Heterochromatin is required for normal distribution of Neurospora crassa CenH3. Mol Cell Biol. 2011;31:2528–2542.
  • Galagan JE, Calvo SE, Borkovich KA, et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature. 2003;422:859–868.
  • Singer MJ, Marcotte BA, Selker EU. DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol Cell Biol. 1995;15:5586.
  • Watters MK, Randall TA, Margolin BS, et al. Action of repeat-induced point mutation on both strands of a duplex and on tandem duplications of various sizes in Neurospora. Genetics. 1999;153:705–714.
  • Hollister JD, Smith LM, Guo YL, et al. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci USA. 2011;108:2322–2327.
  • Zanni V, Eymery A, Coiffet M, et al. Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters. Proc Natl Acad Sci USA. 2013;110:19842.
  • Jeon J, Choi J, Lee G-W, et al. Genome-wide profiling of DNA methylation provides insights into epigenetic regulation of fungal development in a plant pathogenic fungus, Magnaporthe oryzae. Sci Rep. 2015;5:8567.
  • Antequera F, Tamame M, Villanueva JR, et al. DNA methylation in the fungi. J Biol Chem. 1984;259:8033–8036.
  • Binz T, D’Mello N, Horgen PA. A comparison of DNA methylation levels in selected isolates of higher fungi. Mycologia. 1998;90:785–790.
  • Zhang ZB, Wen JW, Li JZ, et al. The evolution of genomic and epigenomic features in two Pleurotus fungi. Sci Rep. 2018;8:8313.
  • Li W, Wang Y, Zhu J, et al. Differential DNA methylation may contribute to temporal and spatial regulation of gene expression and the development of mycelia and conidia in entomopathogenic fungus Metarhizium robertsii. Fungal Biol-Uk. 2017;121:293–303.
  • Wang Y-L, Wang Z-X, Liu C, et al. Genome-wide analysis of DNA methylation in the sexual stage of the insect pathogenic fungus Cordyceps militaris. Fungal Biol-Uk. 2015;119:1246–1254.
  • Zeng Z, Wu J, Kovalchuk A, et al. Genome-wide DNA methylation and transcriptomic profiles in the lifestyle strategies and asexual development of the forest fungal pathogen Heterobasidion parviporum. Epigenetics. 2019;14:16–40.
  • Kinsey JA, Helber J. Isolation of a transposable element from Neurospora crassa. Proc Natl Acad Sci USA. 1989;86:1929–1933.
  • Freitag M, Williams RL, Kothe GO, et al. A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci USA. 2002;99:8802–8807.
  • Kouzminova E, Selker EU. dim-2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora. Embo J. 2001;20:4309–4323.
  • Tamaru H, Selker EU. Synthesis of signals for de novo DNA methylation in Neurospora crassa. Mol Cell Biol. 2003;23:2379–2394.
  • Bewick AJ, Hofmeister BT, Powers RA, et al. Diversity of cytosine methylation across the fungal tree of life. Nat Ecol Evol. 2019;3:479–490.
  • Wicker T, Sabot F, Hua-Van A, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8:973–982.
  • Kidwell MG, Lisch D. Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA. 1997;94:7704.
  • Venner S, Feschotte C, Biémont C. Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet. 2009;25:317–323.
  • Abrusán G, Krambeck H-J. Competition may determine the diversity of transposable elements. Theor Popul Biol. 2006;70:364–375.
  • Selker EU, Tountas NA, Cross SH, et al. The methylated component of the Neurospora crassa genome. Nature. 2003;422:893–897.
  • Irelan JT, Selker EU. Cytosine methylation associated with repeat-induced point mutation causes epigenetic gene silencing in Neurospora crassa. Genetics. 1997;146:509–523.
  • Miao VPW, Freitag M, Selker EU. Short TpA-rich segments of the ζ-η region induce DNA methylation in Neurospora crassa. J Mol Biol. 2000;300:249–273.
  • Lee YCG, Langley CH. Transposable elements in natural populations of Drosophila melanogaster. Philos T R Soc B. 2010;365: 1219–1228.
  • Menkis A, Bastiaans E, Jacobson DJ, et al. Phylogenetic and biological species diversity within the Neurospora tetrasperma complex. J Evol Biol. 2009;22:1923–1936.
  • Vogel HJ. A convenient growth medium for Neurospora (medium N). Microb Genet Bull. 1956;13:42–43.
  • Russo V, Sommer T, Chambers J. A modified Vogel’s medium for crossings, mating-type tests and the isolation of female-sterile mutants of Neurospora crassa. Fungal Genetics Reports. 1985;32: 10.
  • Ellison CE, Stajich JE, Jacobson DJ, et al. Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics. 2011;189:55–69.
  • Sun Y, Svedberg J, Hiltunen M, et al. Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma. Nat Commun. 2017;8:1140.
  • Svedberg J, Hosseini S, Chen J, et al. Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements. Nat Commun. 2018;9:4242.
  • Kurtz S, Phillippy A, Delcher AL, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5:R12.
  • Kersey PJ, Allen JE, Allot A, et al. Ensembl Genomes 2018: an integrated omics infrastructure for non-vertebrate species. Nucleic Acids Res. 2018;46:D802–D808.
  • Cantarel BL, Korf I, Robb SMC, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188–196.
  • Chen C, Huang H, Wu CH. Protein bioinformatics databases and resources. In: Wu CH, editor. Protein bioinformatics: from protein modifications and networks to proteomics. New York, New York, NY: Springer; 2017. p. 3–39. DOI:10.1007/978-1-4939-6783-4_1
  • Smit A, Hubley R, Green P. RepeatMasker open-4.0. 2013-2015.
  • Gioti A, Mushegian AA, Strandberg R, et al. Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements. Mol Biol Evol. 2012;29:3215–3226.
  • Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27:1571–1572.
  • Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012;9:357–U354.
  • Li H, Handsaker B, Wysoker A, et al. Project data processing, the sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079.
  • García-Alcalde F, Okonechnikov K, Carbonell J, et al. Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics. 2012;28:2678–2679.
  • Song Q, Decato B, Hong EE, et al. A reference methylome database and analysis pipeline to facilitate integrative and comparative epigenomics. PLOS One. 2013;8:e81148.
  • Schultz MD, Schmitz RJ, Ecker JR. ‘Leveling’ the playing field for analyses of single-base resolution DNA methylomes. Trends Genet. 2012;28:583–585.
  • Core Team R. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
  • Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842.
  • Hu Y, Yan C, Hsu C-H, et al. OmicCircos: A simple-to-use R package for the circular visualization of multidimensional omics data. Cancer Inform. 2014;13:CIN.S13495.
  • Ramírez F, Dündar F, Diehl S, et al. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 2014;42:W187–W191.
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics. 2014;30:2114–2120.
  • Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
  • Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140.
  • Chen Y, Lun A, Smyth G. From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline [version 2; referees: 5 approved]. F1000Res. 2016;5:1438.